Next Article in Journal
Fungal Aeroallergen Sensitization Patterns among Airway-Allergic Patients in Zagazig, Egypt
Next Article in Special Issue
Diversity and Distribution of Calonectria Species in Soils from Eucalyptus urophylla × E. grandis, Pinus massoniana, and Cunninghamia lanceolata Plantations in Four Provinces in Southern China
Previous Article in Journal
Fungal Whole-Genome Sequencing for Species Identification: From Test Development to Clinical Utilization
Previous Article in Special Issue
The Analysis of the Mycobiota in Plastic Polluted Soil Reveals a Reduction in Metabolic Ability
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes

by
Achala R. Rathnayaka
1,2,3,
K. W. Thilini Chethana
1,2,*,
Alan J. L. Phillips
4,
Jian-Kui Liu
5,
Milan C. Samarakoon
6,
E. B. Gareth Jones
7,
Samantha C. Karunarathna
8 and
Chang-Lin Zhao
9,*
1
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
2
Center of Excellence in Fungal Research, Mae Fah Luang University, Chiang Rai 57100, Thailand
3
Department of Plant Medicine, National Chiayi University, 300 Syuefu Road, Chiayi City 60004, Taiwan
4
Faculdade de Ciências, Biosystems and Integrative Sciences Institute (BioISI), Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal
5
School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China
6
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
7
Department of Botany and Microbiology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
8
Center for Yunnan Plateau Biological Resources Protection and Utilization, College of Biological Resource and Food Engineering, Qujing Normal University, Qujing 655011, China
9
Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming 650224, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2023, 9(2), 184; https://doi.org/10.3390/jof9020184
Submission received: 21 December 2022 / Revised: 25 January 2023 / Accepted: 26 January 2023 / Published: 29 January 2023
(This article belongs to the Special Issue Fungal Biodiversity and Ecology, 3rd Edition)

Abstract

:
Botryosphaeriales (Dothideomycetes, Ascomycota) occur in a wide range of habitats as endophytes, saprobes, and pathogens. The order Botryosphaeriales has not been subjected to evaluation since 2019 by Phillips and co-authors using phylogenetic and evolutionary analyses. Subsequently, many studies introduced novel taxa into the order and revised several families separately. In addition, no ancestral character studies have been conducted for this order. Therefore, in this study, we re-evaluated the character evolution and taxonomic placements of Botryosphaeriales species based on ancestral character evolution, divergence time estimation, and phylogenetic relationships, including all the novel taxa that have been introduced so far. Maximum likelihood, maximum parsimony, and Bayesian inference analyses were conducted on a combined LSU and ITS sequence alignment. Ancestral state reconstruction was carried out for conidial colour, septation, and nutritional mode. Divergence times estimates revealed that Botryosphaeriales originated around 109 Mya in the early epoch of the Cretaceous period. All six families in Botryosphaeriales evolved in the late epoch of the Cretaceous period (66–100 Mya), during which Angiosperms also appeared, rapidly diversified and became dominant on land. Families of Botryosphaeriales diversified during the Paleogene and Neogene periods in the Cenozoic era. The order comprises the families Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae and Saccharataceae. Furthermore, current study assessed two hypotheses; the first one being “All Botryosphaeriales species originated as endophytes and then switched into saprobes when their hosts died or into pathogens when their hosts were under stress”; the second hypothesis states that “There is a link between the conidial colour and nutritional mode in botryosphaerialean taxa”. Ancestral state reconstruction and nutritional mode analyses revealed a pathogenic/saprobic nutritional mode as the ancestral character. However, we could not provide strong evidence for the first hypothesis mainly due to the significantly low number of studies reporting the endophytic botryosphaerialean taxa. Results also showed that hyaline and aseptate conidia were ancestral characters in Botryosphaeriales and supported the relationship between conidial pigmentation and the pathogenicity of Botryosphaeriales species.

1. Introduction

1.1. Botryosphaeriales

Botryosphaeriales was introduced to accommodate Botryosphaeriaceae by Schoch et al. [1]. Following consecutive studies, the families Planistromellaceae [2], Phyllostictaceae [3], Aplosporellaceae, Melanopsaceae, Saccharataceae [4], Septorioideaceae [5], Endomelanconiopsisaceae, and Pseudofusicoccumaceae [6] were recognized in Botryosphaeriales. In a revision based on morphology and phylogeny, Phillips et al. [7] synonymized Endomelanconiopsisaceae under Botryosphaeriaceae. Pseudofusicoccumaceae and Septorioideaceae were also synonymized under Phyllostictaceae and Saccharataceae, respectively. Currently, six families are accepted in Botryosphaeriales, i.e., Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae, and Saccharataceae [7,8,9].
Botryosphaeriales is an order with a variety of lifestyles ranging from endophytes to pathogens and saprobes [10] on a wide range of monocotyledonous and dicotyledonous hosts [11] and lichens [12,13]. Most of the taxa in Botryosphaeriales are endophytes living in the healthy tissues of woody plants for extended periods [10]. Species of Botryosphaeria, Diplodia, Dothiorella, Lasiodiplodia, Neofusicoccum, Phyllosticta, Pseudofusicoccum and Saccharata include endophytes [8,10,14,15]. Some Botryosphaeriales species are important phytopathogens associated with canker diseases, with a worldwide distribution and a broad host range, causing severe ecological and economical damage [7]. Pathogenic species in Botryosphaeriales, such as quiescence pathogens (such as Botryosphaeria and Lasiodiplodia species) cause diseases following an initial stress factor, such as drought or infection by another weak pathogen [5,16]. As an example, water stress affects disease development of Lasiodiplodia theobromae and Sphaeropsis sapinea on Platanus occidentalis and Pinus resinosa, respectively [17].

1.2. Previous Revisions for the Families in Botryosphaeriales

Theissen and Sydow [18] introduced Botryosphaeriaceae to accommodate Botryosphaeria, Dibotryon and Phaeobotryon [7,19]. Botryosphaeriaceae species have a range of nutritional modes from saprobic to parasitic or endophytic [10,20,21,22,23,24,25,26,27]. Members of this family are cosmopolitan in distribution and occur on a wide range of monocotyledonous and dicotyledonous hosts: on woody branches, leaves, stems and culms of grasses, and on twigs and in the thalli of lichens [12,21,28,29,30]. Liu et al. [11] accepted 29 genera in Botryosphaeriaceae based on morphology and molecular data. Phillips et al. [19] provided detailed descriptions and keys for 17 genera in Botryosphaeriaceae. Burgess et al. [31] and Garcia et al. [32] included 24 genera in Botryosphaeriaceae based on morpho-molecular data. However, Dissanayake et al. [33] mentioned that this family consists of 22 genera. This is the largest family in Botryosphaeriales [8,34]. Nearly 280 species have been described in Botryosphaeriaceae based on DNA sequence data [35].
Aplosporellaceae was introduced by Slippers et al. [4] to accommodate Aplosporella and Bagnisiella. Aplosporella are asexual morphs, while Bagnisiella species are known through their sexual morphs [36]. Sharma et al. [37] introduced Alanomyces in this family, which currently consist of two genera: Aplosporella and Alanomyces [34]. Melanopsaceae was introduced with Melanops as the type genus [4] and remains the only genus in the family [34].
Wikee et al. [3] reinstated Phyllostictaceae as a separate family in Botryosphaeriales to accommodate Phyllosticta, which consists of Phyllosticta and Pseudofusicoccum [34]. Phyllosticta species are mostly endophytes, but several are plant pathogens that cause leaf spots in a broad range of hosts worldwide [38,39,40,41,42]. Barr [43] introduced Planistromellaceae, which currently comprises two genera, namely, Kellermania and Umthunziomyces [33]. Saccharataceae is another family in Botryosphaeriales introduced by Slippers et al. [4] and consists of Pileospora, Saccharata and Septorioides [33].

1.3. Morphologies of Botryosphaerialean Taxa

Morphological characters vary between families in this order. Uni-loculate and multi-loculate ascostromata can be found in Botryosphaeriales (Figure 1). Aplosporellaceae, Melanopsaceae and Planistromellaceae are characterized by multiloculate ascostromata, while Botryosphaeriaceae, Phyllostictaceae and Saccharataceae have uni-loculate ascostromata [7]. In Saccharataceae and Phyllostictaceae, solitary, uni-loculate ascostromata have been recorded. In Botryosphaeriaceae, uni-loculate ascostromata are mostly solitary, but in some genera, such as Botryosphaeria, Diplodia and Neofusicoccum, they can be aggregated, which give the impression of being multi-loculate [7].
Ascospores and conidia in Botryosphaeriales have a wide range of morphologies, such as pigmented or hyaline, septate or aseptate and the presence or absence of a mucilaginous sheath (Table 1, Figure 2). Botryosphaeriaceae species have a wide range of conidial morphologies, such as fusiform to ovoid or elliptical, fusicoccum-like, hyaline, aseptate and thin-walled. Hyaline and, aseptate conidia become one or two septate and some species become pale brown before germination (Diplodia corticola, D. cupressi and D. mutila) [19]. Thick-walled and hyaline or brown diplodia-like conidia also occur in Botryosphaeriaceae. They can be aseptate, one-septate or even two- or multi-septate and have ovoid conidia with broadly rounded ends [19]. In Diplodia and Lasiodiplodia, conidia can remain hyaline for a long time and become brown and one-septate only after they are discharged from the conidiomata [19].
The mucilaginous sheath is one morphological character used to separate the families in Botryosphaeriales. Ascospores with mucilaginous sheath and gelatinous caps have been recorded in Melanopsaceae and Phyllostictaceae, respectively [7]. Mature ascospores of some species such as Botryosphaeria agaves and Melanops tulasnei, and immature ascospores of Phaeobotryon cercidis, have a mucilaginous sheath [4,7,11]. Neodeightonia palmicola has wing-like appendages when mounted in water. However, these wing-like appendages are not observed when mounted in 100% lactic acid (Figure 2i,j). Phillips et al. [7] suggested that these wing-like structures are a type of membrane surrounding the ascospores that enlarge and swell when water is absorbed [7].
Spore morphology influences survival in the environment [44]. Spore wall thickness and pigmentation protect spores from extreme conditions, such as heat, microbial attack and UV radiation [44,45]. Pigmentation of conidia is due to the melaninization of the conidial wall or the deposition of oxidized polymers of phenolic compounds [46]. Mainly three pigments (carotenoids, melanin and mycosporines) occur in fungi, and they act as antioxidants and reduce the damage from UV exposure [45]. Melanin can be found in pathogenic, as well as in saprobic taxa, and contributes to survival under harsh environmental conditions [47]. However, melanin production has more of an impact on pathogens because it is directly linked with virulence and pathogenicity [47,48].

1.4. Ancestral State Reconstructions for Fungi

There have been relatively few studies on ancestral state reconstructions in fungi to determine character evolution [4,51,52,53,54]. For more than two decades, character evolution has been highly contentious in lichen systematics [51]. Ekman et al. [51] studied the evolution of the ascus in Lecanorales using ancestral state reconstruction. Slippers et al. [4] performed ancestral state reconstructions for selected characters in Botryosphaeriales, such as ascospore colour, the presence or absence of ascospore septa, conidial colour, the presence or absence of conidial septa and presence or absence of a mucus sheath. However, they did not consider all the species of Botryosphaeriales. No studies have been conducted using ancestral state reconstruction or nutritional mode evolution with all the families or genera in Botryosphaeriales.

1.5. Objectives of the Current Study

This study aims to provide an updated phylogenetic tree for Botryosphaeriales using LSU and ITS sequence data (for ordinal level). Divergence time estimates were performed using the updated phylogeny of Botryosphaeriales. Furthermore, ancestral state reconstruction was performed for selected characters, i.e., conidial colour and septation and nutritional mode in Botryosphaeriales. Two hypotheses were assessed in the current study. The first hypothesis assessed was that “All Botryosphaeriales species originated as endophytes and then switched into saprobes when their hosts died or into pathogens when their hosts were under stress”. The second hypothesis tested was that “There is a link between conidial colour and nutritional mode in botryosphaerialean taxa”. Both hypotheses were tested based on the results from ancestral state reconstructions.

2. Materials and Methods

2.1. Data Collection and Analyses

Sequences were obtained from the GenBank for taxa reported in the recently published data on Botryosphaeriales species (Table S1) [7,8,11]. All the reported nutritional modes of each Botryosphaeriales species were considered for the ancestral state reconstruction analysis of nutritional mode. For other analyses, i.e., maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference (BI) and character analysis, one or two strains of each taxon were used. The tree file resulting from the evolution analysis was used for ancestral state reconstructions. Sequences of each locus were aligned with MAFFT v. 7 [55] and edited in BioEdit v. 7.0.9 [56] when necessary. Phylogenetic analyses were performed using ML, MP and BI as detailed in Dissanayake et al. [57]. The most suitable models for the ML and BI analyses were estimated using MrModeltest v. 2.3 [58] under AIC (Akaike Information Criterion) implemented in PAUP v. 4.0b10. The GTR+I+G model was determined to be the most suitable model for both LSU and ITS gene regions.
The ML analyses were conducted with RAxML-HPC2 on XSEDE v. 8.2.10 [59] in the CIPRES Science Gateway platform [60] using a GTR+I+G substitution model with 1000 bootstrap replicates. Bayesian inference was performed using MrBayes v. 3.2.6 (GTR+I+G model) [61]. Six simultaneous Markov Chain Monte Carlo analyses were run for 3,000,000 generations. The trees were sampled at every 100th generation. The first 10% of trees were discarded and the remaining 90% were used to calculate the posterior probabilities (PP) in the majority rule consensus tree. PAUP v. 4.0b10 [62] was used to perform the MP analysis for the combined dataset. A heuristic search option with 1000 random replicates and the tree bisection-reconnection (TBR) branch-swapping algorithm was used in the MP analysis. MaxTrees were set to 1000, branches of zero length were collapsed, and all multiple parsimonious trees were saved. Descriptive tree statistics for parsimony—tree length (TL), consistency index (CI), retention index (RI), relative consistency index (RC) and homoplasy index (HI)—were calculated for trees generated under different optimality criteria. Phylograms were visualized with the FigTree v. 1.4.0 program [63] and reorganized in Microsoft PowerPoint (2010). The final alignment and tree were deposited in TreeBASE under the submission ID: 28667 (http://www.treebase.org; accessed on 20 August 2021).

2.2. Molecular Clock Analysis

Divergence times were estimated using BEAST 1.8.4 [64]. The XML input file was prepared using BEAUTI v. 1.8.4. The substitution model, clock model and tree prior were set as linked. The GTR+I+G model was used as the nucleotide substitution model. An uncorrelated relaxed clock model [65] with the log-normal distribution rates was used for the analysis. Yule speciation process birth rate was used for the tree prior starting from a randomly generated tree. The crown age of Botryosphaeriales was set as 110 Mya (SD = 5 Mya) [7].
BEAST analyses were run for 60 million generations. Log parameters and trees were sampled every 10,000th generation. Tracer v. 1.6 [66] was used to check that effective sample sizes (ESS) were greater than 200. The first 10% of the trees were discarded and the remaining 5,400 trees were used to generate the maximum clade credibility (MCC) tree using LogCombiner v1.8.0 and TreeAnnotator v1.8.0. The resulting trees were viewed with FigTree v.1.4.0 [63] and edited in Microsoft PowerPoint (2010).

2.3. Ancestral State Reconstructions

Bayesian Binary MCMC in RASP 3.2 (Reconstruct Ancestral State in Phylogenies) [67,68] was used for the ancestral state reconstructions for conidial colour (hyaline or pigmented), conidial septation (septate or aseptate) and nutritional modes (saprobes, pathogens or endophytes). The evolution tree was generated in BEAST 1.8.4 [64] using the parameters given under the molecular clock analysis. Dothideomycetes crown group was calibrated using the secondary calibration data (normal distribution, mean = 290, SD = 30, providing a 95% credibility interval of 339 Mya) [69]. Botryosphaeriales crown group was calibrated using the secondary calibration data (normal distribution, mean = 110, SD = 5, providing a 95% credibility interval of 118 Mya) [7].
BEAST analyses were run for 100 million generations. Log parameters and trees were sampled at every 10,000th generation. MCC tree was generated by discarding the first 10% of the trees (1000 trees). The tree file resulting from the evolution analysis was exported to RASP 3.2. Each terminal in the tree was coded according to Table 2. Bayesian Binary MCMC trees were constructed using the following settings: 50,000 generations sampled every 100 generations, 10 chains and 0.1 temperature. State frequencies and among-site rate variation were set as Estimated (F81) and Gamma (+G), respectively. The analysis was applied only to Botryosphaeriales species and the character matrix used for this analysis is provided in Table S1. Two hypotheses were assessed as given below:
Hypothesis 1. 
All Botryosphaeriales species originated as endophytes and then switched into saprobes when their hosts died or into pathogens when their hosts were under stress.
Hypothesis 2. 
There is a link between the conidial colour and nutritional mode in botryosphaerialean taxa.

