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Review

A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes

by
Laura Gioia
1,*,
Giada d’Errico
1,*,
Martina Sinno
1,
Marta Ranesi
1,
Sheridan Lois Woo
2,3,4 and
Francesco Vinale
4,5
1
Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy
2
Department of Pharmacy, University of Naples Federico II, 80131 Naples, Italy
3
Task Force on Microbiome Studies, University of Naples Federico II, 80128 Naples, Italy
4
National Research Council, Institute for Sustainable Plant Protection, 80055 Portici, Italy
5
Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, 80137 Naples, Italy
*
Authors to whom correspondence should be addressed.
Agriculture 2020, 10(12), 643; https://doi.org/10.3390/agriculture10120643
Submission received: 31 October 2020 / Revised: 7 December 2020 / Accepted: 11 December 2020 / Published: 17 December 2020
(This article belongs to the Special Issue Occurrence and Functions of Endophytic Fungi in Crop Species)
Versions Notes

Abstract

:
An extensive literature search was performed to review current knowledge about endophytic fungi isolated from plants included in the European Food Safety Authority (EFSA) dossier. The selected genera of plants were Acacia, Albizia, Bauhinia, Berberis, Caesalpinia, Cassia, Cornus, Hamamelis, Jasminus, Ligustrum, Lonicera, Nerium, and Robinia. A total of 120 fungal genera have been found in plant tissues originating from several countries. Bauhinia and Cornus showed the highest diversity of endophytes, whereas Hamamelis, Jasminus, Lonicera, and Robinia exhibited the lowest. The most frequently detected fungi were Aspergillus, Colletotrichum, Fusarium, Penicillium, Phyllosticta, and Alternaria. Plants and plant products represent an inoculum source of several mutualistic or pathogenic fungi, including quarantine pathogens. Thus, the movement of living organisms across continents during international trade represents a serious threat to ecosystems and biosecurity measures should be taken at a global level.

1. Introduction

Endophytic fungi are ubiquitous to plants, and are mainly members of Ascomycota or their mitosporic stage, but they also include some taxa of Basidiomycota, Zygomycota, and Oomycota. Endophytes are organisms living within the tissues of plants [1] establishing stable relationships with their host, ranging from non-pathogenic to beneficial [2,3]. The endophytic fungi communities represent an enormous reserve of biodiversity and constitute a rich source of bioactive compounds used in agriculture [4,5]. For these reasons, they have attracted the attention of the scientific community worldwide. By definition, all or at least a significant part of the endophytic fungi life cycle occurs within the plant tissues without causing symptoms to their host [6,7,8]. A wide range of fungi, including pathogens and saprophytes, may be endophytes. Several pathogens live asymptomatically within plant tissues during their latency or quiescent stage, while some saprobes can also be facultative parasites [1,8,9]. Fungal endophytes are influenced by abiotic and biotic factors, occupying different habitats and locations during their life cycle phases. Even if host plants do not show any symptoms, they may represent a source of inoculum for other species [10,11,12,13]. Furthermore, changes in environmental conditions or species hosts may modify the fungal behavior, thus producing disease symptoms [8,11,14]. Large quantities of plants and plant material that are globally traded might contain asymptomatic infections of these fungi. It is generally accepted that the movement of plants and plant products by global trade and human activities is the most common way to introduce exotic pathogens and pests in non-endemic countries. Plant health is increasingly threatened by the introduction of emerging pests and/or pathogens [15,16]. Noticeable examples are represented by the invasion of alien plant pathogens into new areas [17,18,19]. Generally, biological invasions are the main threat to biodiversity [20], causing a decrease in species richness and diversity [20,21] or affecting local biological communities [22], as well as changing ecosystem processes [23,24,25].
In this scenario, the European Food Safety Authority (EFSA) Panel on Plant Health is responsible for the risk assessment, evaluations of risk reduction options, as well as guidance documents [26] in the domain of plant health for the European Union (EU) [26,27]. Commission Implementing Regulation (EU) [28] prohibits the importation of 35 so-called ‘High-Risk Plants, plant products and other objects’ from all third (non-EU) countries as long as no full risk assessment has been carried out. The EFSA Panel on Plant Health was requested to prepare and deliver risk assessments for these commodities [27,28], to evaluate whether the plant material will remain prohibited or removed from the list, with or without the application of additional measures [27,29]. The Commodity Risk Assessment has to be performed on the basis of technical dossiers provided by National Plant Protection Organizations of third countries. Information required for the preparation and submission of technical dossiers includes data on the pests potentially associated with the plant species or genera and on phytosanitary mitigation measures and inspections [30,31].
These plants have been identified as ‘High-Risk Plants’ by the EU since they ‘host commonly hosted pests known to have a major impact on plant species which are of major economic, social or environmental importance to the Union’ [28]. However, among these 35 plant genera, within the meaning of Art. 42 of Regulation (EU) 2016/2031, a list of only 13 taxa have been selected by the EFSA as plants mostly traded for ornamental purposes. According to this list, we have reviewed the following genera: Acacia Mill., Albizia Durazz., Bauhinia L., Berberis L., Caesalpinia L., Cassia L., Cornus L., Hamamelis L., Jasminus L., Ligustrum L., Lonicera L., Nerium L., and Robinia L. In this article, as much as possible, we highlight the potential risks associated with the movement of plants or materials among nations. Although other plant species may also have a significant impact, this review is limited to plants included in EU regulation [28] that do not originate within Europe. Thus, given these perspectives for future assessments, the present investigation offers an up-to-date snapshot of endophytic fungi associated with the so-called ‘High-Risk Plants for ornamental purpose’. The aim is to facilitate the information required for technical dossiers, needed by the EFSA to perform the Commodity Risk Assessment of 13 plants mandated on an EU import list.

2. Endophytic Fungi Occurring in Selected Plants

Table 1 summarizes the abundance of endophytic fungi reported in association with High-Risk Plants for ornamental purposes. Herein, the number of endophytic species found in association with the examined plant genera has been taxonomically grouped by fungal genus. There are important differences in terms of fungi recovered per specific plant genus (SP) as well as in the frequency of a specific fungal genus (SF). These discrepancies could be explained by the different availability of literature data on these specific plants.

2.1. Acacia

The Acacia, commonly known as wattle, belongs to the family Mimosaceae. The genus comprises more than 1350 species found throughout the world: almost 1000 are native of Australia, up to 140 species occur in Africa, 89 from Asia, and about 185 species are found in North and South America. Some Australian wattles are naturalized beyond their native range and have become invasive in many parts of Europe, South Africa, and Florida, especially in conservation areas [32]. Aboriginal communities use some Acacia species as sources of food and medicine. Australian acacias are widely used as wood products, ornamental plants, commercial cut flowers, and perfume crops [33].
Endophytic occurrence (Table 2) has been reported for 61 fungal isolates belonging to genera Lasiodiplodia (7 isolates), Dothiorella (8 isolates), Neofusicoccum (9 isolates), Aspergillus (3 isolates), Chaetomium (3 isolates), Botryosphaeria (1 isolate), Colletotrichum (2 isolates), Aureobasidium (2 isolates), Spencermartinsia (2 isolates), Alternaria (1 isolate), Cochliobolus (1 isolate), Diplodia (2 isolates), Eupenicillium (1 isolate), Fusarium (1 isolate), Moesziomyces (1 isolate), Paraphaeosphaeria (1 isolate), Penicillium (2 isolates), Eutiarosporella (2 isolates), Pestalotia (1 isolate), Peyronellaea (1 isolate), Phaeobotryosphaeria (1 isolate), Phoma (2 isolates), Phyllosticta (1 isolate), Wickerhamomyces (1 isolate), Preussia (1 isolate), Rhizopus (1 isolate), Oblongocollomyces (1 isolate), Trichoderma (1 isolate), and Xylaria (1 isolate). Plant host tissues were collected in Egypt, China, India, Australia, South Africa, La Réunion (France), France, USA, and Hawaii.

2.2. Albizia

The genus Albizia (Mimosaceae) comprises almost 150 species, mostly trees and shrubs native to tropical and subtropical regions of Asia and Africa. They are common components of timber plantations, cropping, and livestock production systems [45]. Albizia synthesizes numerous bioactive compounds with pharmacological properties such as saponins, alkaloids, flavonoids, and phenolics [45]. The species A. lebbeck has been extensively introduced in seasonally dry tropical regions of Africa, Asia, the Caribbean, and South America, mainly as an ornamental plant, and has become naturalized in many areas [46].
Table 3 reports endophytes isolated from Albizia genera. These fungi belong to 14 different genera, most of them found in leaves and twigs of A. lebbeck originating from Iraq, India, Indonesia, and Egypt. Isolated fungi included different species of Aspergillus (9 isolates), which are dominant in comparison to other genera, followed by Fusarium (4 isolates), Penicillium (3 isolates), and Paecilomyces (2 isolates). One isolate for each of the following genera Neocosmospora, Bipolaris, Colletotrichum, Diaporthe, Lasiodiplodia, Rosellinia, Acremonium, Trichoderma, Verticillium, Curvularia, and Nigrospora has been detected.