3. Results and Discussion

3.1. Phylogenetic Analyses

We re-evaluated the phylogenetic relationships within families of Botryosphaeriales based on LSU and ITS sequence data. In our preliminary phylogenetic analyses, we used sequence data from LSU, ITS and tef1 gene regions. Based on the tef1 resolution, Pseudofusicoccum and Phyllosticta formed separate groups within Phyllostictaceae, while Saccharataceae did not form a well-separated clade. Therefore, our final phylogenetic analyses were performed based on LSU and ITS sequence data.
The combined dataset consisted of 306 strains, representing botryosphaerialean taxa (Aplosporellaceae = 14, Botryosphaeriaceae = 236, Melanopsaceae = 4, Phyllostictaceae = 19, Planistromellaceae = 16, Saccharataceae = 17) and two outgroup taxa, Helicosporium guianense (CBS 269.52) and Helicomyces roseus (CBS 283.51) from Tubeufiaceae. The aligned dataset comprised 1452 characters including gaps (LSU = 880, ITS = 572). The best scoring RaxML tree with a final likelihood value of −19,919.245301 is shown in Figure 3. The matrix had 745 distinct alignment patterns with 25.42% undetermined characters or gaps. Estimated base frequencies were obtained as follows: A = 0.240022, C = 0.246955, G = 0.283975, T = 0.229048; substitution rates: AC = 1.641167, AG = 3.230258, AT = 1.788585, CG = 1.459944, CT = 7.210110, GT = 1.000000; gamma distribution shape parameter: α = 0.256314.
In the MP analysis, 775 characters were constant; 173 variable characters were parsimony-uninformative and 740 (37.28 %) characters were parsimony-informative. The most parsimonious tree resulted in the following parameters: TL = 6681, CI = 0.261, RI = 0.825, RC = 0.216, HI = 0.739 (for individual loci, parameters were obtained as follows: LSU, TL = 882, CI = 0.385, RI = 0.866, RC = 0.334, HI = 0.615; and ITS, TL = 2303, CI = 0.283, RI = 0.853, RC = 0.241, HI = 0.717). The average standard deviation of split frequencies was 0.001 after 3,000,000 generations. In the phylogenetic analyses, Aplosporellaceae, Melanopsaceae, Planistromellaceae and Saccharataceae segregated with strong bootstrap support values while, Botryosphaeriaceae and Phyllostictaceae showed moderate bootstrap support (Figure 3).
Phillips et al. [7] also constructed an ML tree for Botryosphaeriales using ITS and LSU sequences. However, except for Botryosphaeriaceae and Phyllostictaceae, the arrangement of Aplosporellaceae, Melanopsaceae, Planistromellaceae and Saccharataceae in the phylogenetic tree is different from this study. Phillips et al. [7] included 100 strains belonging to 28 genera in Botryosphaeriales in their analyses, while 306 Botryosphaeriales strains in 32 genera were used in our study. Even though we used the same loci as Phillips et al. [7], the sequence alignment was affected by the population size of the samples. This could account for the topological differences in the ML trees of the two studies.

3.2. Divergence Times

The topology of the MCC tree (Figure 4) resulting from the evolutionary analysis was similar to the topologies of ML, BI and MP trees. Based on evolutionary analysis, all six families were established during the Cretaceous period. Botryosphaeriaceae and Phyllostictaceae diversified during the Cretaceous period, while the remaining four families diversified during the Paleogene and Neogene periods in the Cenozoic era (0–66 Mya). The crown and stem ages for each family are tabulated in Table 3.
Previously, several studies were conducted to perform the divergence time estimations for Botryosphaeriales [4,7,70]. The number of taxa, gene regions and calibration points they used and the resulting crown and stem ages are given in Table 4.
Previous studies of Slippers et al. [4] and Liu et al. [71] revealed that Botryosphaeriales originated 103 (45–188) Mya. Liu et al. [70] reported the crown age of this order as 114 (73–166) Mya, while Phillips et al. [7] considered it to be at 110 Mya. In our analysis, we used 110 Mya to calibrate Botryosphaeriales. According to results of our analysis, Botryosphaeriales originated at 109 (99–119) Mya (Figure 4). Generally, the diversification of Botryosphaeriales may have occurred during the Cretaceous period associated with a rapid diversification of angiosperms (flowering plants). Liu et al. [70] suggested that orders of Dothideomycetes evolved within 100–220 Mya (crown age) and according to our study, Botryosphaeriales evolved within this range. The evolution of families in Botryosphaeriales is illustrated in Figure 5.
Slippers et al. [4] used SSU, LSU, ITS, tef1, β-tubulin and mtSSU gene regions for the molecular clock dating analysis of Botryosphaeriales, while Liu et al. [70] used LSU, SSU, tef1 and rpb2 for their analysis (Table 4). However, Liu et al. [70] performed their analysis for Dothideomycetes and used both secondary data and fossil data for calibrations. In both studies, most of the crown and stem ages are relatively lower than Phillips et al. [7] and this study (Table 4).
In Phillips et al. [7] and this study, the same gene regions and same calibration points were used to perform the divergence time estimation for Botryosphaeriales with a different number of taxa. Similar results are shown for crown age and stem age in both studies. However, there were slight differences (Table 4). Therefore, further studies are required to investigate how the number of taxa effect crown and stem ages in divergence time estimation.
Previously, Pseudofusicoccum was placed in Botryosphaeriaceae [4]. Subsequently, Yang et al. [6] showed that Pseudofusicoccum forms a separate clade at the base of the family Botryosphaeriaceae and suggested it as a separate family in Botryosphaeriales. Phillips et al. [7] accepted Pseudofusicoccum in Phyllostictaceae with support from the morphology of asexual morphs. The ML and MCC trees (Figure 3 and Figure 4) obtained in this study also show that Pseudofusicoccum group into Phyllostictaceae as in Phillips et al. [7]. Therefore, this study accepts Pseudofusicoccum as one of the genera in Phyllostictaceae. Liu et al. [70] suggested that families should have evolved between 20–100 Mya (crown age) in general. According to our study, all six families in Botryosphaeriales have evolved within this time frame (Table 3). Thus, our results support the establishment of the order Botryosphaeriales and accept Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae and Saccharataceae as families in this order.

3.3. Ancestral State Reconstructions

In ancestral state reconstructions, morphological or ecological data are mapped on molecular phylogenetic information generated from ML, MP and BI approaches [51]. Ancestral state reconstructions for conidial colour and septation, and nutritional mode evolution in botryosphaerialean taxa used the evolution tree results from BEAST 1.8.4 [64] under the Bayesian Binary MCMC method in RASP software (Figure 6) [67,68]. Three different nutritional modes were considered, namely endophytic, pathogenic and saprobic to assess the evolution of nutritional mode analysis. Some botryosphaerialean taxa are hemibiotrophic (Botryosphaeria dothidea), while some are necrotrophic (Phaeobotryon negundinis). Therefore, we included hemibiotrophic and necrotrophic modes under the pathogenic mode. Two hypotheses were tested in the current study as given in the methodology.

3.3.1. Ancestral State Reconstructions on Nutritional Modes of Botryosphaeriales Taxa

This analysis was conducted to assess the hypothesis that “All Botryosphaeriales species originated as endophytes and then switched into saprobes when their hosts died or into pathogens when their hosts were under stress”. This analysis is based mainly on the results of previous studies (Table S1). The endophytic nutritional mode in Ascomycota originated around 590–467 Mya in the stem lineage of Pezizomycotina, and many lineages show an endophytic ancestral character [72,73]. Based on our analysis, Dothideomycetes evolved with an endophytic ancestral nutritional mode around 250 Mya. They switched from endophytic to saprobic around 230 Mya. The supercontinent drift began in the Paleozoic (541–251 Mya), followed by the disintegration of the Pangea plate in the Middle Jurassic (176–161 Mya) [74]. These events resulted in the formation of continental amalgamation in the early Cretaceous, and plants were widely spread during this period. The interaction between plants and fungi facilitates the fungal colonization on land plants and their ability to adapt to different environmental conditions [75,76]. This may influence the Dothideomycetes to switch their nutritional mode from endophytes to saprobic during this period. Promputtha et al. [77] stated that many endophytes have the capacity to degrade cellulose and lignin. Therefore, they became part of the decomposer community by switching into saprobes, increasing saprobic diversity and decomposition rates [78].
This study revealed that most of the botryosphaerialean taxa were pathogens (46%) and few were recorded as endophytes (26%) (Figure 6). Among the 306 botryosphaerialean taxa included in the current study, 94 taxa were recorded exclusively as pathogens (31%), while 68 and 32 taxa were recorded exclusively as saprobes (22%) and endophytes (10%), respectively (Figure 6). Results of this study indicate that a pathogenic/saprobic ancestral nutritional mode for Botryosphaeriales evolved at around 109 Mya, which was derived from a pathogenic/endophytic ancestor around 136 Mya. Later, this pathogenic/saprobic ancestral nutritional mode diversified into endophytic/pathogenic/saprobic at 100 Mya at the late epoch of the Cretaceous period. The results of this analysis could not provide support for our hypothesis, which indicates the endophytic mode to be the ancestral nutritional mode. These results can be influenced by the fact that most of the botryosphaerialean taxa recorded and used in this study are pathogens and saprobes (Table S1), which will be discussed further.
Endophytic species were recorded from all the families of Botryosphaeriales, but the number of studies is very low compared to the saprobic and pathogenic (Table S1). The unbalanced taxon sampling for the analysis may exhibit a bias towards the pathogenic and saprobic modes. Another reason may be that for most of the species in this order, it is very common to be isolated as a pathogen or a saprobe. This is because pathogenic is the form where they become obvious, and researchers have focused their efforts on studies at this stage for economic reasons. Therefore, we do not have evidence to identify their initial nutritional mode and whether they experience nutritional mode shifts during their life cycle. For example, Botryosphaeria dothidea has been commonly reported as a serious plant pathogen, and has also been isolated as an endophyte [10]. Therefore, studies are needed to check whether we can isolate a species as a pathogen and also as an endophyte from the same host at different times. Similar to the current study, where unbalanced taxon sampling exhibits a bias towards the pathogenic and saprobic modes, a study conducted on Pucciniomycotina has shown mycoparasitism as the ancestral nutritional mode, while the mycoparasitic mode seems to be the most widespread in Pucciniomycotina [79,80,81]. This demonstrates that the taxon sampling for the study and the family composition might influence the results of ancestral nutritional mode studies.
In addition, warm environmental conditions that existed in the early epoch of the Cretaceous period (145–100.5 Mya) might also influence the ancestral endophytic taxa to become saprobic. Therefore, this event of diversifying endophytic taxa to saprobic should have occurred at around 109 Mya. In a fossil study at the Deccan Intertrappean Beds of India, both saprobic and pathogenic fungi were recorded in the late Cretaceous (100.5–66 Ma) [82], providing evidence for the occurrence of saprobic and pathogenic fungi in the late Cretaceous period other than endophytes. These may be the reasons why Botryosphaeriales have a pathogenic/saprobic nutritional mode in their ancestors. However, it is difficult to identify the fungal endophytes in fossil materials because it is hard to determine whether the host was alive and functioning or was going through senescence or decay at the time of colonization [83,84].
A study conducted by Schoch et al. [85] using the phylogeny of extant lineages found saprobic and parasitic modes among the ancestral characters of Pezizomycotina. Similarly, Savile [86] proposed the existence of parasitic fungi on vascular plants in the early stages of territorialization. Using this evidence, Lücking et al. [87] formulated the ‘green scenario’ which stated that parasitic fungi from freshwater bodies co-evolved with the ancestors of land plants and diversified to many lifestyles [81]. Together, with all these facts and evidence for the existence of pathogenic and saprobic ancestral modes, we can explain that the pathogenic/saprobic nutritional mode resulted as the ancestral nutritional mode for Botryosphaeriales in our analysis.
As time progresses, the nutritional mode of botryosphaerialean taxa diversified into all three nutritional modes, i.e., endophytes/saprobes/pathogens (around 100 Mya), suggesting multiple switching events during their evolution (Figure 7). Flowering plants and other flora, such as deciduous trees (modern plants), ferns and grasses were abundant during the Cretaceous and Paleogene periods [88,89]. Angiosperms diversified rapidly during the Cretaceous period and Botryosphaeriaceae species are mostly diverse on Angiosperms [4]. Batista et al. [90] mentioned that the high host diversity may affect the fungal diversity in different plant functional groups. Therefore, the diversity of the plant hosts is one of the reasons for the change in the nutritional modes in botryosphaerialean species. This is also evident in other fungal lineages. Some studies have shown that the nutritional mode switch from the ancestral insect-parasitic or plant-pathogenic fungi to endophytic ascomycetes [91,92], and some show a switch from lichen-forming, endolichenic and saprotrophic fungi to endophytic fungi [93].
Stress or pressure on plants is a factor that changes with climatic conditions or extreme weather conditions (high temperatures, cold, drought or extreme rain) and the effect of herbivores or pests on plants [10]. Under this stress or pressure, many endophytic fungi became pathogenic to plants [10,73]. According to the results of our analysis, endophytic/pathogenic botryosphaerialean taxa diversified into pathogenic taxa at around 78 Mya in the late epoch of the Cretaceous (Figure 7). During the Cretaceous period, warmer and humid environments that existed caused increased stress on plants and led to botryosphaerialean taxa changing their nutritional mode from endophytic to pathogenic. Endophytic taxa also become saprobic when environmental conditions are unfavourable to the host or when the host dies [73,94].
In their study, Hyde et al. [73] suggested two scenarios for the evolution of Diaporthomycetidae, i.e., (1) The ancestors of Diaporthomycetidae had endophytic lifestyles that colonized inside the plants similar to some aquatic hyphomycetes that also share endophytic ancestors. These endophytic fungi become active when the plants are under stress or senesced and convert into either saprobes to decay the dead plant parts or pathogens to cause disease. (2) The ancestors of Diaporthomycetidae had non-specific saprobic lifestyles and at some point, they became plant pathogens in specific plants to cause diseases. Based on our results, we also can accept the first hypothesis for the class Dothideomycetes. However, for Botryosphaeriales, none of the hypotheses are applicable.
However, with only a few studies on endophytic botryosphaerialean taxa, we were unable to provide conclusive evidence for our hypothesis that the endophytic nutritional mode could be ancestral for Botryosphaeriales species, and later they diversified into saprobic and pathogenic modes. Therefore, further studies are required related to endophytic species in Botryosphaeriales to investigate this hypothesis.

3.3.2. Ancestral State Reconstructions for Conidial Colour and Septation in Botryosphaeriales Taxa

In this analysis, we assessed our second hypothesis that “There is a link between the conidial colour and nutritional mode in botryosphaerialean taxa”. The evolution of two morphological characters, conidial colour and septation, was reconstructed by employing the tree generated from the evolution analysis (Figure 7). Two parameters were considered: hyaline and pigmented. All light brown, brown and dark brown conidia were considered as pigmented. Septate and aseptate parameters were used for conidial septation. All conidia with one or more septa were included under the septate parameter.
Ancestral character analyses of conidial colour and septation indicate the hyaline and aseptate conidia as the common ancestral character in both Botryosphaeriales and Dothideomycetes. This is not the first study to show hyaline fungal structures as an ancestral form. The hyaline appressoria are considered ancestral in appressorial fungi [54]; similarly, hyaline ascospores in Xylariomycetidae are regarded as ancestral [95].
At around 49 Mya and 47 Mya in the Eocene of the Paleogene (33.9–56 Mya), botryosphaerialean taxa diversified their conidial colour from hyaline to pigmented and conidial septation from aseptate to septate, respectively. Hyaline to pigmented and septate to aseptate conidia occur among taxa in Botryosphaeriaceae. Most of the conidia in Phyllostictaceae are hyaline and aseptate, while few are pigmented and septate [3,39,41,96]. Phyllosticta philoprina and Pseudofusicoccum artocarpi have pigmented conidia and among them, P. artocarpi has septate conidia (Table S1). Both Pseudofusicoccum ardesiacum and P. kimberleyensis have hyaline, septate conidia [19,97]. Hyaline and pigmented conidia occur in Melanopsaceae and Aplosporellaceae, respectively, and are aseptate in both families. Planistromellaceae have both septate and aseptate hyaline conidia. In Saccharataceae, most of the species have hyaline, aseptate conidia, while few have hyaline, septate conidia (Table S1).
The fossil records of Diplodia (Sphaeropsis) have been recorded from permineralized chert from the Deccan Intertrappean bed, India [98]. Two-celled spores 13 μm long and thick-walled, oval and pycnidia have been recorded in the permineralized specimens of D. intertrappea [99]. Therefore, septate conidia were recorded in D. intertrappea in ancient times. Similarly, fossil records of Diplodites rodei (Basionym: Diplodia rodei) and D. sahnii (Basionym: Diplodia sahnii) have been recorded from the Mohgaonkalan locality in Chhindwara District, Madhya Pradesh, India [100]. These fossils belonged to the Late Cretaceous period [100]. According to the fossil records, Diplodites had one-septate dark brown or aseptate light brown conidia [100,101]. Fossils of Diplodites are morphologically similar to the extant fungi of Diplodia, Dothiorella and Macrophoma [100]. This provides evidence that in the late Cretaceous period, ancestors of Diplodia had aseptate or one-septate, light to dark brown conidia [100].
The evolutionary study (Figure 4) indicates Botryosphaeriales originated and evolved during the Cretaceous (66–145 Mya) and Paleogene periods (23–66 Mya). A warm environment existed during the Cretaceous period, which may be in response to volcanic activity and increased atmospheric greenhouse gas concentrations [88]. The temperature of the sea surface during the Cretaceous period varied between 37–42 °C [88]. During the Paleogene period, the temperature dropped to about 23–29 °C (±4.7 °C) and formed a cool and dry environment [89]. According to Hagiwara et al. [102], temperature mainly affects conidial pigmentation. As they suggested, most species produce pigmented conidia at 25 °C or 37 °C [102].
At around 49 Mya, some members of Botryosphaeriales diversified from hyaline conidia to pigmented, while others remained as hyaline. Melanized spores survive under extreme environmental conditions, such as excessive heat or cold, extremely dry conditions, extreme pH or osmotic conditions, hypersaline environments, polychromatic radiation, radionuclides and UV radiation [47]. Non-pigmented spores die under hard UV radiation within a few minutes, but melanized spores survive [46,47]. Based on these observations and our results, we conclude that hyaline conidia diversified to pigmented during the Eocene epoch of the Paleogene period for survival under harsh environmental conditions, such as high temperature variation. The Paleocene–Eocene was considered as the most significant time period of global warming and was followed by a long cool and dry period [103].
In addition, we evaluated sexual morph characters, i.e., ascospore colour and septation in preliminary studies. Due to a lack of variation and representative data, reliable results were not obtained. Therefore, we did not include ascospore characters for the ancestral character analyses in this study.
Belozerskaya et al. [47] showed that both saprobic and pathogenic taxa have melanized conidial walls that appeared as pigmented conidia. Our study confirmed that there was link between conidial colour and nutritional mode in botryosphaerialean taxa, which supports our second hypothesis. Based on the results of the ancestral character analyses, the genera with pigmented conidia show pathogenic and saprobic nutritional modes (Figure 8). Exceptions to this are Endomelanconiopsis species that have pigmented conidia, even though most of them are endophytic (Figure 8). Most Botryosphaeria and Neofusicoccum species are pathogenic and unlike others, most of them have hyaline conidia. Therefore, our second hypothesis is not applicable for all the genera in Botryosphaeriales. Most of the pathogenic genera have pigmented conidia in this order.

4. Conclusions

In this study, updated phylogenetic analyses (ML, MP and BI), evolutionary divergence times, ancestral character analyses for conidial colour and septation and nutritional mode analyses are provided for all families in Botryosphaeriales. Based on our findings, we conclude: (1) Six families, namely, Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae and Saccharataceae in this order were well-separated in our phylogenetic analyses. (2) According to divergence times, Botryosphaeriales may have originated in the Cretaceous period in the Mesozoic era, and all six families evolved during this period. Later, Botryosphaeriaceae and Phyllostictaceae divided into genera during the Mesozoic era (66–251.90 Mya), while other families divided during the Cenozoic era (66 Mya–present). Thus, the results of our divergence times estimation also support establishing Botryosphaeriales as an order and accepting Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae and Saccharataceae as families in this order. (3) Ancestral character analyses of conidial colour and septation and nutritional mode revealed that the common ancestor in Botryosphaeriales had hyaline, aseptate conidia and a pathogenic/ saprobic nutritional mode. Later, at 100 Mya in the late Cretaceous period, this pathogenic/saprobic ancestral nutritional mode diversified into an endophytic/pathogenic/saprobic. Botryosphaerialean taxa diversified their conidial colour from hyaline to pigmented and conidial septation from aseptate to septate in the Paleogene period. During evolution, Botryosphaeriales species diversified their conidial colour, septation and nutritional mode in response to harsh environmental conditions. Here, we investigated the hypothesis that the common ancestor of botryosphaerialean taxa had an endophytic nutritional mode and later deviated into saprobic or pathogenic when their hosts died or were under stress. However, due to the very low number of endophytic studies compared to the saprobic and pathogenic data, it was not possible to draw strong conclusions for the above hypothesis. This study revealed that further studies of endophytic taxa are required and suggested that the taxon sampling and the family composition might have affected the results of ancestral nutritional mode studies. (4) We also tested another hypothesis that related to the link between conidial colour and nutritional mode in botryosphaerialean taxa. Under this hypothesis, we considered the linkage between conidial pigmentation and the pathogenicity of Botryosphaeriales taxa. We suggest that the above correlation is applicable for most of the pathogenic genera in Botryosphaeriales, but not for all genera.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof9020184/s1, [104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185,186,187,188,189,190,191,192,193,194,195,196,197,198,199,200,201,202,203,204,205,206,207,208,209,210,211,212,213,214,215,216,217,218,219,220,221,222,223,224,225,226,227,228,229,230,231,232,233,234,235,236,237,238,239,240,241,242,243,244,245,246,247,248,249,250,251,252,253,254,255,256,257,258,259,260,261,262,263,264,265,266,267,268,269,270,271,272,273,274,275,276,277,278,279,280,281,282,283,284,285,286,287,288,289,290,291,292,293]. Table S1: Nutritional mode variation and conidial characters (colour and septation) and GenBank accession numbers of the sequences used in phylogenetic analysis.

Author Contributions

Conceptualization, A.R.R. and K.W.T.C.; methodology, A.R.R.; software, A.R.R. and M.C.S.; validation, A.R.R. and K.W.T.C.; formal analysis, A.R.R., K.W.T.C. and M.C.S.; investigation, A.R.R.; resources, S.C.K. and C.-L.Z.; data curation, K.W.T.C.; writing—original draft preparation, A.R.R.; writing—review and editing, A.R.R., K.W.T.C., A.J.L.P., J.-K.L., M.C.S., E.B.G.J., S.C.K. and C.-L.Z.; visualization, A.R.R. and K.W.T.C.; supervision, K.W.T.C., A.J.L.P., J.-K.L., M.C.S., and E.B.G.J.; project administration and funding acquisition, J.-K.L. and C.-L.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (Grant No. U1812401).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