2.3. Bauhinia

The genus Bauhinia, commonly known as the orchid tree, belongs to the family Fabaceae. It comprises more than 500 species of shrubs, and small trees mostly native to tropical countries (Africa, Asia, and South America). Many species are widely used as ornamental plants, forage, human food, and in folk medicine [51,52].
A total of 107 fungal endophytes have been found in Bauhinia plant tissues (Table 4). The most common fungi reported were: Aspergillus (13 isolates), Curvularia (8 isolates), Penicillium (7 isolates), Nigrospora (7 isolates), Fusarium (5 isolates), Phoma (3 isolates), Cladosporium (4 isolates), Acremonium (3 isolates), Colletotrichum (3 isolates), Phomopsis (3 isolates), Cochliobolus (3 isolates), and Exserohilum (3 isolates). Furthermore, other genera were found less frequently: Myrothecium (2 isolates), Gibberella (2 isolates), Lasiodiplodia (2 isolates), Khuskia (1 isolate), Nodulisporium (2 isolates), Pestalotiopsis (2 isolates), Alternaria (2 isolates), Gibberella (2 isolates), Pithomyces (1 isolate), Diplococcium (2 isolates), Dothiorella (2 isolates), Ascotricha (2 isolates), Talaromyces (2 isolates), Trichoderma (2 isolates), Spegazzinia (2 isolates), Kiflimonium (1 isolate), Geotrichum (1 isolate), Corynespora (1 isolate), Diaporthe (1 isolate), Glomerella (1 isolate), Pestalotia (1 isolate), Scedosporium (1 isolate), Botrytis (1 isolate), Sporormiella (1 isolate), Phyllosticta (1 isolate), Lasmenia (2 isolates), Albifimbria (1 isolate), Myrmecridium (2 isolates), Sphaeria (1 isolate), Paraboeremia (1 isolate), Pseudopithomyces (1 isolate), Chaetomium (1 isolate), and Torulomyces (1 isolate). All host plants, namely B. fortificata, B. brevipes, B. racemosa, B. guianensis, B. monandra, B. malabarica, B. phoenicea, and B. vahlii, were from Brazil and India.

2.4. Berberis

The genus Berberis (Berberidaceae) comprises almost 500 species of deciduous or evergreen shrubs, which occur in the temperate and subtropical regions of Europe, Asia, Africa, and America [67]. This genus has remarkable pharmacological properties [68]. Berberine and Berbamine are the main compounds produced by these plants, together with alkaloids, tannins, phenolic compounds, sterols, and triterpenes [69].
Numerous endophytic fungi belonging to 19 genera have been isolated from tissues of Berberis from India, China, Kenya, and the USA (Table 5). Isolated fungi included different species of Fusarium (4 isolates) and Colletotrichum (4 isolates), followed by Alternaria (4 isolates), Anguillospora (1 isolate), Phomopsis (1 isolate), Campylospora (1 isolate), Cercospora (1 isolate), Clonostachys (1 isolate), Heliscus (1 isolate), Diaporthe (2 isolates), Microsphaeropsis (1 isolate), Phyllosticta (1 isolate), Paraphalosphaera (1 isolate), Prathoda (1 isolate), Bacillispora (1 isolate), Neocosmospora (1 isolate), Aspergillus (1 isolate), Myrothecium (1 isolate), and Puccinia (1 isolate).

2.5. Caesalpinia

The genus Caesalpinia (Fabaceae) includes approximately 200 species, mainly arboreal and shrubby species, distributed in seasonally dry tropical forests, as well as in tropical and warm temperate savannas, tropical wet forests, and tropical coastal habitats [75]. Several classes of compounds, mainly flavonoids, diterpenes, and steroids, have been isolated from Caesalpinia species, which have shown various medicinal properties [75]. The most common species cultivated as ornamental plants are C. pulcherrima and C. echinata.
A total of 44 fungal endophytes were isolated from leaves, stems, and bark of plants collected from India, Brazil, and Indonesia (Table 6). Fungal genera associated with different species of Caesalpinia were: Aspergillus (10 isolates), followed by Trichoderma (6 isolates) and Fusarium (4 isolates). Other isolated endophytes have been identified as Penicillum (3 isolates), Curvularia (2 isolates), Nectria (2 isolates), Bipolaris (2 isolates), Xylaria (2 isolates), and one isolate for the genera Alternaria, Chrysosporium, Cladosporium, Colletotrichum, Epicoccum, Geotrichum, Helminthosporium, Lasiodiplodia, Talaromyces, Scopulariopsis, and Phyllosticta, respectively.

2.6. Cassia

The genus Cassia (Fabaceae) comprises about 600 species native to tropical and subtropical regions of Southeast Asia, Africa, Northern Australia, and Latin America [82,83]. In particular, C. fistula and C. alata are distributed worldwide and used as ornamental and medicinal plants for their biological and pharmacological properties [82,83,84]. Some investigations on phytochemicals of Cassia revealed that it comprises compounds like anthraquinones, alkaloids, catechols, flavonoids, phenolic compounds, saponins, steroids, tannins, and triterpenoids [83,84,85,86].
Nineteen endophytic fungi have been isolated from different tissues of Cassia species from Thailand, India, Malaysia, and Brazil (Table 7): Aspergillus (2 isolates), Nodulisporium (2 isolates), Penicillium (2 isolates), Phomopsis (2 isolates), Daldinia (1 isolate), Coprinus (1 isolate), Guignardia (1 isolate), Hypoxylon (1 isolate), Nemania (1 isolate), Nigrospora (1 isolate), Papulospora (1 isolate), Periconia (1 isolate), Xylaria (1 isolate), Psathyrella (1 isolate), and Thielaoviopsis (1 isolate).

2.7. Cornus

The genus Cornus (Cornaceae) consists of over 50 species of woody plants, many of which are cultivated as ornamental and medicinal trees [93]. The most widespread ornamental plants of the genus are C. florida and C. stolonifera, called the flowering dogwood, native to northern and central America [93]. The species C. officinalis is widely distributed in China, Korea, and Japan, and used for its several pharmacological activities. Among bioactive compounds, iridoids, tannins, and flavonoids are the major components [94].
About 90 fungal endophytes have been isolated and identified from C. alba, C. alternifolia, C. stolonifera, C. controversa, and C. officinalis collected in Canada, USA, Japan, China, and Korea (Table 8): Penicillium (8 isolates), Fusarium (4 isolates), Cladosporium (5 isolates), Colletotrichum (5 isolates), Alternaria (6 isolates), Pestalotiopsis (5 isolates), Aureobasidium (4 isolates), Botryosphaeria (3 isolates), Cryptodiaporthe (2 isolates), Phomopsis (3 isolates), Talaromyces (4 isolates), Aspergillus (3 isolates), Discula (4 isolates), Diaporthe (3 isolates), Neonectria (2 isolates), Trichoderma (2 isolates), Tubakia (2 isolates), and Didymella (3 isolates). Only one isolate of the following genera has been reported: Ascochyta, Botrytis, Cyrptosporiopsis, Elsinoe, Epicoccum, Helminthosporium, Lecanicillium, Leptosphaerulina, Lophiostoma, Drepanopeziza, Nigrospora, Sarocladium, Cordyceps, Phyllosticta, Phytophthora, Phoma, Pleuroceras, Thelonectria, Sclerotinia, Neofabraea, Septoria, Simplicillium, Stenella, Verticillium, and Xylaria.

2.8. Hamamelis

Hamamelis (Hamamelidaceae), commonly known as witch hazel, comprises six species of ornamental shrubs. This genus is distributed across North America and eastern Asia. Bark extracts contain proanthocyanidins and polyphenolic fractions, with medicinal properties [107,108].
Fungal endophytes belonging to genera Colletotrichum, Nigrospora, Pezicula, and Phyllosticta have been isolated from Hamamelis plant tissues in the USA, China, Netherlands, Canada, and Japan (Table 9).

2.9. Jasminum

The genus Jasminum (Oleaceae) includes more than 200 species distributed in China, Africa, Asia, Australia, South Pacific Islands, and Europe. Jasmines are widely cultivated for ornamental, medical, and cosmetical uses. The species J. sambac, commonly known as Arabian Jasmine, is cultivated throughout India and tropical regions. This genus has been reported for several uses due to the following pharmaceutical activities: antimicrobial [115], antioxidant [116], antidiabetic [117], antiviral [118], and antitumor [119]. Seven species of endophytic fungi of the genus Colletotrichum have been reported from J. sambac in India and Vietnam (Table 10).

2.10. Ligustrum

Ligustrum (Family Oleaceae) is a genus of about 50 species of shrubs and trees from warm areas of Europe to Asia [122]. Several species of the genus have been cultivated in many areas of the world as urban ornamental hedge and street trees. In particular, the most widespread species L. lucidum compete with and inhibit the regeneration of native flora, becoming invasive in many areas with a subtropical and temperate climate, such as North America, South America, Europe, Asia, Africa, and Oceania [123]. Due to its active constituents such as glycosides, flavonoids, phenylpropanoids, phenylethanoid, and terpenoids, Ligustrum spp. have been widely used as a health remedy in European, Chinese, and Japanese communities [124,125].
Collected data showed that 29 species of endophytes belonging to 20 genera have been found in plant tissues of L. lucidum, L. compactum, L. quihoui, L. obsusifoilium, and L. vulgare (Table 11): Guignardia (3 isolates), Alternaria (2 isolates), Colletotrichum (3 isolates), Fusarium (2 isolates), Xylaria (2 isolates), Pestalotiopsis (1 isolate), Trichoderma (2 isolates), Lasiodiplodia (2 isolates), Phomopsis (3 isolates), and one isolate of Diplodia, Geotrichum, Libertella, Neocosmospora, Cladosporium, Peroneutypa, Penicillium, Phyllosticta, Pycnidiella, and Rhizopus, respectively.