A.R.R. offers her profound gratitude to the Thesis or Dissertation Writing Grant, reference no Oh 7702(6)/125, The Center of Excellence in Fungal Research (CEFR) scholarship of the Mae Fah Luang University, Thailand Science Research and Innovation (TSRI) grant ‘Macrofungi diversity research from the Lancang-Mekong Watershed and Surrounding areas’ (grant no. DBG6280009) and Mae Fah Luang University for the financial support. Further, A.R.R. thank Asha Dissanayake, R. J. U. Jayalal, Hasini Ekanayaka and S.N. Wijesinghe for their valuable suggestions and help.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Schoch, C.L.; Shoemaker, R.A.; Seifert, K.A.; Hambleton, S.; Spatafora, J.W.; Crous, P.W. A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 2006, 98, 1041–1052. [Google Scholar] [CrossRef] [PubMed]
  2. Minnis, A.M.; Kennedy, A.H.; Grenier, D.B.; Palm, M.E.; Rossman, A.Y. Phylogeny and taxonomic revision of the Planistromellaceae including its coelomycetous anamorphs: Contributions towards a monograph of the genus Kellermania. Pers. Mol. Phylogeny Evol. Fungi 2012, 29, 11–28. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Wikee, S.; Lombard, L.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Cheewangkoon, R.; McKenzie, E.H.C.; Hyde, K.D.; Crous, P.W. A phylogenetic re-evaluation of Phyllosticta (Botryosphaeriales). Stud. Mycol. 2013, 76, 1–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Slippers, B.; Boissin, E.; Phillips, A.J.L.; Groenewald, J.Z.; Lombard, L.; Wingfield, M.J.; Postma, A.; Burgess, T.; Crous, P.W. Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary framework. Stud. Mycol. 2013, 76, 31–49. [Google Scholar] [CrossRef] [Green Version]
  5. Wyka, S.A.; Broders, K.D. The new family Septorioideaceae, within the Botryosphaeriales and Septorioides strobi as a new species associated with needle defoliation of Pinus strobus in the United States. Fungal Biol. 2016, 120, 1030–1040. [Google Scholar] [CrossRef]
  6. Yang, T.; Groenewald, J.; Cheewangkoon, R.; Jami, F.; Abdollahzadeh, J.; Lombard, L.; Crous, P.W. Families, genera, and species of Botryosphaeriales. Fungal Biol. 2016, 121, 322–346. [Google Scholar] [CrossRef] [PubMed]
  7. Phillips, A.J.L.; Hyde, K.D.; Alves, A.; Liu, J.K. (Jack) Families in Botryosphaeriales: A phylogenetic, morphological and evolutionary perspective. Fungal Divers. 2019, 94, 1–22. [Google Scholar] [CrossRef]
  8. Zhang, W.; Groenewald, J.Z.; Lombard, L.; Schumacher, R.K.; Phillips, A.J.L.; Crous, P.W. Evaluating species in Botryosphaeriales. Pers. Mol. Phylogeny Evol. Fungi 2021, 46, 63–115. [Google Scholar] [CrossRef] [PubMed]
  9. Wu, N.A.; Dissanayake, A.J.; Manawasinghe, I.S.; Rathnayaka, A.R.; Liu, J.K.; Phillips, A.J.L.; Promputtha, I.; Hyde, K.D. https://botryosphaeriales.org/, an online platform for up-to-date classification and account of taxa of Botryosphaeriales. Database 2021, 2021, baab061. [Google Scholar] [CrossRef] [PubMed]
  10. Slippers, B.; Wingfield, M.J. Botryosphaeriaceae as endophytes and latent pathogens of woody plants: Diversity, ecology and impact. Fungal Biol. Rev. 2007, 21, 90–106. [Google Scholar] [CrossRef]
  11. Liu, J.K.; Phookamsak, R.; Doilom, M.; Wikee, S.; Li, Y.M.; Ariyawansha, H.; Boonmee, S.; Chomnunti, P.; Dai, D.Q.; Bhat, J.D.; et al. Towards a natural classification of Botryosphaeriales. Fungal Divers. 2012, 57, 149–210. [Google Scholar] [CrossRef]
  12. Barr, M.E. Prodromus to Class Loculoascomycetes; University of Massachusetts: Amherst, MA, USA, 1987. [Google Scholar]
  13. Von Arx, J.A. Plant pathogenic fungi. Mycologia 1987, 79, 919–920. [Google Scholar] [CrossRef]
  14. Crous, P.W.; Wood, A.R.; Okada, G.; Groenewald, J.Z. Foliicolous microfungi occurring on Encephalartos. Pers. Mol. Phylogeny Evol. Fungi 2008, 21, 135–146. [Google Scholar] [CrossRef] [Green Version]
  15. Crous, P.W.; Wingfield, M.J.; Burgess, T.I.; Hardy, G.E.S.J.; Crane, C.; Barrett, S.; Le Roux, J.J.; Thangavel, R.; Guarro, J.; Stchigel, A.M.; et al. Fungal Planet description sheets: 469–557. Persoonia 2016, 37, 218–403. [Google Scholar] [CrossRef]
  16. Prusky, D.; Alkan, N.; Mengiste, T.; Fluhr, R. Quiescent and Necrotrophic lifestyle choice during postharvest disease development. Annu. Rev. Phytopathol. 2013, 51, 155–176. [Google Scholar] [CrossRef]
  17. Desprez-Loustau, M.L.; Marçais, B.; Nageleisen, L.M.; Piou, D.; Vannini, A. Interactive effects of drought and pathogens in forest trees. Ann. For. Sci. 2006, 63, 597–612. [Google Scholar] [CrossRef] [Green Version]
  18. Theissen, F.; Sydow, H. Vorentwurfe zu den Pseudosphaeriales. Ann. Mycol. 1918, 16, 1–34. [Google Scholar]
  19. Phillips, A.J.L.; Alves, A.; Abdollahzadeh, J.; Slippers, B.; Wingfield, M.J.; Groenewald, J.Z.; Crous, P.W. The Botryosphaeriaceae: Genera and species known from culture. Stud. Mycol. 2013, 76, 51–167. [Google Scholar] [CrossRef] [Green Version]
  20. Smith, H.; Wingfield, M.J.; Crous, P.W.; Coutinho, I.A. Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. South Afr. J. Bot. 1996, 62, 86–88. [Google Scholar] [CrossRef] [Green Version]
  21. Denman, S.; Crous, P.W.; Taylor, J.E.; Kang, J.C.; Pascoe, I.; Wingfield, M.J. An overview of the taxonomic history of Botryosphaeria, and a re-evaluation of its anamorphs based on morphology and ITS rDNa phylogeny. Stud. Mycol. 2000, 45, 129–140. [Google Scholar]
  22. Phillips, A.J.L.; Oudemans, P.V.; Correia, A.; Alves, A. Characterisation and epitypification of Botryosphaeria corticis, the cause of blueberry cane canker. Fungal Divers. 2006, 21, 141–155. [Google Scholar]
  23. Huang, W.Y.; Cai, Y.Z.; Hyde, K.D.; Corke, H.; Sun, M. Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers. 2009, 33, 61–75. [Google Scholar]
  24. Pérez, C.A.; Wingfield, M.J.; Slippers, B.; Altier, N.A.; Blanchette, R.A. Endophytic and canker-associated Botryosphaeriaceae occurring on non-native Eucalyptus and native Myrtaceae trees in Uruguay. Fungal Divers. 2010, 41, 53–69. [Google Scholar] [CrossRef] [Green Version]
  25. Ghimire, S.R.; Charlton, N.D.; Bell, J.D.; Krishnamurthy, Y.L.; Craven, K.D. Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers. 2010, 47, 19–27. [Google Scholar] [CrossRef]
  26. González, V.; Tello, M.L. The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers. 2011, 47, 29–42. [Google Scholar] [CrossRef]
  27. Laurent, B.; Marchand, M.; Chancerel, E.; Saint-Jean, G.; Capdevielle, X.; Poeydebat, C.; Bellée, A.; Comont, G.; Villate, L.; Desprez-Loustau, M.L. A richer community of Botryosphaeriaceae within a less diverse community of fungal endophytes in grapevines than in adjacent forest trees revealed by a mixed metabarcoding strategy. Phytobiomes J. 2020, 4, 252–267. [Google Scholar] [CrossRef]
  28. Mohali, S.R.; Slippers, B.; Wingfield, M.J. Identification of Botryosphaeriaceae from Eucalyptus, Acacia and Pinus in Venezuela. Fungal Divers. 2007, 25, 103–125. [Google Scholar]
  29. Lazzizera, C.; Frisullo, S.; Alves, A.; Lopes, J.; Phillips, A.J.L. Phylogeny and morphology of Diplodia species on olives in Southern Italy and description of Diplodia olivarum sp. nov. Fungal Divers. 2008, 31, 63–71. [Google Scholar]
  30. Marincowitz, S.; Groenewald, J.Z.; Wingfield, M.J.; Crous, P.W. Species of Botryosphaeriaceae occurring on Proteaceae. Pers. Mol. Phylogeny Evol. Fungi 2008, 21, 111–118. [Google Scholar] [CrossRef] [Green Version]
  31. Burgess, T.I.; Tan, Y.P.; Garnas, J.; Edwards, J.; Scarlett, K.A.; Shuttleworth, L.A.; Daniel, R.; Dann, E.K.; Parkinson, L.E.; Dinh, Q.; et al. Current status of the Botryosphaeriaceae in Australia. Australas. Plant Pathol. 2019, 48, 35–44. [Google Scholar] [CrossRef]
  32. Garcia, J.F.; Lawrence, D.P.; Morales-Cruz, A.; Travadon, R.; Minio, A.; Hernandez-Martinez, R.; Rolshausen, P.E.; Baumgartner, K.; Cantu, D. Phylogenomics of plant-associated Botryosphaeriaceae species. Front. Microbiol. 2021, 12, 652802. [Google Scholar] [CrossRef] [PubMed]
  33. Dissanayake, A.J.; Chen, Y.Y.; Cheewangkoon, R.; Liu, J.K. Occurrence and morpho-molecular identification of Botryosphaeriales species from Guizhou Province, China. J. Fungi 2021, 7, 893. [Google Scholar] [CrossRef] [PubMed]
  34. Wijayawardene, N.N.; Hyde, K.D.; Dai, D.Q.; Sánchez-García, M.; Goto, B.T.; Saxena, R.K.; Erdoğdu, M.; Selçuk, F.; Rajeshkumar, K.C.; Aptroot, A.; et al. Outline of Fungi and fungus-like taxa—2021. Mycosphere 2022, 13, 53–453. [Google Scholar] [CrossRef]
  35. Batista, E.; Lopes, A.; Alves, A. What do we know about Botryosphaeriaceae? An overview of a worldwide cured dataset. Forests 2021, 12, 313. [Google Scholar] [CrossRef]
  36. Ekanayaka, A.H.; Dissanayake, A.J.; Jayasiri, S.C.; To-anun, C.; Jones, G.E.B.; Zhao, Q.; Hyde, K.D. Aplosporella thailandica; a novel species revealing the sexual-asexual connection in Aplosporellaceae (Botryosphaeriales). Mycosphere 2016, 7, 440–447. [Google Scholar] [CrossRef]
  37. Sharma, R.; Kulkarni, G.; Sonawane, M.S. Alanomyces, a new genus of Aplosporellaceae based on four loci phylogeny. Phytotaxa 2017, 297, 168–175. [Google Scholar] [CrossRef]
  38. Okane, I.; Lumyong, S.; Nakagiri, A.; Ito, T. Extensive host range of an endophytic fungus, Guignardia endophyllicola (anamorph, Phyllosticta capitalensis). Mycoscience 2003, 44, 353–363. [Google Scholar] [CrossRef]
  39. Glienke, C.; Pereira, O.L.; Stringari, D.; Fabris, J.; Kava-Cordeiro, V.; Galli-Terasawa, L.; Cunnington, J.; Shivas, R.G.; Groenewald, J.Z.; Crous, P.W. Endophytic and pathogenic Phyllosticta species, with reference to those associated with Citrus Black spot. Pers. Mol. Phylogeny Evol. Fungi 2011, 26, 47–56. [Google Scholar] [CrossRef] [Green Version]
  40. Wikee, S.; Udayanga, D.; Crous, P.W.; Chukeatirote, E.; McKenzie, E.H.C.; Bahkali, A.H.; Dai, D.; Hyde, K.D. Phyllosticta—An overview of current status of species recognition. Fungal Divers. 2011, 51, 43–61. [Google Scholar] [CrossRef]
  41. Wikee, S.; Lombard, L.; Crous, P.W.; Nakashima, C.; Motohashi, K.; Chukeatirote, E.; Alias, S.A.; McKenzie, E.H.C.; Hyde, K.D. Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers. 2013, 60, 91–105. [Google Scholar] [CrossRef]
  42. Rashmi, M.; Kushveer, J.S.; Sarma, V.V. A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 2019, 10, 798–1079. [Google Scholar] [CrossRef]
  43. Barr, M.E. Planistromellaceae, a new family in the Dothideales. Mycotaxon 1996, 60, 433–442. [Google Scholar]
  44. Halbwachs, H.; Brandl, R.; Bässler, C. Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles. Fungal Ecol. 2015, 17, 197–204. [Google Scholar] [CrossRef]
  45. Wong, H.J.; Mohamad-Fauzi, N.; Rizman-Idid, M.; Convey, P.; Alias, S.A. Protective mechanisms and responses of micro-fungi towards ultraviolet-induced cellular damage. Polar Sci. 2019, 20, 19–34. [Google Scholar] [CrossRef]
  46. Ho, W.H.; Hyde, K.D. A new type of conidial septal pore in fungi. Fungal Divers. 2004, 15, 171–186. [Google Scholar]
  47. Belozerskaya, T.A.; Gessler, N.N.; Aver, A.A. Fungal Metabolites. In Fungal Metabolites Reference Series in Phytochemistry; Mérillon, J.-M., Ramawat, K.G., Eds.; Springer International Publishing: Cham, Switzerland, 2017; pp. 263–291. ISBN 978-3-31925-001-4. [Google Scholar]
  48. Nosanchuk, J.D.; Casadevall, A. The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 2003, 5, 203–223. [Google Scholar] [CrossRef] [PubMed]
  49. Phillips, A.J.L.; Alves, A.; Pennycook, S.R.; Johnston, P.R.; Ramaley, A.; Akulov, A.; Crous, P.W. Resolving the phylogenetic and taxonomic status of dark-spored teleomorph genera in the Botryosphaeriaceae. Persoonia 2008, 21, 29–55. [Google Scholar] [CrossRef]
  50. Phillips, A.J.L.; Alves, A. Taxonomy, phylogeny, and epitypification of Melanops tulasnei, the type species of Melanops. Fungal Divers. 2009, 38, 155–166. [Google Scholar]
  51. Ekman, S.; Andersen, H.L.; Wedin, M. The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (Lichenized Ascomycota). Syst. Biol. 2008, 57, 141–156. [Google Scholar] [CrossRef] [PubMed]
  52. Mardones, M.; Trampe-Jaschik, T.; Oster, S.; Elliott, M.; Urbina, H.; Schmitt, I.; Piepenbring, M. Phylogeny of the order Phyllachorales (Ascomycota, Sordariomycetes): Among and within order relationships based on five molecular loci. Pers. Mol. Phylogeny Evol. Fungi 2017, 39, 74–90. [Google Scholar] [CrossRef]
  53. Thiyagaraja, V.; Lücking, R.; Ertz, D.; Wanasinghe, D.N.; Karunarathna, S.C.; Camporesi, E.; Hyde, K.D. Evolution of non-lichenized, saprotrophic species of Arthonia (Ascomycota, Arthoniales) and resurrection of Naevia, with notes on Mycoporum. Fungal Divers. 2020, 102, 205–224. [Google Scholar] [CrossRef]
  54. Chethana, K.W.T.; Jayawardena, R.S.; Chen, Y.J.; Konta, S.; Tibpromma, S.; Phukhamsakda, C.; Abeywickrama, P.D.; Samarakoon, M.C.; Senwanna, C.; Mapook, A.; et al. Appressorial interactions with host and their evolution; Springer: Amsterdam, The Netherlands, 2021; Volume 110, ISBN 01-2-3456-789. [Google Scholar]
  55. Katoh, K.; Rozewicki, J.; Yamada, K.D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019, 20, 1160–1166. [Google Scholar] [CrossRef] [Green Version]
  56. Hall, T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41, 95–98. [Google Scholar]
  57. Dissanayake, A.J.; Bhunjun, C.S.; Maharachchikumbura, S.S.N.; Liu, J.K. Applied aspects of methods to infer phylogenetic relationships amongst fungi. Mycosphere 2020, 11, 2652–2676. [Google Scholar] [CrossRef]
  58. Nylander, J.A.A. MrModeltest v2. Program distributed by the author. Evol. Biol. Cent. Uppsala Univ. 2004, 2, 1–2. [Google Scholar]
  59. Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Miller, M.A.; Pfeiffer, W.; Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic Trees. In Proceedings of the 2010 Gateway Computing Environments Workshop (GCE), New Orleans, LA, USA, 14 November 2010; ISBN 978-1-42449-752-2. [Google Scholar]
  61. Ronquist, F.; Teslenko, M.; Van Der Mark, P.; Ayres, D.L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M.A.; Huelsenbeck, J.P. Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012, 61, 539–542. [Google Scholar] [CrossRef] [Green Version]
  62. Swofford, D.L. PAUP: Phylogenetic analysis using parsimony, version 4.0 b10. Sinauer Assoc. Sunderl. 2002, 56, 1776–1788. [Google Scholar] [CrossRef]
  63. Rambaut, A. Fig. Tree. Tree Fig. Drawing Tool, v. 1.4.0. 2012. Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 1 May 2021).
  64. Drummond, A.J.; Suchard, M.A.; Xie, D.; Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29, 1969–1973. [Google Scholar] [CrossRef] [Green Version]
  65. Drummond, A.J.; Ho, S.Y.W.; Phillips, M.J.; Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4, e88. [Google Scholar] [CrossRef]
  66. Rambaut, A.; Suchard, M.A.; Xie, D.; Drummond, A.J.; Tracer Version 1.6. University of Edinburgh. 2013. Available online: http://tree.bio.ed.ac.uk/software/tracer (accessed on 10 April 2021).
  67. Yu, Y.; Harris, A.J.; Blair, C.; He, X. RASP (Reconstruct Ancestral State in Phylogenies): A tool for historical biogeography. Mol. Phylogenet. Evol. 2015, 87, 46–49. [Google Scholar] [CrossRef] [PubMed]
  68. Yu, Y.; Blair, C.; He, X. RASP 4: Ancestral state reconstruction tool for multiple genes and characters. Mol. Phylogenet. Evol. 2019, 37, 604–606. [Google Scholar] [CrossRef] [PubMed]
  69. Pérez-Ortega, S.; Garrido-Benavent, I.; Grube, M.; Olmo, R.; De los Ríos, A. Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Divers. 2016, 80, 285–300. [Google Scholar] [CrossRef]
  70. Liu, J.K.; Hyde, K.D.; Jeewon, R.; Phillips, A.J.L.; Maharachchikumbura, S.S.N.; Ryberg, M.; Liu, Z.Y.; Zhao, Q. Ranking higher taxa using divergence times: A case study in Dothideomycetes. Fungal Divers. 2017, 84, 75–99. [Google Scholar] [CrossRef]
  71. Liu, N.G.; Ariyawansa, H.A.; Hyde, K.D.; Maharachchikumbura, S.S.N.; Zhao, R.L.; Phillips, A.J.L.; Jayawardena, R.S.; Thambugala, K.M.; Dissanayake, A.J.; Wijayawardene, N.N.; et al. Perspectives into the value of genera, families and orders in classification. Mycosphere 2016, 7, 1649–1668. [Google Scholar] [CrossRef]
  72. Lutzoni, F.; Nowak, M.D.; Alfaro, M.E.; Reeb, V.; Miadlikowska, J.; Krug, M.; Arnold, A.E.; Lewis, L.A.; Swofford, D.L.; Hibbett, D.; et al. Contemporaneous radiations of fungi and plants linked to symbiosis. Nat. Commun. 2018, 9, 5451. [Google Scholar] [CrossRef] [Green Version]
  73. Hyde, K.D.; Bao, D.F.; Hongsanan, S.; Chethana, K.W.T.; Yang, J.; Suwannarach, N. Evolution of freshwater Diaporthomycetidae (Sordariomycetes) provides evidence for five new orders and six new families. Fungal Divers. 2021, 107, 71–105. [Google Scholar] [CrossRef]
  74. Peace, A.L.; Phethean, J.J.J.; Franke, D.; Foulger, G.R.; Schiffer, C.; Welford, J.K.; McHone, G.; Rocchi, S.; Schnabel, M.; Doré, A.G. A review of Pangaea dispersal and Large Igneous Provinces—In search of a causative mechanism. Earth Sci. Rev. 2020, 206, 102902. [Google Scholar] [CrossRef]
  75. Heckman, D.S.; Geiser, D.M.; Eidell, B.R.; Stauffer, R.L.; Kardos, N.L.; Hedges, S.B. Molecular evidence for the early colonization of land by fungi and plants. Science 2001, 293, 1129–1133. [Google Scholar] [CrossRef] [Green Version]
  76. Hyde, K.D.; Soytong, K. The fungal endophyte dilemma. Fungal Divers. 2008, 33, 163–173. [Google Scholar]
  77. Promputtha, I.; Hyde, K.D.; McKenzie, E.H.C.; Peberdy, J.F.; Lumyong, S. Can leaf degrading enzymes provide evidence that endophytic fungi becoming saprobes? Fungal Divers. 2010, 41, 89–99. [Google Scholar] [CrossRef]
  78. Purahong, W.; Hyde, K.D. Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers. 2011, 47, 1–7. [Google Scholar] [CrossRef]
  79. Aime, M.C.; Toome, M.; McLaughlin, D.J. Pucciniomycotina. In Systematics and Evolution; Springer: Berlin/Heidelberg, Germany, 2014; pp. 271–294. ISBN 978-3-64255-318-9. [Google Scholar]
  80. Oberwinkler, F. Yeasts in Pucciniomycotina. Mycol. Prog. 2017, 16, 831–856. [Google Scholar] [CrossRef]
  81. Naranjo-Ortiz, M.A.; Gabaldón, T. Fungal evolution: Major ecological adaptations and evolutionary transitions. Biol. Rev. 2019, 94, 1443–1476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Kalgutkar, R.M. Paleogene fungal palynomorphs from Bonnet Plume Formation, Yukon Territory. Contrib. Can. Paleontol. Geol. Surv. Can. Bull. 1993, 444, 51–105. [Google Scholar]
  83. Taylor, T.N.; Krings, M. Fossil microorganisms and land plants: Associations and interactions. Symbiosis 2005, 40, 119–135. [Google Scholar]
  84. Krings, M.; Dotzler, N.; Taylor, T.N.; Galtier, J. A Late Pennsylvanian fungal leaf endophyte from Grand-Croix, France. Rev. Palaeobot. Palynol. 2009, 156, 449–453. [Google Scholar] [CrossRef]
  85. Schoch, C.L.; Sung, G.H.; López-Giráldez, F.; Townsend, J.P.; Miadlikowska, J.; Hofstetter, V.; Robbertse, B.; Matheny, P.B.; Kauff, F.; Wang, Z.; et al. The Ascomycota tree of life: A phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst. Biol. 2009, 58, 224–239. [Google Scholar] [CrossRef]
  86. Savile, D.B.O. Possible interrelationships between fungal groups. In The Fungi: An Advanced Treatise Vol III: The Fungal Population; Ainsworth, G.C., Sussman, A.S., Eds.; Academic Press: New York, NY, USA, 1968. [Google Scholar]
  87. Lücking, R.; Huhndorf, S.; Pfister, D.H.; Plata, E.R.; Lumbsch, H.T. Fungi evolved right on track. Mycologia 2009, 101, 810–822. [Google Scholar] [CrossRef] [Green Version]
  88. Weissert, H. Mesozoic Pelagic Sediments: Archives for Ocean and Climate History During Green-House Conditions, 1st ed.; Hneke, H., Mulder, T., Eds.; Developments in Sedimentology; Elsevier’s Science & Technology Rights Department: Oxford, UK, 2011; Volume 63, pp. 765–792. [Google Scholar]
  89. Vandenberghe, N.; Hilgen, F.J.; Speijer, R.P.; Ogg, J.G.; Gradstein, F.M.; Hammer, O.; Hollis, C.J.; Hooker, J.J. The paleogene period. In The Geologic Time Scale; Elsevier: Amsterdam, The Netherlands, 2012; pp. 855–921. [Google Scholar] [CrossRef]
  90. Batista, E.; Lopes, A.; Alves, A. Botryosphaeriaceae species on forest trees in Portugal: Diversity, distribution and pathogenicity. Eur. J. Plant Pathol. 2020, 158, 693–720. [Google Scholar] [CrossRef]
  91. Rodriguez, R.J.; White, J.F.; Arnold, A.E.; Redman, R.S. Fungal endophytes: Diversity and functional roles: Tansley review. N. Phytol. 2009, 182, 314–330. [Google Scholar] [CrossRef]
  92. Raman, A.; Wheatley, W.; Popay, A. Endophytic fungus-vascular plant-insect interactions. Environ. Entomol. 2012, 41, 433–447. [Google Scholar] [CrossRef]
  93. Wheeler, D.L.; Dung, J.K.S.; Johnson, D.A. From pathogen to endophyte: An endophytic population of Verticillium dahliae evolved from a sympatric pathogenic population. New Phytol. 2019, 222, 497–510. [Google Scholar] [CrossRef] [PubMed]
  94. De Silva, N.I.; Phillips, A.J.L.; Liu, J.K.; Lumyong, S.; Hyde, K.D. Phylogeny and morphology of Lasiodiplodia species associated with Magnolia Forest plants. Sci. Rep. 2019, 9, 14355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Samarakoon, M.C.; Hyde, K.D.; Sajeewa, S.N.; Stadler, M.; Jones, E.B.G.; Promputtha, I.; Camporesi, E.; Bulgakov, T.S.; Liu, J.K. Taxonomy, Phylogeny, Molecular Dating and Ancestral State Reconstruction of Xylariomycetidae (Sordariomycetes). Fungal Divers. 2021, 112, 1–88. [Google Scholar] [CrossRef]
  96. Zhang, K.; Zhang, N.; Cai, L. Typification and phylogenetic study of Phyllosticta ampelicida and P. vaccinii. Mycologia 2013, 105, 1030–1042. [Google Scholar] [CrossRef]
  97. Pavlic, D.; Wingfield, M.J.; Barber, P.; Slippers, B.; Hardy, G.E.S.J.; Burgess, T.I. Seven new species of the Botryosphaeriaceae from baobab and other native trees in Western Australia. Mycologia 2008, 100, 851–866. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. Mahabale, T.S. On a fossil species of Diplodia from the Deccan Intertrappean series, MP, India. Palaeobot. 1968, 17, 295–297. [Google Scholar]
  99. Taylor, T.N.; Krings, M.; Taylor, E.L. Ascomycota. In Fossil Fungi; Academic Press: Cambridge, MA, USA, 2015; pp. 129–171. [Google Scholar]
  100. Saxena, R.K.; Wijayawardene, N.N.; Dai, D.Q.; Hyde, K.D.; Kirk, P.M. Diversity in fossil fungal spores. Mycosphere 2021, 12, 670–874. [Google Scholar] [CrossRef]
  101. Kalgutkar, R.M.; Nambudiri, E.M.V.; Tidwell, W.D. Diplodites sweetii sp. nov. from the Late Cretaceous (Maastrichtian) Deccan Intertrappean Beds of India. Rev. Palaeobot. Palynol. 1993, 77, 107–118. [Google Scholar] [CrossRef]
  102. Hagiwara, D.; Sakai, K.; Suzuki, S.; Umemura, M.; Nogawa, T.; Kato, N.; Osada, H.; Watanabe, A.; Kawamoto, S.; Gonoi, T.; et al. Temperature during conidiation affects stress tolerance, pigmentation, and trypacidin accumulation in the conidia of the airborne pathogen Aspergillus fumigatus. PLoS ONE 2017, 12, e0177050. [Google Scholar] [CrossRef] [PubMed]
  103. Zimmerman, K.A. Cenozoic Era: Facts About Climate, Animals & Plants. 2016. Available online: https://www.livescience.com/40352-cenozoic-era.html (accessed on 12 May 2022).
  104. Dou, Z.P.; Lu, M.; Wu, J.R.; He, W.; Zhang, Y. A new species and interesting records of Aplosporella from China. Sydowia 2017, 69, 1–7. [Google Scholar] [CrossRef]
  105. Fan, X.L.; Hyde, K.D.; Liu, J.K.; Liang, Y.M.; Tian, C.M. Multigene phylogeny and morphology reveal Phaeobotryon rhois sp. nov. (Botryosphaeriales, Ascomycota). Phytotaxa 2015, 205, 90–98. [Google Scholar] [CrossRef] [Green Version]
  106. Trakunyingcharoen, T.; Lombard, L.; Groenewald, J.Z.; Cheewangkoon, R.; To-Anun, C.; Crous, P.W. Caulicolous Botryosphaeriales from Thailand. Pers. Mol. Phylogeny Evol. Fungi 2015, 34, 87–99. [Google Scholar] [CrossRef]
  107. Mapook, A.; Hyde, K.D.; McKenzie, E.H.; Jones, E.G.; Bhat, D.J.; Jeewon, R.; Stadler, M.; Samarakoon, M.C.; Malaithong, M.; Tanunchai, B.; et al. Taxonomic and phylogenetic contributions to fungi associated with the invasive weed Chromolaena odorata (Siam weed). Fungal Divers. 2020, 101, 1–175. [Google Scholar] [CrossRef]
  108. Du, Z.; Fan, X.L.; Yang, Q.; Hyde, K.D.; Tian, C.M. Aplosporella ginkgonis (Aplosporellaceae, Botryosphaeriales), a new species isolated from Ginkgo biloba in China. Mycosphere 2017, 8, 1246–1252. [Google Scholar] [CrossRef]
  109. Deepika, Y.S.; Mahadevakumar, S.; Amruthesh, K.N.; Lakshmidevi, N. A new collar rot disease of cowpea (Vigna unguiculata) caused by Aplosporella hesperidica in India. Lett. Appl. Microbiol. 2020, 71, 154–163. [Google Scholar] [CrossRef]
  110. Crous, P.W.; Wingfield, M.J.; Guarro, J.; Cheewangkoon, R.; Van Der Bank, M.; Swart, W.J.; Stchigel, A.M.; Roux, J.; Madrid, H.; Damm, U.; et al. Fungal Planet description sheets: 154–213. Persoonia 2013, 31, 188–296. [Google Scholar] [CrossRef] [PubMed]
  111. Slippers, B.; Roux, J.; Wingfield, M.J.; Van der Walt, F.J.J.; Jami, F.; Mehl, J.W.M.; Marais, G.J. Confronting the constraints of morphological taxonomy in the Botryosphaeriales. Pers. Mol. Phylogeny Evol. Fungi 2014, 33, 155–168. [Google Scholar] [CrossRef] [Green Version]
  112. Damm, U.; Fourie, P.H.; Crous, P.W. Aplosporella prunicola, a novel species of anamorphic Botryosphaeriaceae. Fungal Divers. 2007, 27, 35–43. [Google Scholar]
  113. Cosoveanu, A.; Cabrera, R. Endophytic fungi in species of Artemisia. J. Fungi 2018, 4, 53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  114. Taylor, K.; Barber, P.A.; Hardy, G.E.S.J.; Burgess, T.I. Botryosphaeriaceae from tuart (Eucalyptus gomphocephala) woodland, including descriptions of four new species. Mycol. Res. 2009, 113, 337–353. [Google Scholar] [CrossRef] [PubMed]
  115. Crous, P.W.; Wingfield, M.J.; Le Roux, J.J.; Richardson, D.M.; Strasberg, D.; Shivas, R.G.; Alvarado, P.; Edwards, J.; Moreno, G.; Sharma, R.; et al. Fungal planet description sheets: 371–399. Pers. Mol. Phylogeny Evol. Fungi 2015, 35, 264–327. [Google Scholar] [CrossRef] [PubMed]
  116. Konta, S.; Hongsanan, S.; Phillips, A.J.L.; Jones, E.B.G.; Boonmee, S.; Hyde, K.D. Botryosphaeriaceae from palms in Thailand II—Two new species of Neodeightonia, N. rattanica and N. rattanicola from Calamus (rattan palm). Mycosphere 2016, 7, 950–961. [Google Scholar] [CrossRef]
  117. Abdollahzadeh, J.; Goltapeh, E.M.; Javadi, A.; Shams-Bakhsh, M.; Zare, R.; Phillips, A.J.L. Barriopsis iraniana and Phaeobotryon cupressi: Two new species of the Botryosphaeriaceae from trees in Iran. Pers. Mol. Phylogeny Evol. Fungi 2009, 23, 1–8. [Google Scholar] [CrossRef]
  118. Doilom, M.; Shuttleworth, L.A.; Roux, J.; Chukeatirote, E.; Hyde, K.D. Barriopsis tectonae sp. nov. a new species of Botryosphaeriaceae from Tectona grandis (teak) in Thailand. Phytotaxa 2014, 176, 81–91. [Google Scholar] [CrossRef] [Green Version]
  119. Tibpromma, S.; Hyde, K.D.; Jeewon, R.; Maharachchikumbura, S.S.N.; Liu, J.K.; Bhat, D.J.; Jones, E.B.G.; McKenzie, E.H.C.; Camporesi, E.; Bulgakov, T.S.; et al. Fungal diversity notes 491–602: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2017, 83, 1–261. [Google Scholar] [CrossRef]
  120. Slippers, B.; Smit, W.A.; Crous, P.W.; Coutinho, T.A.; Wingfield, B.D.; Wingfield, M.J. Taxonomy, phylogeny and identification of Botryosphaeriaceae associated with pome and stone fruit trees in South Africa and other regions of the world. Plant Pathol. 2007, 56, 128–139. [Google Scholar] [CrossRef] [Green Version]
  121. Pan, M.; Zhu, H.; Bezerra, J.D.; Bonthond, G.; Tian, C.; Fan, X. Botryosphaerialean fungi causing canker and dieback of tree hosts from Mount Yudu in China. Mycol. Prog. 2019, 18, 1341–1361. [Google Scholar] [CrossRef]
  122. Dissanayake, A.J.; Camporesi, E.; Hyde, K.D.; Yan, J.Y.; Li, X.H. Saprobic Botryosphaeriaceae, including Dothiorella italica sp. nov., associated with urban and forest trees in Italy. Mycosphere 2017, 8, 1157–1176. [Google Scholar] [CrossRef]
  123. Goodarzian, K.; Ghanbary, M.A.T.; Babaeizad, V.; Mojerlou, S. Identification of root endophytic fungi from rangeland plants in Mazandaran province. Iran. J. For. Range Prot. Res. 2021, 18, 216–232. [Google Scholar]
  124. Ariyawansa, H.A.; Hyde, K.D.; Liu, J.K.; Wu, S.P.; Liu, Z.Y. Additions to Karst Fungi 1: Botryosphaeria minutispermatia sp. nov., from Guizhou Province, China. Phytotaxa 2016, 275, 35–44. [Google Scholar] [CrossRef]
  125. Zhou, Y.; Dou, Z.; He, W.; Zhang, X.; Zhang, Y. Botryosphaeria sinensia sp nov., a new species from China. Phytotaxa 2016, 245, 43–50. [Google Scholar] [CrossRef]
  126. Lee, S.Y.; Ten, L.N.; Back, C.G.; Jung, H.Y. First report of apple decline caused by Botryosphaeria sinensis in Korea. Korean J. Mycol. 2021, 49, 417–423. [Google Scholar] [CrossRef]
  127. Li, G.; Liu, F.; Li, J.; Liu, Q.; Chen, S. Characterization of Botryosphaeria dothidea and Lasiodiplodia pseudotheobromae from English Walnut in China. J. Phytopathol. 2016, 164, 348–353. [Google Scholar] [CrossRef]
  128. Mondragón-Flores, A.; Rodríguez-Alvarado, G.; Gómez-Dorantes, N.; Guerra-Santos, J.J.; Fernández-Pavía, S.P. Botryosphaeriaceae: A complex, diverse and cosmopolitan family of fungi. Rev. Mex. Cienc. Agrícolas 2021, 12, 643–654. [Google Scholar] [CrossRef]
  129. Zhou, J.; Diao, X.; Wang, T.; Chen, G.; Lin, Q.; Yang, X.; Xu, J. Phylogenetic diversity and antioxidant activities of culturable fungal endophytes associated with the mangrove species Rhizophora stylosa and R. mucronata in the South China Sea. PLoS ONE 2018, 13, e0197359. [Google Scholar] [CrossRef] [Green Version]
  130. Xu, C.; Wang, C.; Ju, L.; Zhang, R.; Biggs, A.R.; Tanaka, E.; Li, B.; Sun, G. Multiple locus genealogies and phenotypic characters reappraise the causal agents of apple ring rot in China. Fungal Divers. 2015, 71, 215–231. [Google Scholar] [CrossRef]
  131. Li, G.; Slippers, B.; Wingfield, M.J.; Chen, S. Variation in Botryosphaeriaceae from Eucalyptus plantations in YunNan Province in southwestern China across a climatic gradient. IMA Fungus 2020, 11, 22. [Google Scholar] [CrossRef]
  132. Li, G.Q.; Liu, F.F.; Li, J.Q.; Liu, Q.L.; Chen, S.F. Botryosphaeriaceae from Eucalyptus plantations and adjacent plants in China. Persoonia Mol. Phylogeny Evol. Fungi 2018, 40, 63–95. [Google Scholar] [CrossRef] [Green Version]
  133. Zhou, Y.P.; Zhang, M.; Dou, Z.; Zhang, Y. Botryosphaeria rosaceae sp. nov. and B. ramosa, new botryosphaeriaceous taxa from China. Mycosphere 2017, 8, 162–171. [Google Scholar] [CrossRef]
  134. Li, W.J.; McKenzie, E.H.C.; Liu, J.K.; Bhat, D.J.; Dai, D.Q.; Camporesi, E.; Tian, Q.; Maharachchikumbura, S.S.N.; Luo, Z.L.; Shang, Q.J.; et al. Taxonomy and phylogeny of hyaline-spored coelomycetes. Fungal Divers. 2020, 100, 279–801. [Google Scholar]
  135. Barakat, F.; Vansteelandt, M.; Triastuti, A.; Jargeat, P.; Jacquemin, D.; Graton, J.; Mejia, K.; Cabanillas, B.; Vendier, L.; Stigliani, J.L.; et al. Thiodiketopiperazines with two spirocyclic centers extracted from Botryosphaeria mamane, an endophytic fungus isolated from Bixa orellana L. Phytochemistry 2019, 158, 142–148. [Google Scholar] [CrossRef] [PubMed]
  136. Monteiro, F.; Diniz, I.; Pena, A.R.; Catarino, L.; Baldé, A.; Romeiras, M.; Batista, D. Diversity of the Botryosphaeriaceae family in Guinea-Bissau (West Africa): The beginning of a tale in cashew. In Proceedings of the 15th European Conference on Fungal Genetics, Rome, Italy, 17–20 February 2020; p. 125. [Google Scholar]