2.11. Lonicera

Lonicera (Caprifoliaceae) is a genus that comprises more than 150 species of shrubs and twining climbers, occurring in North America, South Europe, North Africa, Philippines, and Malaysia [134]. L. japonica and L. morrowii, which are native to Asia, are ornamental species distributed in many areas of the world. In the USA, they are considered invasive plants [135]. Only 3 fungal species have been found to grow as endophytes in Lonicera plant tissues (Table 12): Fusarium sp., Phyllosticta sp., and Guignarda mangiferae.

2.12. Nerium

N. oleander, commonly called oleander, is the only species currently classified in the genus Nerium (Family Apocynaceae). This evergreen shrub is native or naturalized to a wide area, from the Mediterranean region to the Arabian Peninsula and Asia [137]. Several biologically active compounds have been reported in the bark (cardenolides, triterpenoidal saponins, oleanderol, rutin, dambonitol in leaves, odorosides), roots (triterpene, steroidal cardenolide, volatile oil, stearic acid, oleic acid), and flowers (gitoxigenin, uzarigenin, strospeside, odoroside H) [137,138,139,140].
Collected data showed that 38 fungi were isolated from leaves, stems, flowers, and roots of plants collected in India and China (Table 13). These isolates belong to the genera, Fusarium (4 isolates), Penicillium (4 isolates), Cladosporium (3 isolates), Chaetomium (3 isolates), Colletotrichum (3 isolates), Aspergillus (3 isolates), Curvularia (2 isolates), Alternaria (2 isolates), Cylindrocephalum (1 isolate), Lasiodiplodia (1 isolate), Torula (1 isolate), Phyllosticta (1 isolate), Phoma (1), Rhizopus (1 isolate), Geomyces (1 isolate), Pseudothielavia (1 isolate), Trichoderma (1 isolate), Xylaria (1 isolate), Bipolaris (1 isolate), Cochliobolus (1 isolate), and Drechslera (1 isolate).

2.13. Robinia

Robinia is a genus of flowering plants of the family Fabaceae. R. pseudoacacia, called black locust, grows naturally on a wide range of sites. It is considered to be one of the 40 most invasive woody species all over the world [147] and it is included in the invasive alien species list of the EU [148,149]. It is used for many purposes, such as ornamental plant, for shelterbelts, land reclamation, fuelwood, and pulp production [147]. Six species of endophytic fungi were isolated from R. pseudoacacia in Germany, Slovakia, Hungary, and China (Table 14).

3. An Overview of Fungal Diversity and Frequency

Investigations on the mycobiota of plants frequently reported new taxa or new species distribution, and several fungi are still undiscovered or undetected. Numerous higher plants have developed a variety of resistance mechanisms to prevent fungal infections. However, the presence of weakly pathogenic fungi in healthy plant tissues highlights the evolutionary continuum between latent pathogens and symptomless endophytes [15]. Generally, all plants have symbiotic interactions with fungal endophytes which can influence host performance in terms of disease resistance [154,155,156], stress tolerance [157], and biomass accumulation [158]. Fungal endophytes may also change according to plant tissues colonized [159], phenological growth stages, host genotypes [160], and geographical distribution areas [161].
In this review, a total of 428 endophytic species belonging to 122 fungal genera have been found in association with 13 plant genera (Table 1). The greatest level of fungal diversity was reported in in association with Bauhinia with 43 fungal genera and 94 fungal species, and Cornus with 44 fungal genera and 78 fungal species. The degree of fungal recovery from Acacia (29 genera, 51 species), Albizia (14 genera, 27 species), Berberis (17 genera, 29 species), Caesalpinia (19 genera, 42 species), Cassia (15 genera, 19 species), Ligustrum (20 genera, 29 species), and Nerium (21 genera, 37 species) was nearly half in comparison to the abundance noted in the genera Bauhinia and Cornus. Nonetheless, the lowest diversity showed for Hamamelis (4 species/genera), Jasminus (7 species, 1 genera), Lonicera (3 species/genera), and Robinia (6 species/genera) was also due to the lack of published research about fungal endophytes in these plant genera.
The literature evidenced that several fungal endophytes live in association with the investigated plants. The most representative genera in terms of abundance of isolated species were Aspergillus (40 spp.), Penicillium (30), Fusarium (29), Colletotrichum (27), Alternaria (14), and Cladosporium (14). These genera include ubiquitous and generalist fungi as well as several plant pathogens and saprobes [162,163,164].
It is worth noting the relative homogeneity in distribution of fungi such as Colletotrichum, Fusarium, and Alternaria among these plant genera. In fact, Colletotrichum was undetected only in Lonicera and Robinia, Fusarium in Caesalpinia, and Hamamelis, Jasminus, and Alternaria in Cassia and Lonicera. Although scarcely abundant, the fungal genus Phyllosticta was almost reported for all selected plants except for Albizia, Jasminus, Robinia, and Hamamelis. Other endophytic fungi were detected more occasionally. Future surveys may reveal the presence of additional fungal species also from less investigated plants, such as Robinia, Jasminum, and Lonicera.
The presence of pathogenic or saprotrophic fungi has already been discussed by several authors [165,166]. Table 1 shows that several of the listed fungi were apparently restricted to a single plant genus or at least exhibit some preference for a particular one. Some common and ubiquitous pathogens have been recovered in more than one plant host. This is the case of F. oxysporum (8 host plant species belonging to 7 different genera), A. alternata, A. niger, C. gloeosporioides (7 host plant species), N. oryzae (4 host plant species), B. dothidea, C. globosum, C. acutatum (3 host plant species), A. ochraceus, A. pullulans, and C. truncatum (3 host plant species).

4. The Most Common Plant Pathogens

The most frequent endophytes detected from the investigated plants are cosmopolitan and ubiquitous pathogens that may cause severe yield losses. In detail, F. oxysporum is responsible for the wilt of vascular tissues on numerous crops that may result in plant death, even if several strains have proved to be non-pathogenic [167]. It has been isolated from 8 different plant species belonging to 7 genera, namely A. hindsii, A. julibrissin, B. malabarica, B. phoenicea, B. aristata, C. officinalis, L. lucidum, and N. oleander. The fungus A. alternata may infect over 380 host plant species causing leaf spots, rots, and blights. It includes opportunistic forms in developing field crops as well as saprophytic strains that may cause harvest and post-harvest spoilage of harvested products. One of the major concerns represented by its infection is related to the production of mycotoxins that may be introduced in the food chain [168]. In this review, A. alternata has been found in association with 3 genera, in 7 plant species (B. malabarica, B. racemosa, B. poiretii, B. aristata, Cornus sp., L. lucidum, and C. pulcherrima). The saprophytic pathogen A. niger is responsible for the spoilage of a wide range of fruit, vegetable, and food products. It is also the causal agent of the black rot of onion bulbs, the kernel rot of maize, and the black mold rot of cherry [169,170]. It has been found within plant tissues of A. arabica, A. lebbeck, B. fortificata, B. malabarica, B. racemosa, C. pulcherrima, and N. oleander (7 plant species or 4 genera). Furthermore, three different species of Colletotrichum have been isolated from reviewed plants. C. gloeosporioides has been isolated from 7 plant species (3 genera), namely A. hindsii, B. racemosa, B. aristata, C. echinata, C. officinalis, C. stolonifera, and L. lucidum, whereas C. acutatum has been found in Cornus spp., Hamamelis sp., and H. virginiana (3 species; 2 genera). Both Colletotrichum species may cause severe fruit rot mainly occurring in pre- and post-harvest [171]. Moreover, C. truncatum, the causal agent of anthracnose disease affecting several leguminous crops [171], has been collected from 2 plant genera, namely A. hindsii and J. sambac. Furthermore, C. lunata, was isolated from the tissues of 4 plant species (2 genera), including B. malabarica, B. racemosa, B. phoenicea, and C. sappan, is the causal agent of seed and seedling blight in several crops, such as rice, millet, sugarcane, and rice, and of maize leaf spot [172]. Besides, B. dothidea reported in association with A. karroo, Cornus sp., and C. officinalis may cause cankers, dieback, fruit rot, and blue stain in woody plants, including Acacia, Eucalyptus, Vitis, and Pistachio [12]. Concerning the species F. lateritium, it has been extensively investigated as the causal agent of chlorotic leaf distortion on sweet potato (Ipomoea batatas) in the USA [173]. This fungus has been isolated from three different plant species and genera (B. aristata, C. controversa, and L. lucidum). Moreover, the common soil-borne fungus G. candidum, found in association with B. vahlii, C. sappan, and L. lucidum, is the causal agent of sour-rot of tomatoes and citrus fruits, and it is also one of the most economically important post-harvest diseases of citrus [174]. Also, C. cladosporioides, detected in B. racemosa, C. echinata, and C. stolonifera, is the causal agent of blossom blight in strawberries [175]. Other pathogenic fungi associated with these selected plants are less widespread and some of them are subjected to containment measures in some countries. This is the case of N. parvum, N. oryzae, L. theobromae, and D. destructiva. In particular, N. parvum, isolated as an endophyte in three Acacia species (A. heterophylla, A. karroo, and A. koa), is one of the most aggressive causal agent of Botryosphaeria dieback on the grapevine and it is known as an aggressive polyphagous pathogen attacking more than 100 plant hosts [176]. Also, N. oryzae, reported from H. mollis, B. phoenicea, B. racemosa, and B. fortificata, may reduce plant growth and seed quality of rice plants as well as Brassica spp., maize, and cotton [177]. Moreover, L. theobromae, found in association with six different plant species (A. karroo, A. koa, B. racemosa, C. echinata, L. lucidum, and N. oleander), is the causal agent of dieback, root rot, and blights for a wide range of plant hosts, mainly located in tropical and subtropical regions [178]. Finally, D. desctructiva, recovered from three different species of Cornus, is the causal agent of the dogwood anthracnose, a devastating disease that was firstly documented in the USA and then introduced into Europe [179].
Generally, closely related organisms, including pathogenic fungi as well as those non-pathogenic, may share similar ecological niches and may potentially interact among themselves. Their co-occurrence could be due to phylogenetic evolution or some unclear biological benefits gained [180,181]. The effects of this interaction may lead to a definition of spaces for development and survival. Nevertheless, it is widely known that non-indigenous species represent one of the greatest threats to native biodiversity [11,23,24,25]. In fact, a fungal invasion into a new ecosystem may change the native endophytic community structure, leading to the extinction of host-specialized fungi [182]. This antagonistic phenomenon is regulated by the production of antifungal compounds, mycoparasitism, or competition for space and resources [180], as well as a synergy of these interactions [181]. Biological invasions may set in motion a long-lasting cascade of effects on the plant host and associated species in unpredictable ways. Generally, the ecological importance of native species prior to the invasion may not be quantified because of the lack of information on fungal communities, especially for non-pathogenic fungal species. As a consequence of global trade and climatic or environmental changes, studies about the impact of new organisms on the ecosystem represent innovative challenges worldwide. In view of these considerations, even if fungal pathogens found in association with investigated plants are widely distributed in the EU [182,183,184,185,186,187,188,189,190], the risk posed by the introduction of potentially noxious species may be very high. Thus, our results suggest the importance of monitoring imported material to avoid the introduction of such alien species.