  137. Damm, U.; Crous, P.W.; Fourie, P.H. Botryosphaeriaceae as potential pathogens of Prunus species in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora sp. nov. Mycologia 2007, 99, 664–680. [Google Scholar] [CrossRef] [PubMed]
  138. Jami, F.; Slippers, B.; Wingfield, M.J.; Gryzenhout, M. Greater Botryosphaeriaceae diversity in healthy than associated diseased Acacia karroo tree tissues. Australas. Plant Pathol. 2013, 42, 421–430. [Google Scholar] [CrossRef]
  139. Hyde, K.D.; Chaiwan, N.; Norphanphoun, C.; Boonmee, S.; Camporesi, E.; Chethana, K.W.T.; Dayarathne, M.C.; De Silva, N.I.; Dissanayake, A.J.; Ekanayaka, A.H.; et al. Mycosphere notes 169–224. Mycosphere 2018, 9, 271–430. [Google Scholar] [CrossRef]
  140. Lawrence, D.P.; Peduto Hand, F.; Gubler, W.D.; Trouillas, F.P. Botryosphaeriaceae species associated with dieback and canker disease of bay laurel in northern California with the description of Dothiorella californica sp. nov. Fungal Biol. 2017, 121, 347–360. [Google Scholar] [CrossRef]
  141. Ariyawansa, H.A.; Hyde, K.D.; Jayasiri, S.C.; Buyck, B.; Chethana, K.W.T.; Dai, D.Q.; Dai, Y.C.; Daranagama, D.A.; Jayawardena, R.S.; Lücking, R.; et al. Fungal diversity notes 111–252—Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2015, 75, 27–274. [Google Scholar] [CrossRef]
  142. González-Domínguez, E.; Alves, A.; León, M.; Armengol, J. Characterization of Botryosphaeriaceae species associated with diseased loquat (Eriobotrya japonica) in Spain. Plant Pathol. 2017, 66, 77–89. [Google Scholar] [CrossRef]
  143. Osorio, J.A.; Crous, C.J.; de Beer, Z.W.; Wingfield, M.J.; Roux, J. Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol. 2017, 121, 361–393. [Google Scholar] [CrossRef] [Green Version]
  144. Elena, G.; León, M.; Abad-Campos, P.; Armengol, J.; Mateu-Andrés, I.; Güemes-Heras, J. First report of Diplodia fraxini causing dieback of Fraxinus angustifolia in Spain. Plant Dis. 2018, 102, 2645–2646. [Google Scholar] [CrossRef]
  145. Hanifeh, S.; Ghoosta, Y.; Abbasi, S.; Phillips, A.J.L. First report of Diplodia malorum Fuckel the causal agent of canker disease of apple trees in Iran. Iran. J. Plant Pathol. 2013, 49, 83–84. [Google Scholar]
  146. Abdollahzadeh, J.; Hosseini, F.; Javadi, A. New records from Botryosphaeriaceae (Ascomycota) for mycobiota of Iran. Mycol. Iran. 2014, 1, 34–41. [Google Scholar]
  147. Linaldeddu, B.T.; Franceschini, A.; Alves, A.; Phillips, A.J.L. Diplodia quercivora sp. nov.: A new species of Diplodia found on declining Quercus canariensis trees in Tunisia. Mycologia 2013, 105, 1266–1274. [Google Scholar] [CrossRef]
  148. Van der Walt, F.J.J. Botryosphaeriaceae associated with native Acacia species in southern Africa with special reference to A. mellifera. Doctoral Dissertation, University of Pretoria, Pretoria, South Africa, 2008. [Google Scholar]
  149. Phillips, A.J.L.; Lopes, J.; Abdollahzadeh, J.; Bobev, S.; Alves, A. Resolving the Diplodia complex on apple and other Rosaceae hosts. Persoonia Mol. Phylogeny Evol. Fungi 2012, 29, 29–38. [Google Scholar] [CrossRef] [Green Version]
  150. Burgess, T.; Wingfield, B.D.; Wingfield, M.J. Comparison of genotypic diversity in native and introduced populations of Sphaeropsis sapinea isolated from Pinus radiata. Mycol. Res. 2001, 105, 1331–1339. [Google Scholar] [CrossRef] [Green Version]
  151. Chakusary, M.K.; Mohammadi, H.; Khodaparast, S.A. Diversity and pathogenicity of Botryosphaeriaceae species on forest trees in the north of Iran. Eur. J. For. Res. 2019, 138, 685–704. [Google Scholar] [CrossRef]
  152. Manzanos, T.; Aragones, A.; Iturritxa, E. Diplodia scrobiculata: A latent pathogen of Pinus radiata reported in northern Spain. Phytopathol. Mediterr. 2017, 56, 274–277. [Google Scholar]
  153. Úrbez-Torres, J.R.; Leavitt, G.M.; Guerrero, J.C.; Guevara, J.; Gubler, W.D. Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agents of bot canker disease of grapevines in Mexico. Plant Dis. 2008, 92, 519–529. [Google Scholar] [CrossRef] [Green Version]
  154. De Errasti, A.; Carmarán, C.C.; Novas, M.V. Diversity and significance of fungal endophytes from living stems of naturalized trees from Argentina. Fungal Divers. 2010, 41, 29–40. [Google Scholar] [CrossRef]
  155. Alves, A.; Linaldeddu, B.T.; Deidda, A.; Scanu, B.; Phillips, A.J.L. The complex of Diplodia species associated with Fraxinus and some other woody hosts in Italy and Portugal. Fungal Divers. 2014, 67, 143–156. [Google Scholar] [CrossRef]
  156. Linaldeddu, B.T.; Bottecchia, F.; Bregant, C.; Maddau, L.; Montecchio, L. Diplodia fraxini and Diplodia subglobosa: The main species associated with cankers and dieback of Fraxinus excelsior in North-Eastern Italy. Forests 2020, 11, 883. [Google Scholar] [CrossRef]
  157. Yuan, H.S.; Lu, X.; Dai, Y.C.; Hyde, K.D.; Kan, Y.H.; Kušan, I.; He, S.H.; Liu, N.G.; Sarma, V.V.; Zhao, C.L.; et al. Fungal diversity notes 1277–1386: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2020, 104, 1–266. [Google Scholar] [CrossRef]
  158. Phookamsak, R.; Hyde, K.D.; Jeewon, R.; Bhat, D.J.; Jones, E.B.G.; Maharachchikumbura, S.S.N.; Raspé, O.; Karunarathna, S.C.; Wanasinghe, D.N.; Hongsanan, S.; et al. Fungal diversity notes 929–1035: Taxonomic and phylogenetic contributions on genera and species of fungi. Fungal Divers. 2019, 95, 1–273. [Google Scholar] [CrossRef] [Green Version]
  159. Zhang, M.; He, W.; Wu, J.R.; Zhang, Y. Two new species of Spencermartinsia (Botryosphaeriaceae, Botryosphaeriales) from China. Mycosphere 2016, 7, 942–949. [Google Scholar] [CrossRef]
  160. Xiao, X.E.; Wang, W.; Crous, P.W.; Wang, H.K.; Jiao, C.; Huang, F.; Pu, Z.X.; Zhu, Z.R.; Li, H.Y. Species of Botryosphaeriaceae associated with citrus branch diseases in China. Pers. Mol. Phylogeny Evol. Fungi 2021, 47, 106–135. [Google Scholar] [CrossRef]
  161. Hyde, K.D.; de Silva, N.I.; Jeewon, R.; Bhat, D.J.; Phookamsak, R.; Doilom, M.; Boonmee, S.; Jayawardena, R.S.; Maharachchikumbura, S.S.N.; Senanayake, I.C.; et al. AJOM new records and collections of fungi: 1–100. Asian J. Mycol. 2020, 3, 22–294. [Google Scholar] [CrossRef]
  162. De Wet, J.; Slippers, B.; Preisig, O.; Wingfield, B.D.; Tsopelas, P.; Wingfield, M.J. Molecular and morphological characterization of Dothiorella casuarini sp. nov. and other Botryosphaeriaceae with diplodia-like conidia. Mycologia 2009, 101, 503–511. [Google Scholar] [CrossRef] [Green Version]
  163. Hyde, K.D.; Hongsanan, S.; Jeewon, R.; Bhat, D.J.; McKenzie, E.H.C.; Jones, E.B.G.; Phookamsak, R.; Ariyawansa, H.A.; Boonmee, S.; Zhao, Q.; et al. Fungal diversity notes 367–490: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2016, 80, 1–270. [Google Scholar] [CrossRef]
  164. Jayasiri, S.C.; Hyde, K.D.; Jones, E.B.G.; McKenzie, E.H.C.; Jeewon, R.; Phillips, A.J.L.; Bhat, D.J.; Wanasinghe, D.N.; Liu, J.K.; Lu, Y.Z.; et al. Diversity, morphology and molecular phylogeny of Dothideomycetes on decaying wild seed pods and fruits. Mycosphere 2019, 10, 1–186. [Google Scholar] [CrossRef]
  165. You, C.J.; Liu, X.; Li, L.X.; Tsui, C.K.M.; Tian, C.M. Dothiorella magnoliae, a new species associated with dieback of Magnolia grandiflora from China. Mycosphere 2017, 8, 1031–1041. [Google Scholar] [CrossRef]
  166. Li, G.J.; Hyde, K.D.; Zhao, R.L.; Hongsanan, S.; Abdel-Aziz, F.A.; Abdel-Wahab, M.A.; Alvarado, P.; Alves-Silva, G.; Ammirati, J.F.; Ariyawansa, H.A.; et al. Fungal diversity notes 253–366: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 2016, 78, 1–237. [Google Scholar] [CrossRef]
  167. Li, W.; Liu, J.; Bhat, D.J.; Camporesi, E.; Xu, J.; Hyde, K.D. Introducing the novel species, Dothiorella symphoricarposicola, from Snowberry in Italy. Cryptogam. Mycol. 2014, 35, 257–270. [Google Scholar] [CrossRef]
  168. Linaldeddu, B.T.; Maddau, L.; Franceschini, A.; Alves, A.; Phillips, A.J.L. Botryosphaeriaceae species associated with lentisk dieback in Italy and description of Diplodia insularis sp. nov. Mycosphere 2016, 7, 962–977. [Google Scholar] [CrossRef]
  169. Tian, Q.; Li, W.J.; Hyde, K.D.; Camporesi, E.; Bhat, D.J.; Chomnunti, P.; Xu, J.C. Molecular taxonomy of five species of microfungi on Alnus spp. from Italy. Mycol. Prog. 2018, 17, 255–274. [Google Scholar] [CrossRef]
  170. Doll, D.A.; Rolshausen, P.E.; Pouzoulet, J.; Michailides, T.J. First report of Dothiorella iberica causing trunk and scaffold cankers of almond in California. Plant Dis. 2015, 99, 1185. [Google Scholar] [CrossRef]
  171. Váczy, K.Z.; Németh, M.Z.; Csikós, A.; Kovács, G.M.; Kiss, L. Dothiorella omnivora isolated from grapevine with trunk disease symptoms in Hungary. Eur. J. Plant Pathol. 2018, 150, 817–824. [Google Scholar] [CrossRef]
  172. Pavlic-Zupanc, D.; Piškur, B.; Slippers, B.; Wingfield, M.J.; Jurc, D. Molecular and morphological characterization of Dothiorella species associated with dieback of Ostrya carpinifolia in Slovenia and Italy. Phytopathol. Mediterr. 2015, 54, 241–252. [Google Scholar]
  173. Pitt, W.M.; Úrbez-Torres, J.R.; Trouillas, F.P. Dothiorella and Spencermartinsia, new species and records from grapevines in Australia. Australas. Plant Pathol. 2015, 44, 43–56. [Google Scholar] [CrossRef]
  174. Doilom, M.; Shuttleworth, L.A.; Roux, J.; Chukeatirote, E.; Hyde, K.D. Botryosphaeriaceae associated with Tectona grandis (teak) in Northern Thailand. Phytotaxa 2015, 233, 1–26. [Google Scholar] [CrossRef] [Green Version]
  175. Zhang, R.; Guo, X.; Sun, G.; Tang, M.; Gleason, M.L. Dothiorella viticola on Populus cathayana in China: A new record. Mycotaxon 2009, 109, 129–135. [Google Scholar] [CrossRef]
  176. Ramabulana, E.; Kunjeku, E.; Slippers, B.; Coetzee, M.P.A. Diversity of endophytes in the Botryosphaeriaceae differs on Anacardiaceae in disturbed and undisturbed ecosystems in South Africa. Forests 2022, 13, 341. [Google Scholar] [CrossRef]
  177. Douanla-Meli, C.; Scharnhorst, A. Palm foliage as pathways of pathogenic Botryosphaeriaceae fungi and host of new Lasiodiplodia species from Mexico. Pathogens 2021, 10, 1297. [Google Scholar] [CrossRef]
  178. Rojas, E.I.; Herre, E.A.; Mejia, L.C.; Arnold, A.E.; Chaverri, P.; Samuels, G.J. Endomelanconiopsis, a new anamorph genus in the Botryosphaeriaceae. Mycologia 2008, 100, 760–775. [Google Scholar] [CrossRef] [PubMed]
  179. Verkley, G.J.M.; van der Aa, H.A. Endomelanconium microsporum, a new coelomycete isolated from soil in Papua New Guinea. Mycologia 1997, 89, 967–970. [Google Scholar] [CrossRef]
  180. Jami, F.; Slippers, B.; Wingfield, M.J.; Gryzenhout, M. Botryosphaeriaceae species overlap on four unrelated, native South African hosts. Fungal Biol. 2014, 118, 168–179. [Google Scholar] [CrossRef] [Green Version]
  181. Thambugala, K.M.; Daranagama, D.A.; Camporesi, E.; Singtripop, C.; Liu, Z.Y.; Hyde, K.D. Multi-locus phylogeny reveals the sexual state of Tiarosporella in Botryosphaeriaceae. Cryptogam. Mycol. 2014, 35, 359–367. [Google Scholar] [CrossRef]
  182. Thynne, E.; McDonald, M.C.; Evans, M.; Wallwork, H.; Neate, S.; Solomon, P.S. Re-classification of the causal agent of white grain disorder on wheat as three separate species of Eutiarosporella. Australas. Plant Pathol. 2015, 44, 527–539. [Google Scholar] [CrossRef]
  183. Crous, P.W.; Muller, M.M.; Sanchez, R.M.; Giordano, L.; Bianchinotti, M.V.; Anderson, F.E.; Groenewald, J.Z. Resolving Tiarosporella spp. allied to Botryosphaeriaceae and Phacidiaceae. Phytotaxa 2015, 202, 73–93. [Google Scholar] [CrossRef]
  184. Jami, F.; Slippers, B.; Wingfield, M.; Gryzenhout, M. Five New Species of the Botryosphaeriaceae from Acacia karroo in South Africa. Cryptogam. Mycol. 2012, 33, 245–266. [Google Scholar] [CrossRef] [Green Version]
  185. Wang, Y.; Lin, S.; Zhao, L.; Sun, X.; He, W.; Zhang, Y.; Dai, Y.C. Lasiodiplodia spp. associated with Aquilaria crassna in Laos. Mycol. Prog. 2019, 18, 683–701. [Google Scholar] [CrossRef]
  186. Aguiar, F.M.; Costa, R.V.; Silva, D.D.; Lana, U.G.P.; Gomes, E.A.; Cota, L.V. First report of Lasiodiplodia brasiliense causing maize stalk rot. Australas. Plant Dis. Notes 2018, 13, 41. [Google Scholar] [CrossRef] [Green Version]
  187. Jiang, N.; Phillips, A.J.L.; Zhang, Z.X.; Tian, C.M. Morphological and molecular identification of two novel species of Melanops in China. Mycosphere 2018, 9, 1187–1196. [Google Scholar] [CrossRef]
  188. Chen, S.F.; Fichtner, E.; Morgan, D.P.; Michailides, T.J. First report of Lasiodiplodia citricola and Neoscytalidium dimidiatum causing death of graft union of English walnut in California. Plant Dis. 2013, 97, 993. [Google Scholar] [CrossRef]
  189. Machado, A.R.; Pinho, D.B.; Pereira, O.L. Phylogeny, identification and pathogenicity of the Botryosphaeriaceae associated with collar and root rot of the biofuel plant Jatropha curcas in Brazil, with a description of new species of Lasiodiplodia. Fungal Divers. 2014, 67, 231–247. [Google Scholar] [CrossRef]
  190. Cruywagen, E.M.; Slippers, B.; Roux, J.; Wingfield, M.J. Phylogenetic species recognition and hybridisation in Lasiodiplodia: A case study on species from baobabs. Fungal Biol. 2016, 121, 420–436. [Google Scholar] [CrossRef] [Green Version]
  191. Abdollahzadeh, J.; Javadi, A.; Goltapeh, E.M.; Zare, R.; Phillips, A.J.L. Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Pers. Mol. Phylogeny Evol. Fungi 2010, 25, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  192. Correia, K.C.; Silva, M.A.; De Morais, M.A.; Armengol, J.; Phillips, A.J.L.; Câmara, M.P.S.; Michereff, S.J. Phylogeny, distribution and pathogenicity of Lasiodiplodia species associated with dieback of table grape in the main Brazilian exporting region. Plant Pathol. 2016, 65, 92–103. [Google Scholar] [CrossRef]
  193. Pavlic, D.; Slippers, B.; Coutinho, T.A.; Wingfield, M.J. Botryosphaeriaceae occurring on native Syzygium cordatum in South Africa and their potential threat to Eucalyptus. Plant Pathol. 2007, 56, 624–636. [Google Scholar] [CrossRef] [Green Version]
  194. Pavlic, D.; Slippers, B.; Coutinho, T.A.; Gryzenhout, M.; Wingfield, M.J. Lasiodiplodia gonubiensis sp. nov., a new Botryosphaeria anamorph from native Syzygium cordatum in South Africa. Stud. Mycol. 2004, 50, 313–322. [Google Scholar]
  195. Netto, M.S.; Lima, W.G.; Correia, K.C.; Da Silva, C.F.; Thon, M.; Martins, R.B.; Miller, R.N.; Michereff, S.J.; Câmara, M.P. Analysis of phylogeny, distribution, and pathogenicity of Botryosphaeriaceae species associated with gummosis of Anacardium in Brazil, with a new species of Lasiodiplodia. Fungal Biol. 2016, 121, 437–451. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  196. Custódio, F.A.; Machado, A.R.; Soares, D.J.; Pereira, O.L. Lasiodiplodia hormozganensis causing basal stem rot on Ricinus communis in Brazil. Australas. Plant Dis. Notes 2018, 13, 25. [Google Scholar] [CrossRef]
  197. Al-Sadi, A.M.; Al-Wehaibi, A.N.; Al-Shariqi, R.M.; Al-Hammadi, M.S.; Al-Hosni, I.A.; Al-Mahmooli, I.H.; Al-Ghaithi, A.G. Population genetic analysis reveals diversity in Lasiodiplodia species infecting date palm, citrus, and mango in Oman and the UAE. Plant Dis. 2013, 97, 1363–1369. [Google Scholar] [CrossRef] [Green Version]
  198. Dayarathne, M.C.; Jones, E.B.G.; Maharachchikumbura, S.S.N.; Devadatha, B.; Sarma, V.V.; Khongphinitbunjong, K.; Chomnunti, P.; Hyde, K.D. Morpho-molecular characterization of microfungi associated with marine based habitats. Mycosphere 2020, 11, 1–188. [Google Scholar] [CrossRef]