5. Emerging and Potential Threats Due to Commercial Trade

Several species reported in this review are Quarantine Pests (QP) or Regulated as Non-Quarantine Pests (RNQP), as defined by containment measures within the importing country [191]. Among the fungal pathogens found in Cornus species, Elsinoe fawcettii is listed as a QP in the EU, Tunisia, and Israel. This fungus is the causal agent of Citrus scab and it is one of the most important pathogens in many areas of citrus production [192]. E. fawcettii is common in South America and its presence has been detected in other areas such as Central and South Africa, India and South-Eastern Asia, and Australia [192].
Furthermore, the following pathogens are RNQP in the EU: F. verticilloides (isolated from B. malabarica and A. lebbeck), C. acutatum (isolated from Cornus spp., H. virginiana, and Hamamelis sp.), S. sclerotiorum (isolated from C. stolonifera), and V. dahliae (isolated from Cornus sp.). Outside the EU, the following species are listed as QP: L. theobromae and P. palmivora (in Morocco), A. nidulans, A. macrospora, C. kahawae, C. citrullina, C. herbarum, C. pallescens, A. brassicicola, F. semitectum, F. verticillioides, N. oryzae, and P. longissima (in Mexico), P. graminis (Canada and USA), Diaporthe tersa (in Israel), C. acutatum (in Tunisia and Israel), and C. gloeosporioides and P. capitalensis (in Egypt) [192].
Organisms that move across continents may or may not become dangerous depending on several factors, and unexpected consequences may occur [193,194]. The current knowledge about the fungal community associated with ornamental plants and their interaction with the environment is fragmentary. Fungi species generally well known as pathogens, are not necessarily pathogenic when isolated as endophytes [6,7,8]. Genetic mutation can occur in virulent pathogens, transforming the original pathogen into a nonpathogenic strain [9]. Likewise, even though some endophytes are mutualistic, this does not imply that they will not have negative impacts if introduced in a new ecosystem [6,9]. Alien pathogens can often encounter more susceptible host plants and different microbial and abiotic environments without their own ‘natural enemies’. The so-called ‘risk pathway’ defined by international protocols tend to assume that the pathogen will attack a plant host taxonomically similar to that of the susceptibile plant species in its native countries. However, an invasive pathogen may spread to new target hosts, when introduced in a new ecosystem, and novel pathogen combinations can occur [11]. The disease outcomes of these combinations may be extremely complex and the invasive pathogen populations can reach explosive distribution levels that are usually difficult to eradicate once established [23,24,25]. Beyond the damage which may occur on the host plant species and local microbial communities, biological invasions may affect entire ecosystems and the connected ecosystem processes and services, such as soil fertility, fire control, hydrology, and recreation and tourism amenities [23,24,25]. In response to expanding global trade, several EU regulations [27,28,29] and international protocols [195,196] are aimed at regulating over-dissemination and accidental introduction of plant diseases. However, despite existing laws and efforts to prevent the introduction of potential pathogens at ports of entry, many of them will evade detection and establish alien populations [197,198]. Many pathogenic fungi may be undetected, transported in the form of inocula as endophytes, propagules, mycelium, or spores of vegetative material. In addition, large import volumes often permit the inspection of only a small proportion of the introduced plants. According to the precautionary principle, all imported plant species should be considered as a potential threat (vectors of fungi), therefore the presence and establishment may not depend on the number of arrivals. As a consequence, even a reduced amount of infected plants, which can easily escape phytosanitary inspections, may cause the introduction and the spread of diseases with devastating outcomes [199]. The development of tools, such as new molecular diagnosistics [200] and volatile compounds detection devices [201], that allow the rapid and on-site identification of potentially invasive species and the screening of large volumes of plants, clearly appears to be essential [202]. Despite increasing trade, targeted investment in biosecurity may be effective to reduce pathogen introduction and limit the establishment of alien microorganisms. Thus, we highlight the importance of surveillance due to the potential risk of accidental introductions in the absence of effective biosecurity measures.

6. Conclusions

Globalization has led to intensified movement of people, plants, and plant products, and an increase in the unintentional introduction of non-native fungal species into new ecosystems. Many plant pathogens are biological opportunistic invaders causing several billion dollars in losses to crops, pastures, and forests annually, worldwide. Consideration needs to be given to building resilience in the new environments, from the perspective of pathogen introductions. In particular, the monitoring of plants and plant products, plus early identification-detection of pathogen risks are key steps towards ensuring successful regulation to exclude potential disorders caused by pathogens. This review demonstrated the broad fungal diversity recovered from a small group of ornamental plants that have been relatively unexplored as fungal hosts. Even if the reviewed plant genera are not recognized as sources of significant forest diseases, that have had an ecosystemic impact on a continental scale in the past, we highlight the risk represented by plants as inoculum sources of potentially harmful organisms. Overall, many other species not listed by the EU have represented or may cause important impact in many ecosystemic, environmental, and ecological issues. Our literature search revealed that fungal species may also be introduced through a few hundred plants and invade new ecosystems. In this context, it is important to underline that the amount of imported plant material may not be related to a specific risk, but needs to be considered and evaluated to estimate the negative impacts on agriculture, forestry, and public health, associated with non-indigenous species in European ecosystems. For example, little is known about the effects of invasive species on ecosystem services, although some historic pest invasions (e.g., chestnut blight from North America to Europe) have destroyed host tree species in their locations. The true challenge lies in preventing further damage to natural and managed ecosystems. For this reason, preventative policies need to take into account the means through which pathogens gain access to the EU. The accidental introduction of potentially harmful pathogens also links to other issues of major policy concern (i.e., biotechnology, human health, climate change, etc.) that should be addressed through improved international cooperation and a holistic approach. We should expect that some strategies should be continued or further established to prevent or monitor future introductions, especially at airports, seaports, and other ports of entry, to reduce risks to an acceptable level and preserve natural and agricultural ecosystems.

Author Contributions

Conceptualization, L.G., G.d., F.V. and S.L.W.; literature investigation L.G., G.d., M.S. and M.R.; writing—original draft preparation, L.G. and G.d.; writing—review and editing, project administration, F.V. and S.L.W.; funding acquisition, F.V. and S.L.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the following projects: MIURPON (Grant number Linfa 03PE_00026_1; Grant number Marea 03PE_00106); POR FESR CAMPANIA 2014/2020-O.S. 1.1 (Grant number Bioagro 559); MISE CRESO (Grant number Protection n. F/050421/01-03/X32); PSR Veneto 16.1.1 (Grant number Divine n. 3589659); PSR Campania 2014/2020 Misura 16-Tipologia di intervento 16.1–Azione 2 ‘Sostegno ai Progetti Operativi di Innovazione (POI)’—Progetto ‘DI.O.N.IS.O.’, C.U.P. B98H19005010009; European Union Horizon 2020 Research and Innovation Program, ECOSTACK (Grant agreement no. 773554); PRIN 2017 (Grant number PROSPECT 2017JLN833).

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Endophytic fungi isolated from Acacia (AC), Albizia (AL)., Bauhinia (BA), Berberis (BE), Caesalpinia (CP), Cassia (CS), Cornus (CO), Hamamelis (HA), Jasminus (JA), Ligustrum (LI), Lonicera (LO), Nerium (NE), Robinia (RO). Columns report the number of isolated fungal species. The total number of records calculated per fungal genus is indicated as Tot. SF. The total number of records per plant genera is indicated as Tot. SP. Fungal genera are sorted by alphabetic order.
Table 1. Endophytic fungi isolated from Acacia (AC), Albizia (AL)., Bauhinia (BA), Berberis (BE), Caesalpinia (CP), Cassia (CS), Cornus (CO), Hamamelis (HA), Jasminus (JA), Ligustrum (LI), Lonicera (LO), Nerium (NE), Robinia (RO). Columns report the number of isolated fungal species. The total number of records calculated per fungal genus is indicated as Tot. SF. The total number of records per plant genera is indicated as Tot. SP. Fungal genera are sorted by alphabetic order.
Fungi GeneraPlant Genera
AC AL BA BE CP CS CO HA JA LI LO NE RO Tot
SF
Acremonium 13 4
Albifimbria 1 1
Alternaria1 141 3 2 2 14
Anguillospora 1 1
Ascochyta 1 1
Ascotricha 2 2
Aspergillus38111923 3 40
Aureobasidium2 4 6
Bacillispora 1 1
Beauveria 11
Bipolaris 1 2 1 4
Botryosphaeria1 2 3
Botrytis 1 1 2
Campylospora 1 1
Cercospora 1 1
Chaetomium2 1 3 6
Chrysosporium 1 1
Cladosporium 4 1 5 1 3 14
Clonostachys 1 1 13
Cochliobolus1 3 1 5
Colletotrichum21341 2173 3 27
Coprinus 1 1
Cordyceps 1 1
Corynespora 1 1
Cryptodiaporthe 1 1
Cryptodiaporthe 1 1
Curvularia 15 2 2 10
Cylindrocarpon 1 1
Cyrptosporiopsis 1 1
Daldinia 1 1
Diaporthe 112 2 17
Didymella 2 2
Diplococcium 2 2
Diplodia1 1 2
Discula 1 1
Dothiorella6 2 8
Drechslera 1 1
Drepanopeziza 1 1
Elsinoe 1 1
Epicoccum 1 1 2
Eupenicillium1 1
Eutiarosporella1 1
Exserohilum 1 2
Fusarium14444 4 214129
Fusidium 1 1
Geomyces 1 1
Geotrichum 1 1 1 3
Gibberella 2 2
Glomerella 1 1
Gloniopsis 11
Guignardia 1 11 3
Heliscus 1 1
Helminthosporium 1 1 2
Hypoxylon 1 1
Khuskia 1 1
Kiflimonium 1 1
Lasiodiplodia611 1 2 1 12
Lasmenia 2 2
Lecanicillium 1 1
Leptosphaerulina 1 1
Libertella 1 1
Lophiostoma 1 1
Microsphaeropsis 1 1
Moesziomyces1 12
Myrmecridium 2 2
Myrothecium 1 3
Nectria 2 2
Nemania 1 1
Neocosmospora 1 1 1 3
Neofabraea 1 1
Neofusicoccum6 6
Neonectria 2 2
Nigrospora 4 111 1 8
Nodulisporium 2 2 4
Oblongocollomyces1 1
Paecilomyces 2 2
Papulospora 1 1
Paraboeremia 1 1
Paraphaeosphaeria1 1 2
Penicillium237 328 1 4 30
Periconia 1 1
Peroneutypa 1 1
Pestalotia1 1 2
Pestalotiopsis 2 4 1 7
Peyronellaea1 1
Pezicula 1 1
Phaeobotryosphaeria1 1
Phoma2 3 1 1 7
Phomopsis 31 23 3 12
Phyllosticta1 111 11 111 9
Phytophthora 1 1
Pithomyces 1 1
Pleuroceras 1 1
Prathoda 1 1
Preussia1 1
Psathyrella 1 1
Pseudopithomyces 1 1
Pseudothielavia 1 1
Puccinia 1 1
Pycnidiella 1 1
Rhizopus1 1 2
Rosellinia 1 1
Sarocladium 1 1
Scedosporium 1 1
Sclerotinia 1 1
Scopulariopsis 1 1
Septoria 1 1
Simplicillium 1 1
Spegazzinia 2 2
Spencermartinsia1 1
Sphaeria 1 1
Sporormiella 1 1
Stenella 1 1
Talaromyces 3 2 3 8
Thelioviopsis 1 1
Thelonectria 1 1
Torula 1 3
Trichoderma112 6 1 2 1 14
Tubakia 2 2
Verticillium 1 1 2
Xylaria1 211 2 1 8
Wickerhamomyces1 1
Tot. SP5127942942197847293376
Table
Table 2. Endophytic fungi isolated from Acacia species.
Table 2. Endophytic fungi isolated from Acacia species.
SpeciesHost PlantPlant PartCountryReference
Phyllosticta sp.A. amaraleafMasinagudi, India[34]
Xylaria sp.A. amaraleafMasinagudi, India[34]
Aspergillus nigerA. arabicaleafPunjab, India[35]
Aspergillus sp.A. auriculaeformisrootGuangdong, China[36]
Trichoderma sp.A. auriculaeformisrootGuangdong, China[36]
Aureobasidium pullulansA. baileyanaphyllodeMelbourne, Australia[37]
Alternaria sp.A. decurrensleaf, stemYunnan, China[38]
Penicillium sp.A. decurrensleaf, stemYunnan, China[38]
Peyronellaea sp.A. decurrensleaf, stemYunnan, China[38]
Phoma sp.A. decurrensleaf, stemYunnan, China[38]
Rhizopus sp.A. decurrensleaf, stemYunnan, China[38]
Aureobasidium pullulansA. floribundaphyllodeMelbourne, Australia[37]
Chaetomium globosumA. floribundaphyllodeMelbourne, Australia[37]
Dothiorella heterophyllaeA. heterophyllabranchLa Réunion, France[39]
Dothiorella reunionisA. heterophyllabranchLa Réunion, France[39]
Lasiodiplodia iranensisA. heterophyllabranchLa Réunion, France[39]
Lasiodiplodia rubropurpureaA. heterophyllabranchLa Réunion, France[39]
Neofusicoccum parvumA. heterophyllabranchLa Réunion, France[39]
Cochliobolus geniculatusA. hindsiileafMexico[40]
Colletotrichum gloeosporioidesA. hindsiileafMexico[40]
Colletotrichum truncatumA. hindsiileafMexico[40]
Eupenicillium javanicumA. hindsiileafMexico[40]
Fusarium oxysporumA. hindsiileafMexico[40]
Moesziomyces bullatusA. hindsiileafMexico[40]
Paraphaeosphaeria sp.A. hindsiileafMexico[40]
Phoma sp.A. hindsiileafMexico[40]
Wickerhamomyces anomalusA. hindsiileafMexico[40]
Botryosphaeria dothideaA. karroobranchSouth Africa[41]
Diplodia allocellulaA. karroobranchSouth Africa[41,42]
Dothiorella brevicollisA. karroobranchSouth Africa[41,42]
Dothiorella dulcispinaeA. karroobranchSouth Africa[42]
Dothiorella pretoriensisA. karroobranchSouth Africa[41,42]
Eutiarosporella urbis-rosarumA. karroobranchSouth Africa[41,42]
Lasiodiplodia pseudotheobromaeA. karroobranchSouth Africa[41]
Lasiodiplodia theobromaeA. karroobranchSouth Africa[41]
Lasiodiplodia gonubiensisA. karroobranchSouth Africa[41]
Neofusicoccum kwambonambienseA. karroobranchSouth Africa[41]
Neofusicoccum protearumA. karroobranchSouth Africa[41]
Neofusicoccum vitifusiformeA. karroobranchSouth Africa[41,42]
Neofusicoccum australeA. karroobranchSouth Africa[41]
Neofusicoccum parvumA. karroobranchSouth Africa[41]
Oblongocollomyces variabilisA. karroobranchSouth Africa[41]
Phaeobotryosphaeria variabilisA. karroobranchSouth Africa[42]
Spencermartinsia viticolaA. karroobranchSouth Africa[41,42]
Dothiorella koaeA. koabranchHawaii, USA[39]
Lasiodiplodia theobromaeA. koabranchHawaii, USA[39]
Lasiodiplodia exiguaA. koabranchHawaii, USA[39]
Neofusicoccum occulatumA. koabranchHawaii, USA[39]
Neofusicoccum parvumA. koabranchHawaii, USA[39]
Aspergillus ochraceusA. niloticastemAl-Sharqia, Egypt[43]
Penicillium sp.A. niloticastemAl-Sharqia, Egypt[43]
Pestalotia sp.A. niloticastemAl-Sharqia, Egypt[43]
Chaetomium globosumA. podalyriifoliaphyllodeMelbourne, Australia[37]
Chaetomium sp.A. podalyriifoliaphyllodeMelbourne, Australia[37]
Preussia sp.A. victoriaeleafArizona, USA[44]
Table
Table 3. Endophytic fungi isolated from Albizia species.
Table 3. Endophytic fungi isolated from Albizia species.
SpeciesHost PlantPlant PartCountryReference
Acremonium sp.A. lebbeck-Indonesia[47]
Aspergillus fumigatusA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus fumigatusA. lebbeckleafAl-Sharqia, Egypt[43]
Aspergillus glaucusA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus nigerA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus raperiA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus sclerotionigerA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus flavusA. lebbeckleaf and twigBaghdad, Iraq[48]
Aspergillus sp.A. lebbeck-Indonesia[47]
A. lebbeckleaf and twigBaghdad, Iraq[48]
Bipolaris australiensisA. lebbeckleaf and twigBaghdad, Iraq[48]
Colletotrichum sp.A. amaraleafMasinagudi, India[34]
Curvularia cymbopogonisA. lebbeckleaf and twigBaghdad, Iraq[48]
Diaporthe sp.A. amaraleafMasinagudi, India[34]
Fusarium verticilloidesA. lebbeckleaf and twigBaghdad, Iraq[48]
Fusarium sp.A. amaraleafMasinagudi, India[34]
A. lebbeck-Indonesia[47]
Fusarium oxysporumA. julibrissin--[49]
Lasiodiplodia sp.A. amaraleafMasinagudi, India[34]
Neocosmospora solaniA. lebbeckleaf and twigBaghdad, Iraq[48]
Paecilomyces variotiiA. lebbeckleaf and twigBaghdad, Iraq[48]
Paecilomyces sp.A. lebbeckleaf and twigBaghdad, Iraq[48]
Penicillium sp.A. lebbeck-Indonesia[47]
A. lebbeckleafAl-Sharqia, Egypt[43]
A. lebbeckleaf and twigBaghdad, Iraq[48]
Rosellinia sanctae-crucianaA. lebbeckleafJammu, India[50]
Trichoderma sp.A. lebbeck-Indonesia[47]
Verticillium sp.A. lebbeck-Indonesia[47]
Table
Table 4. Endophytic fungi isolated with Bauhinia species.
Table 4. Endophytic fungi isolated with Bauhinia species.
SpeciesHost PlantPlant PartCountryReference
Acremonium sp.B. brevipes-Brazil[53]
B. forficata-Brazil[53]
B. brevipesleafPirapitinga, Brazil[54]
AlbifimbriaverrucariaB. fortificatastemRecife, Brazil[55]
Alternaria alternataB. malabaricastemChennai, India[56]
B. racemosaleafMudumalai, India[57]
Ascotricha sp.B. forficata-Brazil[53]
Ascotricha chartarumB. fortificataseedRecife, Brazil[55]
Aspergillus sp.B. forficata-Brazil[53]
B. monandraleafRecife, Brazil[58]
B. guianensis-Brazil[53,59,60]
Aspergillus flavusB. malabaricaleaf, rootChennai, India[56]
Aspergillus nigerB. fortificatastemRecife, Brazil[55]
B. malabaricaleaf, root, stemChennai, India[56]
B. racemosaleafMudumalai, India[57]
Aspergillus ochraceusB. fortificatastem, seedRecife, Brazil[55]
Aspergillus tamariiB. malabaricaleaf, stemChennai, India[56]
Aspergillus terreusB. malabaricaleaf, rootChennai, India[56]
Aspergillus versicolorB. vahliileafChilkigarh, India[61]
Botrytis cinereaB. racemosaleafMudumalai, India[57]
Chaetomium globosumB. malabaricaleafChennai, India[56]
Cladosporium sphaerospermumB. fortificataleafRecife, Brazil[55]
Cladosporium sp.B. forficata-Brazil[53]
Cladosporium cladosporioidesB. racemosaleafMudumalai, India[57]
Cladosporium oxysporumB. fortificatasepalRecife, Brazil[55]
Cochliobolus sp.B. forficata-Brazil[53]
Cochliobolus australiensisB. fortificataleafRecife, Brazil[55]
Cochliobolus lunatusB. fortificataleaf, stemRecife, Brazil[55]
Colletotrichum sp.B. forficata-Brazil[53]
Colletotrichum coccodesB. guianensisstemBelem, Brazil[62]
Colletotrichum gloeosporioidesB. racemosaleafMudumalai, India[57]
Corynespora cassiicolaB. racemosaleafMudumalai, India[63]
Curvularia sp.B. monandraleafRecife, Brazil[58]
Curvularia brachysporaB. malabaricaleafChennai, India[56]
Curvularia clavataB. guianensisstemBelem, Brazil[62]
B. phoenicealeafKudremukh range, India[64]
Curvularia lunataB. malabaricaleafChennai, India[56]
B. racemosaleafMudumalai, India[57]
B. phoeniceabark, leafKudremukh range, India[64]
Curvularia pallescensB. phoenicealeafKudremukh range, India[64]
Diaporthe sp.B. brevipesleafPirapitinga, Brazil[54]
Diplococcium sp.B. forficata-Brazil[53]
Diplococcium spicatumB. fortificataleafRecife, Brazil[55]
Dothiorella sp.B. brevipes-Brazil[53]
leafPirapitinga, Brazil[54]
Exserohilum rostratumB. racemosaleaf, stemSathyamangalam, India[65]
B. guianensisstemBelem, Brazil[62,66]
Fusarium culmorumB. malabaricaleaf, stemChennai, India[56]
Fusarium verticillioidesB. malabaricarootChennai, India[56]
Fusarium oxysporumB. malabaricaleaf, root, stemChennai, India[56]
B. phoenicealeafKudremukh range, India[64]
Fusarium sp.B. forficata-Brazil[53]
Fusidium virideB. vahliipetioleChilkigarh, India[61]
Geotrichum candidumB. vahliileaf, petioleChilkigarh, India[61]
Gibberella fujikuroiB. fortificataleaf, stemRecife, Brazil[55]
Gibberella sp.B. forficata-Brazil[53]
Glomerella sp.B. forficata-Brazil[53]
Kiflimonium curvulumB. fortificatasepal, stemRecife, Brazil[55]
Khuskia sp.B. forficata-Brazil[53]
Lasiodiplodia theobromaeB. racemosaleafMudumalai, India[57,63]
Lasmenia sp.B. forficata-Brazil[53]
LasmeniabalansaeB. fortificatastemRecife, Brazil[55]
Myrmecridium sp.B. forficata-Brazil[53]
Myrmecridium schulzeriB. fortificatasepalRecife, Brazil[55]
Nigrospora oryzaeB. racemosaleafMudumalai, India[57]
B. phoeniceastem, leafKudremukh range, India[64]
B. fortificatasepalRecife, Brazil[55]
Nigrospora sacchariB. phoenicealeafKudremukh range, India[64]
Nigrospora sp.B. forficata-Brazil[53]
Nigrospora sphaericaB. vahliistemChilkigarh, India[61]
B. racemosaleaf, stemSathyamangalam, India[65]
Nodulisporium sp.B. forficata-Brazil[53]
B. fortificatastemRecife, Brazil[55]
Paraboeremia putaminumB. fortificatasepalRecife, Brazil[55]
Penicillium communeB. fortificatasepalRecife, Brazil[55]
Penicillium corylophilumB. fortificataseedRecife, Brazil[55]
Penicillium glabrumB. fortificatastem, seedRecife, Brazil[55]
Penicillium implicatumB. fortificatastemRecife, Brazil[55]
Penicillium sp.B. forficata-Brazil[53]
B. monandraleafRecife, Brazil[58]
Penicillium aurantiogriseumB. fortificataseedRecife, Brazil[55]
Pestalotia sp.B. forficata-Brazil[53]
Pestalotiopsis sp.B. brevipesleafPirapitinga, Brazil[54]
B. brevipes-Brazil[53]
Phoma sp.B. forficata-Brazil[53]
B. brevipes-Brazil[53]
leafPirapitinga, Brazil[54]
Phomopsis sp.B. brevipes-Brazil[53]
B. forficata-Brazil[53]
Phomopsis diacheniiB. fortificataleafRecife, Brazil[55]
Phyllosticta capitalensisB. racemosaleafMudumalai, India[57]
Pithomyces sp.B. forficata-Brazil[53]
Pseudopithomycesatro-olivaceusB. fortificataseedRecife, Brazil[55]
Scedosporium apiospermumB. guianensisstemBelem, Brazil[62]
Spegazzinia sp.B. forficata-Brazil[53]
Spegazzinia tessarthraB. fortificataleafRecife, Brazil[55]
Sphaeria baccataB. fortificatasepalRecife, Brazil[55]
Sporormiella minimaB. racemosaleafMudumalai, India[57]
Talaromyces sp.B. forficata-Brazil[53]
Talaromyces funiculosusB. fortificataleafRecife, Brazil[55]
Torulomyces lagenaB. racemosaleafMudumalai, India[57]
Trichoderma piluliferumB. fortificatastemRecife, Brazil[55]
Trichoderma sp.B. forficata-Brazil[53]
Table
Table 5. Endophytic fungi isolated from Berberis species.
Table 5. Endophytic fungi isolated from Berberis species.
SpeciesHost PlantPlant PartCountryReference
Alternaria alternataB. poiretiileaf, twigBeijing, China[70]
B. aristataleafSial Sui, District Rajouri, J&K, India[68]
Alternaria macrosporaB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Alternaria solaniB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Anguillospora crassaBerberis sp.rootWestern Himalaya[71]
Aspergillus flavusB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Campylospora parvulaBerberis sp.rootWestern Himalaya[71]
Cercospora citrullinaB. aristatastemSial Sui, District Rajouri, J&K, India[68]
Clonostachys roseaB. aristatarootSial Sui, District Rajouri, J&K, India[68]
Colletotrichum coccodesB. aristatarootSial Sui, District Rajouri, J&K, India[68]
Colletotrichum coffeanumB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Colletotrichum gloeosporioidesB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Colletotrichum kahawaeB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Bacillispora aquaticaBerberis sp.rootWestern Himalaya[71]
Diaporthe sp.B. vulgarisleaf, stemKenya[72]
Neocosmospora falciformisB. aristatarootSial Sui, District Rajouri, J&K, India[68]
Fusarium lateritiumB. aristatastemSial Sui, District Rajouri, J&K, India[68]
Fusarium nematophilumB. aristatarootSial Sui, District Rajouri, J&K, India[68]
Fusarium oxysporumB. aristatastemSial Sui, District Rajouri, J&K, India[68]
Fusarium solaniB. aristatarootSial Sui, District Rajouri, J&K, India[68]
Heliscus lugdunensisBerberis sp.rootWestern Himalaya[71]
Microsphaeropsis conielloidesB. poiretiitwigBeijing, China[70]
Myrothecium inundatumB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Paraphaeosphaeria sp.B. thunbergiistemChina[73]
Phomopsis sp.B. poiretiitwigBeijing, China[70]
Diaporthe tersaB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Phyllosticta capitalensisB. aristataleafSial Sui, District Rajouri, J&K, India[68]
Prathoda longissimaBerberis sp.rootWestern Himalaya[71]
Puccinia graminis f. sp. triticiB. vulgaris-Pacific Northwest USA[74]
Table
Table 6. Endophytic fungi isolated from Caesalpinia species.
Table 6. Endophytic fungi isolated from Caesalpinia species.
SpeciesHost PlantPlant PartCountryReference
Alternaria alternataC. pulcherrimaleafIndia[76]
Aspergillus flavusC. pulcherrimaleafIndia[76]
Aspergillus fumigatusC. pulcherrimaleafIndia[76]
Aspergillus nigerC. pulcherrimaleafIndia[76]
Aspergillus flavus var. oryzaeC. pulcherrimaleafIndia[76]
Aspergillus rugulosusC. pulcherrimaleafIndia[76]
Aspergillus terreusC. pulcherrimaleafIndia[76]
Aspergillus sp.C. pyramidalisleafBrazil[53]
C. echinataleafBrazil[53]
C. echinatastem, barkBrazil[77]
Aspergillus nidulansC. pulcherrimaleafIndia[76]
Bipolaris oryzaeC. pulcherrimaleafIndia[76]
Bipolaris sp.C. pulcherrimaleafIndia[76]
Chrysosporium sp.C. sappanstemIndonesia[78]
Cladosporium cladosporioidesC. echinataleafBrazil[79]
Colletotrichum gloeosporioidesC. echinataleafBrazil[79]
Curvularia lunataC. sappanstemIndonesia[78]
Curvularia pallescensC. echinataleafBrazil[79]
Epicoccum sp.C. echinata Brazil[53]
Fusarium sp.C. echinataleafBrazil[53]
stemBrazil[77]
stem, barkBrazil[77]
C. pulcherrimaleafIndia[76]
Geotrichum candidumC. sappanstemIndonesia[78]
Helminthosporium sp.C. pulcherrimaleafIndia[76]
Lasiodiplodia theobromaeC. echinataleafBrazil[79]
Nectria sp.C. echinata-Brazil[53]
Nectria pseudotrichiaC. echinatastem, barkBrazil[77]
stem [80]
Penicillium citrinumC. pulcherrimaleafIndia[76]
Penicillium chrysogenumC. pulcherrimaleafIndia[76]
Penicillium sp.C. sappanstemIndonesia[78]
Phyllosticta sorghinaC. echinatastem, barkBrazil[77]
Scopulariopsis coprophilaC. echinataleafBrazil[79]
Talaromyces sp.C. echinatastem, barkBrazil[77]
leafBrazil[53]
Trichoderma atrovirideC. pyramidalisstem, barkBrazil[81]
Trichoderma harzianumC. pyramidalisstem, barkBrazil[81]
Trichoderma koningiopsisC. pyramidalisstem, barkBrazil[81]
Trichoderma longibrachiatumC. pyramidalisstem, barkBrazil[81]
Trichoderma virensC. pyramidalisstem, barkBrazil[81]
Trichoderma sp.C. sappanstemIndonesia[78]
Xylaria sp.C. echinataleafBrazil[53]
Xylaria berteriC. echinatastem, barkBrazil[77]
Table
Table 7. Endophytic fungi isolated from Cassia species.
Table 7. Endophytic fungi isolated from Cassia species.
SpeciesHost PlantPlant PartCountryReference
Aspergillus flavusC. siamealeafMalaysia[87]
Aspergillus sp.C. fistulaleaf, stem, fruitIndia[88]
Coprinus sp.C. fistulaleafBangkok, Thailand[89]
Daldinia sp.C. fistulaleafBangkok, Thailand[89]
Guignardia sp.C. occidentalisleafBrazil[53]
Hypoxylon sp.C. fistulaleafBangkok, Thailand[89]
Nemania sp.C. fistulaleafBangkok, Thailand[89]
Nigrospora sp.C. fistulaleafBangkok, Thailand[89]
Nodulisporium sp.C. fistulaleafBangkok, Thailand[89]
--[90]
Papulospora sp.C. fistulabarkIndia[91]
Penicillium sclerotiorumC. fistula-India[92]
Penicillium sp.C. fistulaleafBangkok, Thailand[89]
Periconia sp.C. fistulabarkIndia[91]
Phomopsis cassiaeC. spectabilis-Brazil[52]
Phomopsis sp.C. fistulaleafBangkok, Thailand[89]
Psathyrella sp.C. fistulaleafBangkok, Thailand[89]
Thelioviopsis sp.C. fistulaleafIndia[91]
Xylaria sp.C. fistulaleafBangkok, Thailand[89]
Table
Table 8. Endophytic fungi isolated from Cornus species.
Table 8. Endophytic fungi isolated from Cornus species.
SpeciesHost PlantPlant PartCountryReference
Alternaria alternataCornus spp.leafJapan, USA[95]
Alternaria sp.C. stoloniferaleafCanada[96]
Alternaria tenuissimaC. officinalistwig, leafChina[97]
Cornus spp.leafJapan[95]
Ascochyta medicaginicolaC. officinalistwigChina[97]
Aspergillus flavus var. oryzaeC. albaleaf-[98]
Aspergillus sp.Cornus spp.leafJapan, USA [95]
Aureobasidium pullulansCornus spp.leafUSA[95]
Aureobasidium sp.C. stoloniferaleafCanada[96]
Cornus spp.leafJapan, USA[95]
Botryosphaeria dothideaC. officinalistwig, leafChina[97]
Cornus spp.leafJapan[95]
Botryosphaeria sp.Cornus spp.leafJapan[95]
Botrytis sp.C. stoloniferaleafCanada[96]
Cladosporium cladosporioidesC. stoloniferaleafCanada[96]
Cladosporium herbarumC. stoloniferaleafCanada[96]
Cladosporium sp.C. stoloniferaleafCanada[96]
Cornus spp.leafJapan[95]
Cladosporium sphaerospermumC. stoloniferaleafCanada[96]
Colletotrichum acutatumCornus spp.leafUSA, Japan[95]
Colletotrichum gloeosporioidesC. officinalistwig, leafChina[97]
C. stoloniferaleafCanada[96]
Colletotrichum sp.Cornus spp.leafJapan[95]
CordycepsfarinoseC. stoloniferaleafCanada[96]
Cryptodiaporthe corniC. alternifoliastemUSA[99]
bark, phloemUSA[100]
Cyrptosporiopsis sp.Cornus spp.leafUSA[95]
Diaporthe amygdaliCornus spp.leafUSA, Japan[95]
Diaporthe lagerstroemiaeCornus spp.leafJapan[95]
DidymellapinodellaC. officinalistwigChina[97]
Didymella glomerataCornus spp.leafUSA, Japan[95]
Discula destructivaCornus spp.leafUSA[101]
leafUSA[95]
C. floridaleafGermany[102]
leafItaly[103]
Drepanopeziza populiC. officinalistwigChina[97]
Elsinoe fawcettiiCornus spp.leafUSA[95]
Epicoccum nigrumC. stoloniferaleafCanada[96]
Fusarium lateritiumC. controversastemKorea[104]
Fusarium oxysporumC. officinalisrootChina[97]
Fusarium sp.Cornus spp.leafJapan[95]
C. stoloniferaleafCanada[96]
Helminthosporium velutinumC. officinalistwigChina[97]
Lecanicillium psalliotaeC. stoloniferaleafCanada[96]
Leptosphaerulina australisC. officinalistwigChina[97]
Lophiostoma sp.Cornus spp.leafUSA[95]
Neofabraea sp.Cornus spp.leafUSA[95]
Neonectria sp.Cornus spp.leafUSA, Japan[95]
Nigrospora sphaericaC. floridastemTennessee, USA[105]
Penicillium brevicompactumC. stoloniferaleafCanada[96]
Penicillium chrysogenumCornus spp.leafUSA[95]
Penicillium citrinumC. stoloniferaleafCanada[96]
Penicillium miczynskiiC. stoloniferaleafCanada[96]
Penicillium simplicissimumCornus spp.leafUSA[95]
Penicillium sp.C. stoloniferaleafCanada[96]
Penicillium spinulosumCornus spp.leafJapan[95]
Penicillium thomiiC. stoloniferaleafCanada[96]
Phytophthora palmivoraC. floridaleaf, shootUSA[106]
Pestalotiopsis mangiferaeCornus spp.leafJapan[95]
Pestalotiopsis microsporaCornus spp.leafUSA, Japan[95]
Pestalotiopsis monochaetaCornus spp.leafJapan[95]
Pestalotiopsis sp.Cornus spp.leafJapan[95]
Phoma moricolaC. officinalistwigChina[97]
Phomopsis sp.C. stoloniferaleafCanada[96]
Cornus spp.leafUSA, Japan[95]
Phyllosticta fallopiaeC. officinalisleafChina[97]
Phytophthora nicotianaeC. floridaleaf, shootUSA[106]
Pleuroceras tenellumCornus spp.leafUSA[95]
SarocladiumkilienseC. stoloniferaleafCanada[96]
Sclerotinia sclerotiorumC. stoloniferaleafCanada[96]
Septoria sp.C. stoloniferaleafCanada[96]
Simplicillium lanosoniveumC. officinalisfruitChina[97]
Stenella sp.C. stoloniferaleafCanada[96]
Talaromyces assiutensisC. officinalisrootChina[97]
TalaromycescecidicolaCornus spp.leafUSA, Japan[95]
Talaromyces trachyspermusC. officinalisrootChina[97]
ThelonectriadiscophoraCornus spp.leafJapan[95]
Trichoderma lixiiCornus spp.leafUSA, Japan[95]
Tubakia sp.Cornus spp.leafUSA, Japan[95]
Verticillium dahliaeCornus spp.leafUSA[95]
Xylaria sp.Cornus spp.leafUSA[95]
Table
Table 9. Endophytic fungi isolated from Hamamelis species.
Table 9. Endophytic fungi isolated from Hamamelis species.
SpeciesHost PlantPlant PartCountryReference
Colletotrichum acutatumH. virginianaleafDutchess Co., USA[109]
Hamamelis sp.leafLitchfield, USA[109]
Nigrospora oryzaeH. mollisleafChina[110]
Pezicula sporulosaH. mollis-Netherlands[111]
H. virginiana-Canada[112]
Phyllosticta hamamelidisH. japonicaleafJapan[113,114]
Table
Table 10. Endophytic fungi isolated from Jasminum species.
Table 10. Endophytic fungi isolated from Jasminum species.
SpeciesHost PlantPlant PartCountryReference
Colletotrichum dematiumJ. sambacleafIndia[120]
Colletotrichum truncatumJ. sambacleafVietnam[121]
Colletotrichum jasminicolaJ. sambacleaf, shootIndia[120]
Colletotrichum jasminigenumJ. sambacleafVietnam[121]
Colletotrichum jasmini-sambacJ. sambacleafVietnam[121]
Colletotrichum siamenseJ. sambacleafVietnam[121]
Colletotrichum sp.J. sambacleafVietnam[121]
Table
Table 11. Endophytic fungi isolated from Ligustrum species.
Table 11. Endophytic fungi isolated from Ligustrum species.
SpeciesHost PlantPlant PartCountryReference
Alternaria alternataL. lucidumleaf, petioleBuenos Aires, Argentina[126]
Alternaria cheiranthiL. lucidumleafBuenos Aires, Argentina[126]
Cladosporium oxysporumL. lucidumleafBuenos Aires, Argentina[126]
Colletotrichum crassipesL. lucidumleafBuenos Aires, Argentina[126]
Colletotrichum sp.L. roxburghiileafBhavani, India[34]
Colletotrichum gloeosporioidesL. lucidumleafBuenos Aires, Argentina[126]
Diplodia mutilaL. lucidumstemBuenos Aires, Argentina[127]
Fusarium oxysporumL. lucidum-Jiangsu, China[128]
Fusarium lateritiumL. lucidumstemBuenos Aires, Argentina[127]
Geotrichum candidumL. lucidumleafBuenos Aires, Argentina[126]
Guignardia mangiferaeL. compactum var. tschonskileafKyoto, Japan[129]
L. quihouileafKyoto, Japan[129]
L. obsusifoiliumleafKyoto, Japan[129]
Lasiodiplodia theobromaeL. lucidumstemBuenos Aires, Argentina[127]
Lasiodiplodia sp.L. roxburghiileafBhavani, India[34]
Libertella sp.L. lucidumbranchesArgentina[130]
Neocosmospora solaniL. lucidum-Jiangsu, China[128]
Peroneutypa scopariaL. lucidumbranchesArgentina[130]
Penicillum sp.L. lucidumleafChina[131]
Pestalotiopsis sp.L. roxburghiileafIndia[132]
Bhavani, India[34]
Phomopsis ligustri-vulgarisL. lucidumleafBuenos Aires, Argentina[126]
Phomopsis sp.L. vulgareleafBraunschweig, Germany[133]
L. roxburghiileafBhavani, India[34]
Phyllosticta sp.L. roxburghiileafBhavani, India[34]
Pycnidiella resinaeL. lucidumleafBuenos Aires, Argentina[126]
Rhizopus microsporusL. lucidumstemBuenos Aires, Argentina[127]
Trichoderma harzianumL. lucidumleafBuenos Aires, Argentina[126]
Trichoderma koningiiL. lucidumstemBuenos Aires, Argentina[127]
Xylaria sp.L. roxburghiileafBhavani, India[34]
L. lucidumleafBuenos Aires, Argentina[126]
Table
Table 12. Endophytic fungi isolated from Lonicera species.
Table 12. Endophytic fungi isolated from Lonicera species.
SpeciesHost PlantPlant PartCountryReference
Fusarium sp.L. japonicaleafHenan, China[136]
Guignardia mangiferaeL. morrowiileafKyoto, Japan[129]
Phyllosticta sp.L. morrowiileafKyoto, Japan[129]
Table
Table 13. Endophytic fungi isolated from Nerium species.
Table 13. Endophytic fungi isolated from Nerium species.
SpeciesHost PlantPlant PartCountryReference
Alternaria brassicicolaN. oleanderstem, flowerIndia[141]
Alternaria sp.N. oleanderleafSouthern India[142]
Aspergillus flavusN. oleanderflowerChennai, India[143]
Aspergillus nigerN. oleanderflowerChennai, India[143]
Aspergillus sp.N. oleanderstem, rootChina[144]
Bipolaris sp.N. oleanderstem, flowerIndia[141]
Chaetomium sp.N. oleanderstem, flowerIndia[141]
N. oleanderstemHong Kong, China[145]
N. oleanderleafSouthern India[142]
Cladosporium sp.N. oleanderstemHong Kong, China[145]
N. oleanderstemIndia[141]
N. oleanderleafSouthern India[142]
Cochliobolus sp.N. oleanderstem, flowerIndia[141]
Colletotrichum sp.N. oleanderstemHong Kong, China[145]
N. oleanderflowerChennai, India[143]
N. oleanderleafSouthern India[142]
Curvularia brachysporaN. oleanderstem, flowerIndia[141]
Curvularia sp.N. oleanderstem, flowerIndia[141]
Cylindrocephalum sp.N. oleanderstem, flowerIndia[141]
Drechslera sp.N. oleanderstemIndia[141]
Fusarium oxysporumN. oleanderflowerChennai, India[143]
Fusarium semitectumN. oleanderstem, flowerIndia[141]
Fusarium sp.N. oleanderstem, flowerIndia[141]
N. oleanderleafSouthern India[142]
Geomyces sp.N. oleanderstemChina[144]
Lasiodiplodia theobromaeN. oleanderflowerChennai, India[143]
Nigrospora sp.N. oleanderrootChina[144]
Penicillium sp.N. oleanderstemChina[144]
N. oleanderstem, flowerIndia[141]
N. oleanderrootChina[146]
N. oleanderleafSouthern India[142]
Phoma sp.N. oleanderstemHong Kong, China[145]
Phyllosticta sp.N. oleanderleafSouthern India[142]
Rhizopus stoloniferaN. oleanderflowerChennai, India[143]
Pseudothielavia terricolaN. oleanderstemIndia[141]
Torula sp.N. oleanderstemHong Kong, China[145]
Trichoderma sp.N. oleanderstem, rootChina[144]
Xylaria sp.N. oleanderleafSouthern India[142]
Table
Table 14. Endophytic fungi isolated from Robinia species.
Table 14. Endophytic fungi isolated from Robinia species.
SpeciesHost PlantPlant PartCountryReference
Beauveria bassianaR. pseudoacacia-Mlyňany, Slovakia[150]
Diaporthe oncostomaR. pseudoacaciastemHungary[151]
Monodictys fluctuataR. pseudoacacia-Germany[152]
Fusarium sp.R. pseudoacacia-Huaxi district, China[153]
Gloniopsis sp.R. pseudoacacia-Huaxi district, China[153]
Clonostachys sp.R. pseudoacacia-Huaxi district, China[153]
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Gioia, L.; d’Errico, G.; Sinno, M.; Ranesi, M.; Woo, S.L.; Vinale, F. A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes. Agriculture 2020, 10, 643. https://doi.org/10.3390/agriculture10120643

AMA Style

Gioia L, d’Errico G, Sinno M, Ranesi M, Woo SL, Vinale F. A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes. Agriculture. 2020; 10(12):643. https://doi.org/10.3390/agriculture10120643

Chicago/Turabian Style

Gioia, Laura, Giada d’Errico, Martina Sinno, Marta Ranesi, Sheridan Lois Woo, and Francesco Vinale. 2020. "A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes" Agriculture 10, no. 12: 643. https://doi.org/10.3390/agriculture10120643

APA Style

Gioia, L., d’Errico, G., Sinno, M., Ranesi, M., Woo, S. L., & Vinale, F. (2020). A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes. Agriculture, 10(12), 643. https://doi.org/10.3390/agriculture10120643

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