  199. Rodríguez-Gálvez, E.; Guerrero, P.; Barradas, C.; Crous, P.W.; Alves, A. Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol. 2017, 121, 452–465. [Google Scholar] [CrossRef] [PubMed]
  200. Dou, Z.P.; He, W.; Zhang, Y. Does morphology matter in taxonomy of Lasiodiplodia? An answer from Lasiodiplodia hyalina sp. nov. Mycosphere 2017, 8, 1014–1027. [Google Scholar] [CrossRef]
  201. Coutinho, I.B.L.; Freire, F.C.O.; Lima, C.S.; Lima, J.S.; Gonçalves, F.J.T.; Machado, A.R.; Silva, A.M.S.; Cardoso, J.E. Diversity of genus Lasiodiplodia associated with perennial tropical fruit plants in northeastern Brazil. Plant Pathol. 2017, 66, 90–104. [Google Scholar] [CrossRef]
  202. Linaldeddu, B.T.; Deidda, A.; Scanu, B.; Franceschini, A.; Serra, S.; Berraf-Tebbal, A.; Zouaoui Boutiti, M.; Ben Jamâa, M.L.; Phillips, A.J.L. Diversity of Botryosphaeriaceae species associated with grapevine and other woody hosts in Italy, Algeria and Tunisia, with descriptions of Lasiodiplodia exigua and Lasiodiplodia mediterranea sp. nov. Fungal Divers. 2015, 71, 201–214. [Google Scholar] [CrossRef]
  203. Akgül, D.S.; Savaş, N.G.; Özarslandan, M. First Report of Wood Canker caused by Lasiodiplodia exigua and Neoscytalidium novaehollandiae on Grapevine in Turkey. Plant Dis. 2019, 103, 1036. [Google Scholar] [CrossRef]
  204. Zhang, Q.; Lu, Z.; Ding, Y.; Liu, H.; Feng, L. Canker on Machilus pauhoi caused by Lasiodiplodia margaritacea in the Fujian Province of China. Plant Dis. 2019, 103, 1417. [Google Scholar] [CrossRef]
  205. Meng, C.R.; Zhang, Q.; Yang, Z.F.; Geng, K.; Zeng, X.Y.; Chethana, K.W.T.; Wang, Y. Lasiodiplodia syzygii sp. nov. (Botryosphaeriaceae) causing post-harvest water-soaked brown lesions on Syzygium samarangense in Chiang Rai, Thailand. Biodivers. Data J. 2021, 9, e60604. [Google Scholar] [CrossRef] [PubMed]
  206. Tennakoon, D.S.; Kuo, C.H.; Maharachchikumbura, S.S.N.; Thambugala, K.M.; Gentekaki, E.; Phillips, A.J.L.; Bhat, D.J.; Wanasinghe, D.N.; de Silva, N.I.; Promputtha, I.; et al. Taxonomic and phylogenetic contributions to Celtis formosana, Ficus ampelas, F. septica, Macaranga tanarius and Morus australis leaf litter inhabiting microfungi. Fungal Divers. 2021, 108, 1–215. [Google Scholar] [CrossRef]
  207. Zaher, A.M.; Moharram, A.M.; Davis, R.; Panizzi, P.; Makboul, M.A.; Calderón, A.I. Characterisation of the metabolites of an antibacterial endophyte Botryodiplodia theobromae Pat. of Dracaena draco L. by LC–MS/MS. Nat. Prod. Res. 2015, 29, 2275–2281. [Google Scholar] [CrossRef] [PubMed]
  208. Sharma, R.; Tangjang, S.; Shukla, A.C. New Taxon of Fungal Endophytes from Phrynium capitatum Willd: A promising ethnomedicinal plant in Northeast India and its systematic and phylogenetic analysis. Sci. Technol. J. 2019, 7, 29–36. [Google Scholar] [CrossRef]
  209. Machado, A.R.; Pinho, D.B.; Soares, D.J.; Gomes, A.A.M.; Pereira, O.L. Bayesian analyses of five gene regions reveal a new phylogenetic species of Macrophomina associated with charcoal rot on oilseed crops in Brazil. Eur. J. Plant Pathol. 2019, 153, 89–100. [Google Scholar] [CrossRef]
  210. Sarr, M.P.; Ndiaye, M.B.; Groenewald, J.Z.; Crous, P.W. Genetic diversity in Macrophomina phaseolina, the causal agent of charcoal rot. Phytopathol. Mediterr. 2014, 53, 250–268. [Google Scholar]
  211. Zhao, L.; Cai, J.; He, W.; Zhang, Y. Macrophomina vaccinii sp. Nov. Causing blueberry stem blight in China. MycoKeys 2019, 55, 1–14. [Google Scholar] [CrossRef]
  212. Adamčík, S.; Cai, L.; Chakraborty, D.; Chen, X.H.; Cotter, H.V.T.; Dai, D.Q.; Dai, Y.C.; Das, K.; Deng, C.; Ghobad-Nejhad, M.; et al. Fungal biodiversity profiles 1-10. Cryptogam. Mycol. 2015, 36, 121–166. [Google Scholar] [CrossRef]
  213. Dai, D.Q.; Phookamsak, R.; Wijayawardene, N.N.; Li, W.J.; Bhat, D.J.; Xu, J.C.; Taylor, J.E.; Hyde, K.D.; Chukeatirote, E. Bambusicolous fungi. Fungal Divers. 2017, 82, 1–105. [Google Scholar] [CrossRef]
  214. Mukhtar, I.; Quan, X.; Khokhar, I.; Chou, T.; Huang, Q.; Jiang, S.; Yan, J.; Chen, B.; Huang, R.; Ashraf, H.J.; et al. First Report of Leaf Spot on Caryota mitis (Fishtail Palm) Caused by Neodeightonia palmicola in China. Plant Dis. 2019, 103, 2675. [Google Scholar] [CrossRef]
  215. Ligoxigakis, E.K.; Markakis, E.A.; Papaioannou, I.A.; Typas, M.A. First report of palm rot of Phoenix spp. caused by Neodeightonia phoenicum in Greece. Plant Dis. 2013, 97, 286. [Google Scholar] [CrossRef] [PubMed]
  216. Zhang, W.; Song, X.L. Occurrence of leaf spot caused by Neodeightonia phoenicum on pygmy date plam (Phoenix roebelenii) in China. Plant Dis. 2021, 106, 2269. [Google Scholar] [CrossRef]
  217. Hipol, R.; Magtoto, L.; Tamang, S.M.; Amor, M. Antioxidant activities of fungal endophytes isolated from strawberry Fragaria x Ananassa fruit. Electron. J. Biol. 2014, 10, 107–112. [Google Scholar]
  218. Shetty, K.G.; Rivadeneira, D.V.; Jayachandran, K.; Walker, D.M. Isolation and molecular characterization of the fungal endophytic microbiome from conventionally and organically grown avocado trees in South Florida. Mycol. Prog. 2016, 15, 977–986. [Google Scholar] [CrossRef]
  219. Espinoza, J.G.; Briceño, E.X.; Chávez, E.R.; Úrbez-Torres, J.R.; Latorre, B.A. Neofusicoccum spp. associated with stem canker and dieback of blueberry in Chile. Plant Dis. 2009, 93, 1187–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  220. Coutinho, I.B.L.; Cardoso, J.E.; Lima, C.S.; Lima, J.S.; Gonçalves, F.J.T.; Silva, A.M.S.; Freire, F.C.O. An emended description of Neofusicoccum brasiliense and characterization of Neoscytalidium and Pseudofusicoccum species associated with tropical fruit plants in northeastern Brazil. Phytotaxa 2018, 358, 251–264. [Google Scholar] [CrossRef]
  221. Linaldeddu, B.T.; Alves, A.; Phillips, A.J.L. Sardiniella urbana gen. et sp. nov., a new member of the Botryosphaeriaceae isolated from declining Celtis australis trees in Sardinian streetscapes. Mycosphere 2016, 7, 893–905. [Google Scholar] [CrossRef]
  222. Demissie, A.G.; Darge, W.A.; Cafà, G. Neofusicoccum parvum causing Eucalyptus canker and die-back diseases in Ethiopia. Int. J. Plant Pathol. 2019, 11, 1–5. [Google Scholar] [CrossRef] [Green Version]
  223. Hokama, Y.M.; Savi, D.C.; Assad, B.; Aluizio, R.; Gomes-Figueiredo, J.A.; Adamoski, D.M.; Possiede, Y.M.; Glienke, C. Endophytic fungi isolated from Vochysia divergens in the pantanal, mato grosso do sul: Diversity, phylogeny and biocontrol of Phyllosticta citricarpa. In Endophytic Fungi: Diversity, Characterization and Biocontrol; Nova Publishers: Hauppauge, NY, USA, 2016; pp. 93–123. ISBN 978-1-53610-358-8. [Google Scholar]
  224. Crous, P.W.; Groenewald, J.Z.; Shivas, R.G.; Edwards, J.; Seifert, K.A.; Alfenas, A.C.; Alfenas, R.F.; Burgess, T.I.; Carnegie, A.J.; Hardy, G.E.S.J.; et al. Fungal planet description sheets: 69-91. Pers. Mol. Phylogeny Evol. Fungi 2011, 26, 108–156. [Google Scholar] [CrossRef]
  225. Chen, S.; Li, G.; Liu, F.; Michailides, T.J. Novel species of Botryosphaeriaceae associated with shoot blight of pistachio. Mycologia 2015, 107, 780–792. [Google Scholar] [CrossRef]
  226. Zhang, M.; Lin, S.; He, W.; Zhang, Y. Three species of Neofusicoccum (Botryosphaeriaceae, Botryosphaeriales) associated with woody plants from southern China. Mycosphere 2017, 8, 797–808. [Google Scholar] [CrossRef]
  227. Jami, F.; Slippers, B.; Wingfield, M.J.; Loots, M.T.; Gryzenhout, M. Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecol. 2015, 15, 51–62. [Google Scholar] [CrossRef] [Green Version]
  228. Dissanayake, A.J.; Zhang, W.; Li, X.; Zhou, Y.; Chethana, T.; Chukeatirote, E.; Hyde, K.D.; Yan, J.; Zhang, G.; Zhao, W. First report of Neofusicoccum mangiferae associated with grapevine dieback in China. Phytopathol. Mediterr. 2015, 54, 414–419. [Google Scholar]
  229. Krishnapillai, N.; Wilson Wijeratnam, R.S. First report of Neofusicoccum mediterraneum causing stem end rot on Karuthakolumban mangoes. Plant Dis. 2015, 99, 1858. [Google Scholar] [CrossRef]
  230. Marin-Felix, Y.; Groenewald, J.Z.; Cai, L.; Chen, Q.; Marincowitz, S.; Barnes, I.; Bensch, K.; Braun, U.; Camporesi, E.; Damm, U.; et al. Genera of phytopathogenic fungi: GOPHY 1. Stud. Mycol. 2017, 86, 99–216. [Google Scholar] [CrossRef] [PubMed]
  231. Pérez, F.S.; Meriño-Gergichevich, C.; Guerrero, C.J. Detection of Neofusicoccum nonquaesitum causing dieback and canker in highbush blueberry from Southern Chile. J. Soil Sci. Plant Nutr. 2014, 14, 581–588. [Google Scholar] [CrossRef] [Green Version]
  232. Berraf-Tebbal, A.; Guereiro, M.A.; Phillips, A.J.; Von Arx, J.A. Phylogeny of Neofusicoccum species associated with grapevine trunk diseases in Algeria, with description of Neofusicoccum algeriense sp. nov. Phytopathol. Mediterr. 2014, 53, 416–427. [Google Scholar]
  233. Ngobisa, A.I.C.N.; Abidin, M.A.Z.; Wong, M.Y.; Noordin, M.W.D.W. Neofusicoccum ribis associated with leaf blight on rubber (Hevea brasiliensis) in Peninsular Malaysia. Plant Pathol. J. 2013, 29, 10–16. [Google Scholar] [CrossRef] [Green Version]
  234. Boyogueno, A.D.B. Characterization of Botryosphaeriaceae and Cryphonectriaceae associated with Terminalia spp. In Africa; University of Pretoria: Pretoria, South Africa, 2010. [Google Scholar]
  235. Summerell, B.A.; Groenewald, J.Z.; Carnegie, A.; Summerbell, R.C.; Crous, P.W. Eucalyptus microfungi known from culture. 2. Alysidiella, Fusculina and Phlogicylindrium genera nova, with notes on some other poorly known taxa. Fungal Divers. 2006, 23, 323–350. [Google Scholar]
  236. Mohd, M.H.; Salleh, B.; Zakaria, L. Identification and molecular characterizations of Neoscytalidium dimidiatum causing stem canker of red-fleshed dragon fruit (Hylocereus polyrhizus) in Malaysia. J. Phytopathol. 2013, 161, 841–849. [Google Scholar] [CrossRef]
  237. Abdel-Motaal, F.F.; Nassar, M.S.M.; El-Zayat, S.A.; El-Sayed, M.A.; Shin-Ichi, I. Antifungal activity of endophytic fungi isolated from Egyptian henbane (Hyoscyamus muticus L.). Pakistan J. Bot. 2010, 42, 2883–2894. [Google Scholar]
  238. Huang, S.K.; Tangthirasunun, N.; Phillips, A.J.L.; Dai, D.Q.; Wanasinghe, D.N.; Wen, T.C.; Bahkali, A.H.; Hyde, K.D.; Kang, J.C. Morphology and phylogeny of Neoscytalidium orchidacearum sp. nov. (Botryosphaeriaceae). Mycobiology 2016, 44, 79–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  239. Suwannarach, N.; Kumla, J.; Lumyong, S. Leaf spot on cattleya orchid caused by Neoscytalidium orchidacearum in Thailand. Can. J. Plant Pathol. 2018, 40, 109–114. [Google Scholar] [CrossRef]
  240. Daranagama, D.A.; Thambugala, K.M.; Campino, B.; Alves, A.; Bulgakov, T.S.; Phillips, A.J.L.; Liu, X.; Hyde, K.D. Phaeobotryon negundinis sp. nov. (Botryosphaeriales) from Russia. Mycosphere 2016, 7, 933–941. [Google Scholar] [CrossRef]
  241. Úrbez-Torres, J.R. The status of Botryosphaeriaceae species infecting grapevines. Phytopathol. Mediterr. 2011, 50, 5–45. [Google Scholar]
  242. Zlatković, M.; Keča, N.; Wingfield, M.J.; Jami, F.; Slippers, B. Botryosphaeriaceae associated with the die-back of ornamental trees in the Western Balkans. Antonie van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 2016, 109, 543–564. [Google Scholar] [CrossRef] [Green Version]
  243. Crous, P.W.; Wingfield, M.J.; Burgess, T.I.; Carnegie, A.J.; Hardy, G.E.S.J.; Smith, D.; Summerell, B.A.; Cano-Lira, J.F.; Guarro, J.; Houbraken, J.; et al. Fungal planet description sheets: 558-624. Persoonia 2017, 38, 240–384. [Google Scholar] [CrossRef]
  244. Norphanphoun, C.; Hongsanan, S.; Gentekaki, E.; Chen, Y.J.; Kuo, C.H.; Hyde, K.D. Differentiation of species complexes in Phyllosticta enables better species resolution. Mycosphere 2020, 11, 2542–2628. [Google Scholar] [CrossRef]
  245. Sharma, R.; Kulkarni, G.; Shouche, Y.S. Pseudofusicoccum adansoniae isolated as an endophyte from Jatropha podagrica: New record for India. Mycotaxon 2013, 123, 39–45. [Google Scholar] [CrossRef]
  246. Senwanna, C.; Hongsanan, S.; Hyde, K.D.; Cheewangkoon, R.; Konta, S.; Wang, Y. First report of the sexual morph of Pseudofusicoccum adansoniae Pavlic, T.I.Burgess & M.J.Wingf. on Para rubber Chanokned. Cryptogam. Mycol. 2020, 41, 133–146. [Google Scholar]
  247. Li, L.; Mohd, M.H.; Mohamed Nor, N.M.I.; Subramaniam, S.; Latiffah, Z. Identification of Botryosphaeriaceae associated with stem-end rot of mango (Mangifera indica L.) in Malaysia. J. Appl. Microbiol. 2021, 130, 1273–1284. [Google Scholar] [CrossRef] [PubMed]
  248. Horst, R.K. Westcott’s Plant Disease Handbook; Springer: Berlin/Heidelberg, Germany, 2008; ISBN 978-1-40204-585-1. [Google Scholar]
  249. Monkai, J.; Liu, J.K.; Boonmee, S.; Chomnunti, P.; Chukeatirote, E.; Jones, E.B.G.; Wang, Y.; Hyde, K.D. Planistromellaceae (Botryosphaeriales). Cryptogam. Mycol. 2013, 34, 45–77. [Google Scholar] [CrossRef]
  250. Crous, P.W.; Giraldo, A.; Hawksworth, D.L.; Robert, V.; Kirk, P.M.; Guarro, J.; Robbertse, B.; Schoch, C.L.; Damm, U.; Trakunyingcharoen, T.; et al. The Genera of Fungi: Fixing the application of type species of generic names. IMA Fungus 2014, 5, 141–160. [Google Scholar] [CrossRef] [PubMed]
  251. Tanney, J.B.; Seifert, K.A. Pileospora piceae gen. et sp. nov. (Septorioideaceae, Botryosphaeriales) from Picea rubens. Mycol. Prog. 2019, 18, 163–174. [Google Scholar] [CrossRef]
  252. Crous, P.W.; Wingfield, M.J.; Burgess, T.I.; Carnegie, A.J.; Hardy, G.E.S.J.; Smith, D.; Summerell, B.A.; Guarro, J.; Houbraken, J.; Lombard, L.; et al. Fungal Planet description sheets: 625–715. Pers. -Mol. Phylogeny Evol. Fungi 2017, 32, 270–464. [Google Scholar] [CrossRef]
  253. Crous, S.; Taylor, J.E. Saccharata intermedia. Persoon 2009, 23, 198–199. [Google Scholar]
  254. Quaedvlieg, W.; Verkley, G.J.M.; Shin, H.D.; Barreto, R.W.; Alfenas, A.C.; Swart, W.J.; Groenewald, J.Z.; Crous, P.W. Sizing up septoria. Stud. Mycol. 2013, 75, 307–390. [Google Scholar] [CrossRef] [Green Version]
  255. Hyde, K.D.; Tennakoon, D.S.; Jeewon, R.; Bhat, D.J.; Maharachchikumbura, S.S.N.; Rossi, W.; Leonardi, M.; Lee, H.B.; Mun, H.Y.; Houbraken, J.; et al. Fungal diversity notes 1036–1150: Taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers. 2019, 96, 1–242. [Google Scholar] [CrossRef]
  256. Zhang, Z.B.; Zeng, Q.G.; Yan, R.M.; Wang, Y.; Zou, Z.R.; Zhu, D. Endophytic fungus Cladosporium cladosporioides LF70 from Huperzia serrata produces Huperzine A. World J. Microbiol. Biotechnol. 2011, 27, 479–486. [Google Scholar] [CrossRef]
  257. Tibpromma, S.; Hyde, K.D.; Bhat, J.D.; Mortimer, P.E.; Xu, J.; Promputtha, I.; Doilom, M.; Yang, J.B.; Tang, A.M.C.; Karunarathna, S.C. Identification of endophytic fungi from leaves of Pandanaceae based on their morphotypes and DNA sequence data from southern Thailand. MycoKeys 2018, 33, 25–67. [Google Scholar] [CrossRef] [Green Version]
  258. Bezerra, J.D.P.; Sandoval-Denis, M.; Paiva, L.M.; Silva, G.A.; Groenewald, J.Z.; Souza-Motta, C.M.; Crous, P.W. New endophytic Toxicocladosporium species from cacti in Brazil, and description of Neocladosporium gen. nov. IMA Fungus 2017, 8, 77–97. [Google Scholar] [CrossRef] [PubMed]
  259. Aghdam, S.A.; Fotouhifar, K. Identification of some endophytic fungi of cherry trees (Prunus avium) in Iran. Iran. J. Plant Prot. Sci. 2017, 48, 43–57. [Google Scholar] [CrossRef]
  260. Ali, A.; Bilal, S.; Khan, A.L.; Mabood, F.; Al-Harrasi, A.; Lee, I.J. Endophytic Aureobasidium pullulans BSS6 assisted developments in phytoremediation potentials of Cucumis sativus under Cd and Pb stress. J. Plant Interact. 2019, 14, 303–313. [Google Scholar] [CrossRef] [Green Version]
  261. Patil, M.; Patil, R.; Mohammad, S.; Maheshwari, V. Bioactivities of phenolics-rich fraction from Diaporthe arengae TATW2, an endophytic fungus from Terminalia arjuna (Roxb.). Biocatal. Agric. Biotechnol. 2017, 10, 396–402. [Google Scholar] [CrossRef]
  262. Bills, G.F.; Menéndez, V.G.; Platas, G. Kabatiella bupleuri sp. nov. (Dothideales), a pleomorphic epiphyte and endophyte of the Mediterranean plant Bupleurum gibraltarium (Apiaceae). Mycologia 2012, 104, 962–973. [Google Scholar] [CrossRef]
  263. Silva, A.C.; Henriques, J.; Diogo, E.; Ramos, A.P.; Bragança, H. First report of Sydowia polyspora causing disease on Pinus pinea shoots. For. Pathol. 2020, 50, 27–30. [Google Scholar] [CrossRef]
  264. Pang, K.L.; Hyde, K.D.; Alias, S.A.; Suetrong, S.; Guo, S.Y.; Idid, R.; Gareth Jones, E.B. Dyfrolomycetaceae, a new family in the Dothideomycetes, Ascomycota. Cryptogam. Mycol. 2013, 34, 223–232. [Google Scholar] [CrossRef]
  265. Li, W.L.; Maharachchikumbura, S.S.N.; Cheewangkoon, R.; Liu, J.K. Reassessment of Dyfrolomyces and four new species of Melomastia from Olive (Olea europaea) in Sichuan Province, China. J. Fungi 2022, 8, 76. [Google Scholar] [CrossRef]
  266. Fungi of Great Britain and Ireland. 2021. Available online: https://fungi.myspecies.info/all-fungi/hysterium-angustatum (accessed on 14 April 2022).
  267. Kohlmeyer, J.; Kohlmeyer, E. Marine Fungi from Tropical America and Africa. Mycologia 1971, 63, 831–861. [Google Scholar] [CrossRef]
  268. Heuchert, B.; Braun, U.; Diederich, P.; Ertz, D. Taxonomic monograph of the genus Taeniolella s. lat. (Ascomycota). Fungal Syst. Evol. 2018, 2, 69–261. [Google Scholar] [CrossRef] [Green Version]
  269. Hernández-Restrepo, M.; Bezerra, J.D.P.; Tan, Y.P.; Wiederhold, N.; Crous, P.W.; Guarro, J.; Gené, J. Re-evaluation of Mycoleptodiscus species and morphologically similar fungi. Persoonia Mol. Phylogeny Evol. Fungi 2019, 42, 205–227. [Google Scholar] [CrossRef] [PubMed]
  270. Bao, D.F.; Hyde, K.D.; Luo, Z.L.; Su, H.Y.; Nalumpang, S. Minutisphaera aquaticum sp. nov. increases the known diversity of Minutisphaeraceae. Asian J. Mycol. 2019, 2, 306–314. [Google Scholar] [CrossRef]
  271. Ferrer, A.; Miller, A.N.; Shearer, C.A. Minutisphaera and Natipusilla: Two new genera of freshwater Dothideomycetes. Mycologia 2011, 103, 411–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  272. Mapook, A.; Hyde, K.D.; Dai, D.Q.; Li, J.; Jones, E.B.G.; Bahkali, A.H.; Boonmee, S. Muyocopronales, ord. Nov., (Dothideomycetes, Ascomycota) and a reappraisal of Muyocopron species from northern Thailand. Phytotaxa 2016, 265, 225–237. [Google Scholar] [CrossRef]
  273. Selbmann, L.; De Hoog, G.S.; Zucconi, L.; Isola, D.; Ruisi, S.; Gerrits van den Ende, A.H.G.; Ruibal, C.; De Leo, F.; Urzì, C.; Onofri, S. Drought meets acid: Three new genera in a dothidealean clade of extremotolerant fungi. Stud. Mycol. 2008, 61, 1–20. [Google Scholar] [CrossRef] [PubMed]
  274. Oerke, E.C.; Leucker, M.; Steiner, U. Sensory assessment of Cercospora beticola sporulation for phenotyping the partial disease resistance of sugar beet genotypes. Plant Methods 2019, 15, 133. [Google Scholar] [CrossRef] [Green Version]
  275. Shivas, R.G.; McTaggart, A.R.; Young, A.J.; Crous, P.W. Zasmidium scaevolicola. Fungal Planet 47. Persoonia 2010, 24, 132–133. [Google Scholar]
  276. Farr, D.F.; Miller, M.E.; Bruton, B.D. Rhizopycnis vagum gen. et sp. nov., a New coelomycetous fungus from roots of melons and sugarcane. Mycologia 1998, 90, 290–296. [Google Scholar] [CrossRef]
  277. McKenzie, E. Alternaria alternata (Alternaria alternata). 2013. Available online: http://www.padil.gov.au. (accessed on 20 August 2022).
  278. Tymon, L.S.; Peever, T.L.; Johnson, D.A. Identification and enumeration of small-spored Alternaria species associated with potato in the U.S. Northwest. Plant Dis. 2016, 100, 465–472. [Google Scholar] [CrossRef] [Green Version]
  279. Dai, D.; Bhat, D.J.; Liu, J.; Chukeatirote, E.; Zhao, R.; Hyde, K.D. Bambusicola, a new genus from bamboo with asexual and sexual morphs. Cryptogam. Mycol. 2012, 33, 363–379. [Google Scholar] [CrossRef]
  280. Manamgoda, D.S.; Rossman, A.Y.; Castlebury, L.A.; Crous, P.W.; Madrid, H.; Chukeatirote, E.; Hyde, K.D. The genus Bipolaris. Stud. Mycol. 2014, 79, 221–288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  281. Khiralla, A.; Mohamed, I.E.; Tzanova, T.; Schohn, H.; Slezack-Deschaumes, S.; Hehn, A.; André, P.; Carre, G.; Spina, R.; Lobstein, A.; et al. Endophytic fungi associated with Sudanese medicinal plants show cytotoxic and antibiotic potential. FEMS Microbiol. Lett. 2016, 363, fnw089. [Google Scholar] [CrossRef] [PubMed]
  282. Ahmadpour, A.; Heidarian, Z.; Karami, S.; Tsukiboshi, T.; Zhang, M.; Javan-Nikkhah, M. New species of Bipolaris and Curvularia on grass species in Iran. Rostaniha 2012, 13, 69–82. [Google Scholar]
  283. Boonmee, S.; Ko, T.W.K.; Chukeatirote, E.; Hyde, K.D.; Chen, H.; Cai, L.; McKenzie, E.H.C.; Jones, E.B.G.; Kodsueb, R.; Hassan, B.A. Two new Kirschsteiniothelia species with Dendryphiopsis anamorphs cluster in Kirschsteiniotheliaceae fam. nov. Mycologia 2012, 104, 698–714. [Google Scholar] [CrossRef]
  284. Crous, P.W.; Wingfield, M.J.; Guarro, J.; Sutton, D.A.; Acharya, K.; Barber, P.A.; Boekhout, T.; Dimitrov, R.A.; Dueñas, M.; Dutta, A.K.; et al. Fungal Planet description sheets. Persoonia 2015, 34, 167–266. [Google Scholar] [CrossRef] [PubMed]
  285. Budziszewska, J.; Szypuła, W.; Wilk, M.; Wrzosek, M. Paraconiothyrium babiogorense sp. nov., a new endophyte from fir club moss Huperzia selago (Huperziaceae). Mycotaxon 2011, 115, 457–468. [Google Scholar] [CrossRef]
  286. CEMAS (Center for Asturian Mycological Studies). 2022. Available online: https://www.centrodeestudiosmicologicosasturianos.org/?p=47642 (accessed on 10 May 2022).
  287. Blixt, E.; Djurle, A.; Yuen, J.; Olson, Å. Fungicide sensitivity in Swedish isolates of Phaeosphaeria nodorum. Plant Pathol. 2009, 58, 655–664. [Google Scholar] [CrossRef]
  288. Jiang, S.H.; Wei, X.L.; Wei, J.C. Two new species of Strigula (lichenised Dothideomycetes, Ascomycota) from China, with a key to the Chinese foliicolous species. MycoKeys 2017, 19, 31–42. [Google Scholar] [CrossRef] [Green Version]
  289. Schubert, K.; Rischel, A.; Braun, D.U. A monograph of Fusicladium s.lat. (Hyphomycetes). Schlechtendalia 2013, 9, 1–132. [Google Scholar]
  290. Shen, M.; Zhang, J.Q.; Zhao, L.L.; Groenewald, J.Z.; Crous, P.W.; Zhang, Y. Venturiales. Stud. Mycol. 2020, 96, 185–308. [Google Scholar] [CrossRef]
  291. Ibrahim, M.; Schlegel, M.; Sieber, T.N. Venturia orni sp. nov., a species distinct from Venturia fraxini, living in the leaves of Fraxinus ornus. Mycol. Prog. 2016, 15, 29. [Google Scholar] [CrossRef]
  292. Zhao, G.; Liu, X.; Wu, W. Helicosporous hyphomycetes from China. Fungal Divers. 2007, 26, 313–524. [Google Scholar]
  293. Sati, S.C.; Pathak, R. New root endophytic water borne conidial fungi from Kumaun Himalaya. Curr. Bot. 2017, 8, 12. [Google Scholar] [CrossRef]
Figure 1. Uni-loculate and multi-loculate ascostromata/conidiomata. (a,b) Uni-loculate conidiomata of Dothiorella viticola. (c,d) Uni-loculate ascostromata of Sphaeropsis sp. (e,f) Multi-loculate ascostromata of Aplosporella thailandica [36]. Scale bars: (a,c,d) = 200 μm, b = 100 μm, (e,f) = 500 μm.
Figure 1. Uni-loculate and multi-loculate ascostromata/conidiomata. (a,b) Uni-loculate conidiomata of Dothiorella viticola. (c,d) Uni-loculate ascostromata of Sphaeropsis sp. (e,f) Multi-loculate ascostromata of Aplosporella thailandica [36]. Scale bars: (a,c,d) = 200 μm, b = 100 μm, (e,f) = 500 μm.
Jof 09 00184 g001
Figure 2. Conidial and ascospore colour and septation. (a) Hyaline and aseptate conidia of Lasiodiplodia sp. (b) Hyaline and aseptate conidia of Botryosphaeria dothidea. (c) Brown and aseptate conidia of Aplosporella thailandica [36]. (d) Brown and septate conidia of Dothiorella viticola. (e) Brown and aseptate ascospores of Sphaeropsis sp. (f) Hyaline and aseptate ascospore of Botryosphaeria fabicerciana. (g) Hyaline and aseptate ascospore of Neofusicoccum parvum. (h) Brown and aseptate ascospore of Barriopsis archontophoenicis. (i) Wing-like appendages of Neodeightonia palmicola ascospore (in water). (j) Neodeightonia palmicola ascospore in 100% lactic acid. Scale bars: (a,d,e) = 20 μm, (b,c,fj) = 10 μm.
Figure 2. Conidial and ascospore colour and septation. (a) Hyaline and aseptate conidia of Lasiodiplodia sp. (b) Hyaline and aseptate conidia of Botryosphaeria dothidea. (c) Brown and aseptate conidia of Aplosporella thailandica [36]. (d) Brown and septate conidia of Dothiorella viticola. (e) Brown and aseptate ascospores of Sphaeropsis sp. (f) Hyaline and aseptate ascospore of Botryosphaeria fabicerciana. (g) Hyaline and aseptate ascospore of Neofusicoccum parvum. (h) Brown and aseptate ascospore of Barriopsis archontophoenicis. (i) Wing-like appendages of Neodeightonia palmicola ascospore (in water). (j) Neodeightonia palmicola ascospore in 100% lactic acid. Scale bars: (a,d,e) = 20 μm, (b,c,fj) = 10 μm.
Jof 09 00184 g002
Figure 3. Phylogram generated from ML analysis based on combined LSU and ITS sequence data. ML and MP bootstrap support values ≥ 60% and Bayesian posterior probabilities (PP) ≥ 0.90 are mentioned at the nodes as ML/MP/PP. Strain numbers are noted at the end of the species name. The tree is rooted to Helicosporium guianense (CBS 269.52) and Helicomyces roseus (CBS 283.51).
Figure 3. Phylogram generated from ML analysis based on combined LSU and ITS sequence data. ML and MP bootstrap support values ≥ 60% and Bayesian posterior probabilities (PP) ≥ 0.90 are mentioned at the nodes as ML/MP/PP. Strain numbers are noted at the end of the species name. The tree is rooted to Helicosporium guianense (CBS 269.52) and Helicomyces roseus (CBS 283.51).
Jof 09 00184 g003aJof 09 00184 g003bJof 09 00184 g003cJof 09 00184 g003d
Figure 4. Maximum clade credibility (MCC) tree for LSU and ITS sequence data using a GTR+G+I nucleotide substitution model. The tree was calibrated by setting the crown age of Botryosphaeriales at 110 Mya. Values at the nodes are given in millions of years and the blue bars indicate standard deviations.
Figure 4. Maximum clade credibility (MCC) tree for LSU and ITS sequence data using a GTR+G+I nucleotide substitution model. The tree was calibrated by setting the crown age of Botryosphaeriales at 110 Mya. Values at the nodes are given in millions of years and the blue bars indicate standard deviations.
Jof 09 00184 g004aJof 09 00184 g004bJof 09 00184 g004cJof 09 00184 g004dJof 09 00184 g004e
Figure 5. Diagram representing the evolution of families in Botryosphaeriales with crown age and stem age.
Figure 5. Diagram representing the evolution of families in Botryosphaeriales with crown age and stem age.
Jof 09 00184 g005
Figure 6. Nutritional modes recorded in Botryosphaeriales taxa.
Figure 6. Nutritional modes recorded in Botryosphaeriales taxa.
Jof 09 00184 g006
Figure 7. Ancestral character state analysis for nutritional mode (left) and conidial colour and septation (right) in Botryosphaeriales, using Bayesian Binary MCMC approaches. Pie charts at terminals show the most likely states (MLS) only and the internal nodes represent the marginal probabilities for each ancestral area.
Figure 7. Ancestral character state analysis for nutritional mode (left) and conidial colour and septation (right) in Botryosphaeriales, using Bayesian Binary MCMC approaches. Pie charts at terminals show the most likely states (MLS) only and the internal nodes represent the marginal probabilities for each ancestral area.
Jof 09 00184 g007aJof 09 00184 g007bJof 09 00184 g007cJof 09 00184 g007d
Figure 8. Genera with pigmented conidia and their nutritional modes.
Figure 8. Genera with pigmented conidia and their nutritional modes.
Jof 09 00184 g008
Table 1. Ascospore and conidial morphology (colour and septation) in Botryosphaeriales families.
Table 1. Ascospore and conidial morphology (colour and septation) in Botryosphaeriales families.
Character AplosporellaceaeBotryosphaeriaceaeMelanopsaceaePhyllostictaceaePlanistromellaceaeSaccharataceaeReferences
ColourAscosporePigmented [3,4,7,36,49]
Hyaline
ConidiaPigmented [3,4,50]
Hyaline
SeptationAscosporeSeptate [7]
Aseptate
ConidiaSeptate [7,11,19,50]
Aseptate
Table 2. Parameters of each character used in ancestral state reconstructions.
Table 2. Parameters of each character used in ancestral state reconstructions.
CharacterParameter
Conidial colourHyaline (A), pigmented (B) and no asexual morph recorded (C)
Conidial septationAseptate (A), septate (B) and no asexual morph recorded (C)
Nutritional modeSaprobes (A), pathogens (B) and endophytes (C)
Table 3. Divergence times of crown age and stem age of families of Botryosphaeriales.
Table 3. Divergence times of crown age and stem age of families of Botryosphaeriales.
FamilyDivergence Times of Crown
Age (Mya)
Divergence Times of Stem
Age (Mya)
Aplosporellaceae42.8 (20.1–68.9)72.4 (46.9–101.2)
Botryosphaeriaceae69.9 (50.5–89.5)81.1 (60.9–102.1)
Melanopsaceae16.8 (5.1–36.8)72.9 (49.3–95.7)
Phyllostictaceae68. 6 (48.4–88.4)81.1 (60.9–102.1)
Planistromellaceae53.9 (34.5–72.7)72.9 (49.3–95.7)
Saccharataceae52.9 (31.3–79.5)72.4 (46.9–101.2)
Table 4. Details of the divergence times of crown age and stem age of Botryosphaeriales families in different studies.
Table 4. Details of the divergence times of crown age and stem age of Botryosphaeriales families in different studies.
Study Slippers et al. [4]Liu et al. [70]Phillips et al. [7]This Study
No. of taxa 140364100306
Gene regions SSU, LSU, ITS, tef1, β-tubulin and mtSSU (mitochondrial ribosomal small subunit)LSU, SSU, tef1 and rpb2ITS and LSUITS and LSU
Calibration/s Mean = 0.000113
(SD = 0.000006)
Mean = 582.5 Mya
(SD = 50.15 Mya)
Fossil data
100 Mya
(SD = 150 Mya) fossil Metacapnodiaceae
Mean = 110 Mya
(SD = 5 Mya)
Mean = 110 Mya (SD = 5 Mya)
Divergence time of crown age
(Mya)
Aplosporellaceae--4043
Botryosphaeriaceae44446170
Melanopsaceae--Not estimated17
Phyllostictaceae26276369
Planistromellaceae38255254
Saccharataceae-285053
Divergence time of stem age
(Mya)
Aplosporellaceae57-9472
Botryosphaeriaceae87529481
Melanopsaceae75-7473
Phyllostictaceae87508181
Planistromellaceae75858173
Saccharataceae-1147472
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Rathnayaka, A.R.; Chethana, K.W.T.; Phillips, A.J.L.; Liu, J.-K.; Samarakoon, M.C.; Jones, E.B.G.; Karunarathna, S.C.; Zhao, C.-L. Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes. J. Fungi 2023, 9, 184. https://doi.org/10.3390/jof9020184

AMA Style

Rathnayaka AR, Chethana KWT, Phillips AJL, Liu J-K, Samarakoon MC, Jones EBG, Karunarathna SC, Zhao C-L. Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes. Journal of Fungi. 2023; 9(2):184. https://doi.org/10.3390/jof9020184

Chicago/Turabian Style

Rathnayaka, Achala R., K. W. Thilini Chethana, Alan J. L. Phillips, Jian-Kui Liu, Milan C. Samarakoon, E. B. Gareth Jones, Samantha C. Karunarathna, and Chang-Lin Zhao. 2023. "Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes" Journal of Fungi 9, no. 2: 184. https://doi.org/10.3390/jof9020184

APA Style

Rathnayaka, A. R., Chethana, K. W. T., Phillips, A. J. L., Liu, J. -K., Samarakoon, M. C., Jones, E. B. G., Karunarathna, S. C., & Zhao, C. -L. (2023). Re-Evaluating Botryosphaeriales: Ancestral State Reconstructions of Selected Characters and Evolution of Nutritional Modes. Journal of Fungi, 9(2), 184. https://doi.org/10.3390/jof9020184

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop