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Article

Entomopathogenic Fungi in the Soils of China and Their Bioactivity against Striped Flea Beetles Phyllotretastriolata

by
Ke Zhang
,
Xiaofeng Zhang
,
Qiongbo Hu
* and
Qunfang Weng
*
Key Laboratory of Bio-Pesticide Innovation and Application of Guangdong Province, College of Plant Protection, South China Agricultural University, Guangzhou 510642, China
*
Authors to whom correspondence should be addressed.
Diversity 2022, 14(6), 464; https://doi.org/10.3390/d14060464
Submission received: 12 April 2022 / Revised: 7 June 2022 / Accepted: 8 June 2022 / Published: 9 June 2022
(This article belongs to the Topic Fungal Diversity)
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Abstract

:
The present research aims to explore the occurrence and diversity of entomopathogenic fungi (EPF) in cultivated and uncultivated lands from different provinces of China and to search for EPF against Phyllotreta striolata. In this study, first, the EPF biodiversity from the soil of four provinces (Hunan, Hubei, Henan and Hebei) was surveyed. There were 302 fungal isolates obtained from 226 soil samples collected from croplands (114), arbor (79), grasslands (97) and fallow land (12); 188 EPF isolates were identified as 11 genera. The data indicate that Hubei Province has the greatest EPF diversity, with a Shannon Evenness Index (SHEI) value of 0.88. Here, the grassland, arbor and cropland had an EPF diversity with SHEI values of 0.81, 0.86 and 0.76, respectively, while the fallow land had the highest SHEI value of 1.00, which suggests that cultivation by humans affected the count and richness of soil fungi: the less human activity, the more kinds of fungi found. Finally, the pathogenicity of 47 fungal strains against the adult P. striolata was determined. Isaria javanica (IsjaHN3002) had the highest mortality. In conclusion, this study reports the EPF distribution and biodiversity in the soil from four provinces in China, showing that the amount and type of fungi in the soil varied by region and vegetation and that soil was one of the resources for acquiring EPF. The potential of I. javanica as a biocontrol must be studied further.

1. Introduction

Entomopathogenic fungi (EPFs) are ubiquitous in nature. Biological plant protection with EPFs plays a key role in sustainable pest management programs [1]. In addition to absorbing nutrients for their own growth, some EPFs can control insect populations at low levels for long periods [2]. Fungi-based insecticides have great potential as a form of pest control [3]. Not only are EPFs are harmless to human beings, animals and crops, but they also have the advantages of long-term validity, non-resistance, no residue, no pollution, no damage to natural enemies, high epidemic potential and ease of production [4,5]. Therefore, using EPFs to control agricultural and forestry pests has become a new trend in pest control. EPFs are the largest group of insect-pathogenic microorganisms. According to incomplete statistics, about 100 genera and 1000 species of EPFs have been recorded around the world [6], and more than 40 genera and more than 400 species have been found in China [7], including Beauveria, Metarhizium, Penicillium and Fusarium. Beauveria bassiana and Metarhizium anisopliae have been extensively developed as mycoinsecticides [8]. These species are naturally present in agricultural soils, but the spore numbers in nature are often too low to result in the effective control of pest population outbreaks [9].
Through in-depth studies on the physiology, ecology and molecular biology of EPFs, the effect of applying EPFs to control insects has been significantly improved. Under the premise that pests generally develop resistance, more and more attention has been paid to sustainable development and pollution-free pest management, and researchers prefer the development and utilization of EPFs [10]. Some fungi have a unique method of infection (they can infect pests through the main body wall), which cannot be replicated by other microbial insecticides. The process of EPFs infecting insects mainly includes host recognition, mechanical destruction, toxin secretion and metabolism interference. The combined effect of various factors leads to the death of the host insects [8]. The host species of EPFs are highly specific, and the host spectrum and virulence of different strains are also quite different. Therefore, the isolation and identification of more strains will help us to enrich the resources of EPF and provide more materials for the development of biological control pesticides using EPF [11].
Phyllotreta striolata (Coleoptera: Chrysomelidae) is a prominent pest of Brassicaceae, Solanaceae, Cucurbitaceae and Leguminosae vegetables [12,13,14,15]. Brassicaceae are important crops in south China [16]. Their management is based on synthetic chemical pesticides, leading to insect resistance [17,18]. Few registered varieties of biopesticides can meet the needs of green prevention and control. EPFs represent the most promising candidates in the integrated pest management (IPM) program approach [19].
Popular EPFs, such as Beauveria bassiana, Metarhizium anisopliae, Purpureocillium lilacinum and Isaria (=Cordyceps) javanica, have been developed as mycopesticides to control agricultural, forest and disease vector pests such as locusts, grubs, aphids, whiteflies, moths, mosquitoes and phytopathogenic nematodes [20,21]. It was found that B. bassiana and M. anisopliae can infect the larvae and adults of P. striolata [22,23], but this research is still at the laboratory stage. Because most EPFs are soil-dwelling microbes, investigating soil fungi will be beneficial for exploring new species of EPF resources [24,25,26].
The Hebei, Henan, Hubei and Hunan provinces have complex and diverse landforms, with a variety of plateaus, mountains, hills, basins and plains, as well as a large latitude span in the Yellow River and Yangtze River basins, which have sufficient water and diverse climate types and are suitable for farming. They are the main agricultural production areas in China and have rich agricultural ecological landscapes. However, the distributions of soil EPFs in these regions are not clear. Therefore, this research aims to investigate the distribution and abundance of EPFs in different soil habits of these Chinese provinces. Moreover, the impacts of human activities and changes in the environment on EPFs are analyzed and discussed. The study of EPFs in the soil of the four areas is beneficial for the exploration of new strains to enrich the diversity of EPFs and for mining highly pathogenic strains.

2. Materials and Methods

2.1. Soil Sample Collection

The soil samples were collected from different sites (cropland, fallow land, arbor and grassland). The longitude and latitude of each site were recorded by ICEGPS 100C (Shenzhen, China). From each site, approximately 200 g of soil (10~15 cm depth) from three points was collected, mixed and stored in a plastic bag at 4 °C until further use. In total, 226 samples were collected from these sites (Table A1, Appendix A).

2.2. Isolation of Fungi from the Soil Samples

The method from our previous work was used to isolate fungal strains from the soil samples [27]. Soil suspensions of 0.02 g/mL were prepared with 0.1% Tween-80 solution; then, 0.1 mL of the suspension was inoculated onto a selective medium (PDA, 0.2 g/L cycloheximide, 0.2 g/L chloramphenicol and 0.013 g/L Bengal red) and cultured at 25 ± 1 °C. When the fungi grew out, a single colony was transferred onto the PDA plate and cultured at 25 ± 1 °C, purified and cultured until a new colony was formed [28].

2.3. Identification of Fungal Species and Analysis of Genetic Homology

The identification of fungal isolates was based on the morphological characteristics and similarity of the rDNA-ITS sequences. DNA extraction kits (DP3112, Bio-Teke, Beijing) were used to extract the total DNA from fungal isolates. The primers ITS1 (5′-TCCGTAGGTGAACCTGCGG-3′) and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′) were used to amplify the ITS region on a T100TM Thermal Cycler (BIO-RAD, Hercules, CA, USA) via a standard PCR cycling protocol (94 °C for 3 min, 94 °C for 30 s, 55 °C for 30 s and 72 °C for 1 min for 33 cycles, then 72 °C for 10 min). The obtained ITS rDNA sequences were submitted to GenBank and compared with similar sequences through the BLAST tool of NCBI. The phylogenetic trees of the fungi were constructed by MEGA X via the statistical method of maximum likelihood, a bootstrap test of 500 replications and the Jukes–Cantor model [29]. The fungal strains are listed in Table 1.

2.4. Evaluation of the Shannon Evenness Index

The biodiversity of fungi and EPFs in different soils was evaluated using the Shannon Evenness Index (SHEI). The SHEI was calculated via the formula SHEI = − ∑ i s P i ln P i /lnS, where s is the total number of species in the sample, i is the total number of individuals in one species, Pi is the proportion of species in the sample, lnPi is the value of the natural logarithm of Pi and S is the total number of species.

2.5. Bioassay of the Fungal Strains against P. striolata

The isolates of fungal species were subject to a bioassay against P. striolata based on the work of [27]. In summary, fungal conidia suspensions of 1.0 × 108 spores/mL were prepared with 0.02% Tween-80 solution. Spore suspension concentrations of 1.0 × 104, 1.0 × 105, 1.0 × 106, 1.0 × 107 and 1.0 × 108 spores/mL were prepared by culturing with a light cycle of 12:12 at 25 °C for 7 days. The population of P. striolata was fed with radish lumps, which changed every day. Adults were paralyzed with carbon dioxide and dipped into the conidial suspension for 20 s. The pest populations were surveyed every 24 h after treatment. The 0.02% Tween-80 solution was used as a control group. The experiment was replicated thrice, and 20 adults were used for each treatment.

2.6. Scanning Electron Microscopy

The samples were placed in a 2 mL centrifuge tube, fixed with 2.5% glutaraldehyde overnight, washed with physiological saline and dehydrated using a graded series of ethanol; isoamyl acetate was replaced overnight. They were vacuum-dried, fixed onto the platform and then coated with platinum with an ion coater before being observed using a scanning electron microscope.

2.7. Statistical Analysis

Analyses of the bioassay data were carried out using IBM SPSS Statistics version 20.0 (IBM Corp., Armonk, NY, USA). The data were expressed as mean ± SD and were subjected to one-way ANOVA, followed by Duncan’s multiple range test (DMRT). Significant differences were accepted at p < 0.05.

3. Results

3.1. EPF Species Diversity in the Soils of China

In total, 302 fungal isolates were purified. Among these, 188 EPF isolates were identified as belonging to 11 genera according to the morphological and molecular analyses. Purpureocillium lavendulum, with 69 isolates, was the dominant species, and the congeneric species Purpureocillium lilacinum had only 13 isolates (Figure 1, Table A1). The genus Metarhizium had three species—M. anisopliae, M. marquandii and M. sp.—for which 49, 33 and 17 isolates, respectively, were obtained (Figure 1, Table A1). Penicillium had six species—Penicillium subrubescens, Penicillium guttulosum, Penicillium rubens, Penicillium chrysogenum, Penicillium citrinum and Penicillium mirabile—with 12, 2, 3, 1, 11 and 6 isolates found, respectively (Figure 2, Table A1). Aspergillus had 12 species (Figure 2, Table A1). Talaromyces had four species (Figure 3, Table A1), and both Beauveria and Isaria had three species each (Figure 3, Table A1). Both Lecanicillium and Simplicillium had four species each (Figure 4, Table A1). Fusarium, Coniochaeta and Clonostachys each had six species (Figure 4, Table A1). Other species with one to four isolates were identified as Tolypocladium album, Acremonium exuviarum, Acrophialophora nainiana, Nectria mauritiicola, Hawksworthiomyces taylorii, Chloridium aseptatum, Trichurus terrophilus, Chrysosporium lobatum, Arthropsis hispanica, Malbranchea aurantiaca, Auxarthron alboluteum, Arthrographis kalrae, Melanoctona tectonae, Phialophora livistonae, Xenopolyscytalum pinea, Oidiodendron fuscum, Cutaneotrichosporon dermatis, Apiotrichum cacaoliposimilis, Mucor ellipsoideus, Gongronella butleri and Cunninghamella elegans. (Figure 5, Table A1). The other 73 isolates have not been classified yet. Obviously, Purpureocillium lavendulum, M. anisopliae, M. marquandii, Purpureocillium lilacinum and B. bassiana were the most abundant EPF species.

3.2. Distribution of Soil EPF in Different Regions

There were different numbers and isolating rates of EPFs in different regions. Compared with the average fungal isolating rates of 83.70% and 61.92% in all fungi and EPFs, Henan had the highest rate of >90% (Table 2). However, the Shannon Evenness Index indicated that Hubei and Hunan were districts with the highest EPF biodiversity, while Hunan and Hebei had the EPF biodiversity with SHEI values of 0.87 and 0.88, respectively (Table 2).

3.3. The Biodiversity of Soil EPF in Different Environments

There were different numbers and isolating rates of EPF in Central China. Compared with the average fungal isolating rates of 87.42% and 61.16% for all fungi and EPFs, cropland samples had higher rates of >69% (Table 3). However, the SHEI indicated that cropland had the lowest EPF biodiversity, while fallow land samples had the most abundant EPF biodiversity (Table 3).

3.4. The Pathogenicity of Fungal Isolates against P. striolata

Forty-seven isolates were subjected to a bioassay against P. striolata. The results indicate that I. javanica (IsjaHN3002) had the highest mortality, and Aspergillus spp., Fusarium falciforme, Lecanicillium spp., Metarhizium spp. and Talaromyces spp. all had obvious pathogenicity against P. striolata (Table 4).

3.5. The Pathogenicity of I. javanica against P. striolata

According to the results shown in Table 5, the number of muscardine cadavers increased with the spore concentration. The lethal rate of 1.0 × 108 spores/mL spore suspension treatment group was as high as 80%. When the spore concentration was lower than 1.0 × 106 spores/mL, no hyphae were observed on the body wall of P. striolata in the first 3 days. There was no significant difference in the rate of zombies in the groups treated with spore suspensions at concentrations of 1.0 × 104 and 1.0 × 105, 1.0 × 106 spores/mL in the first 3 days, but there was a significant difference in the rate of zombies in the group treated with spore suspensions with concentrations of 1.0 × 107 and 1.0 × 108 spores/mL in the first 3 days. After the seventh day, the differences among the treatment groups were revealed. Compared with other treatment groups, there was a significant difference in the lethal rate of the spore suspension with a concentration of 1.0 × 108 spores/mL.

3.6. Scanning Electron Microscopy Observations of Infection Process of I. javanica

The results showed that the attachment of conidia of I. javanica to different parts of the body surface was very different. After 2 h, the attachment of conidia was observed. No attachment of conidia was found on the head, abdomen, shard or other smooth surfaces. The conidia were mainly attached to the bristly areas and internodes such as the antennae, foot joints, chest and chest feet. The most densely attached site was the intersegmental membrane of the chest feet, followed by the foot joints (Figure 6).
After 12 h of inoculation, some conidia began to germinate, forming short germ tubes at the top. Twenty-four hours after infection, the top of the germ tube expanded to form an appressorium and continued in the direction of the intersegmental membrane, forming tendrils (Figure 7A–C) and looking for a suitable invasion site. The germ tube could also directly invade the body wall (Figure 7D). At 48 h, hyphae began to grow between the foot internode, and new conidiophores and conidia sprouted (Figure 8A). Next, 48–72 h after inoculation, the surface of the insect body was gradually covered by mycelia until it was completely covered (Figure 8B–D). Through stereoscopic observation, the mycelia were observed to grow from the body surface on the third day, and then the mycelium coverage increased day by day (Figure 9), while the control group never experienced mycelial growth.

4. Discussion

This study surveyed the EPF distribution at a broad scale in China. ITS sequences are small and easy to analyze and have been widely used in the phylogenetic analysis of different fungal species, but their accuracy is controversial. Therefore, the identification of the fungal species in this study has some defects. Undoubtedly, our results initially provide a large amount of information about the soil fungi in these areas. Moreover, the results indicate that the soil environment strongly impacts the distribution of EPFs. Compared to arbor and non-cultivated land, the cropland samples had fewer EPFs. The isolation rate of EPFs was not high, which showed that soil fungi were not abundant in these areas and that the sampling and isolation methods also affected the isolation of fungi. The EPF diversity may be affected by the use of fungicides in croplands. China is a heavy consumer of pesticides, and a large number of broad-spectrum fungicides such as carbendazim, chlorothalonil and azoxystrobin, etc., are sprayed on croplands and probably inhibit fungi [59,60].
EPFs can parasitize insects and cause insect diseases, including some obligate parasitism that may not cause insect death but that can reduce the vitality of the host insects and weaken them [61] or affect insect spawning [62]; as such, when using EPFs, we can observe changes in the behavior of host insects [63,64]. Some studies have suggested that insects can actively identify fungi, with the target location being the cell wall of the fungi, while the fungi will take a series of measures to evade the host’s defenses in the face of insect recognition [65]. Therefore, the invasion of host insects by EPF is a process of mutual influence and interaction [66]. As a result, the body surface of P. striolata may be able to recognize I. javanica, and the resistance and defense of I. javanica may also take measures to promote the germination of conidia in advance. In view of this fact, we can further explore what receptor binds the cell wall of conidia of I. javanica to produce signal molecules and promote spore germination, determining the factors promoting spore germination and improving pathogenicity.
Through scanning electron microscope observation, 12 h after infection with I. javanica, some conidia began to germinate, as shown in Figure 7. After 24 h of infection, only some scattered spores germinated. Because of the hard shell and dense structure on the body surface, the structure of the body wall varies greatly in different parts, and the outer skin has hydrophobic components. However, in tests of the bioactivity of different concentrations of spore suspensions against P. striolata, it was found that the spore suspension concentration of I. javanica had a stimulative effect on the production of zombies. This may be the QS phenomenon observed in I. javanica, which refers to a change in the physiological and biochemical characteristics of the microbial population in the process of its growth due to an increase in the population density, showing the characteristics of a small number of bacteria or a single bacterium. Cells use the QS mechanism to carry out cell-to-cell communication so that they can coordinate in a complex environment, and their “team combat ability” better ensures that the whole population survives. At present, the study of QSM is mainly focused on bacteria, and QSM has also been reported in related fungi [67]. In recent years, more reports have confirmed that fungi have QSM [68,69] and have QSM pheromones that are similar to the bacterial regulation of the physiological behavior of fungi [70,71,72]. However, in-depth studies of fungal QSM have not been carried out. Therefore, in the production of fungicidal insecticides using I. javanica, we can choose the appropriate formulation or use new production technology to help I. javanica survive in the form of sporangia, and it can also attach to the body surface after application to invade the body faster and improve its pathogenicity.
Several species have not been reported as EPF, namely Aspergillus, Lecanicillium, Monascus, Talaromyces and Fusarium. Their pathogenicity against P. striolata was discovered, and their potential for pest control deserves further research. Our experiment will provide new insight into the distribution characteristics of EPF and the conservation of their biodiversity.

5. Conclusions

In conclusion, 188 EPF isolates were identified from 226 soil samples, and the amount and types of fungi in the soil varied by region and vegetation type. Metarhizium, with 89 isolates, was recognized as the dominant EPF species, whereas Purpureocillium and Beauveria (respectively with 81 and 11 isolates) were the richer genera. Finally, it was first reported that I. javanica had pathogenicity against P. striolata, and we described its infection process.

Author Contributions

K.Z. and X.Z. completed most of the experiments, including the collection of the soil samples, the isolation and identification of the fungi strains and the bioassay and data analysis. Q.H. designed the experiments and collected partial soil samples. K.Z. and Q.W. wrote the article. All authors have read and agreed to the published version of the manuscript.

Funding

This project was supported by Guangdong Province Science and Technology Project (2016B020234005) and the National Natural Science Foundation of China (31572053).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analyzed in this study. These data can be found here: https://www.ncbi.nlm.nih.gov/nuccore/?term=OM372687:OM373035[accn], submission ID SUB9030162; accessed on 25 January 2022.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table
Table A1. The information of the soil samples collected and fungal isolates.
Table A1. The information of the soil samples collected and fungal isolates.
SiteIsolateGenBank
Access No.		Species
NO.AddressLatitude and LongitudeSample
Environment
HB01Xianning, Hubei29.267 N, 113.746 E Fallow landHB01Z01--
HB01Z02--
PeruHB01Z03OM372687Penicillium rubens
HB01Z04--
CropHB01G01--
PesuHB01G02OM372688Penicillium subrubescens
HB02Xianning, Hubei29.568 N, 114.193 ECrop----
ArborHB02S01--
MeanHB02S02OM372689Metarhizium anisopliae
GrassTapiHB0201OM372690Talaromyces pinophilus
HB0202--
PemiHB0203OM372691Penicillium mirabile
HB03Daye, Hubei29.973 N, 114.667 ECropHB03Y01--
AsteHB03Y02OM372692Aspergillus terreus
HB03Y03--
GrassHB0301--
HB04Huanggang, Hubei30.372 N, 115.161 EFallow landTapiHB04Z01OM372693Talaromyces pinophilus
CropMeanHB04F01OM372694Metarhizium anisopliae
AsudHB04F02OM372695Aspergillus udagawae
AsfuHB04F03OM372696Aspergillus fumigatus
HB05Xinzhou, Hubei30.863 N, 114.881 ECropMema sp. HB05N01OM372697Metarhizium marquandii
TapiHB05N02OM372698Talaromyces pinophilus
GrassTapiHB0501OM372699Talaromyces pinophilus
HB06Huanggang, Hubei31.257 N, 115.056 EArborHB06S01--
Fallow landPulaHB06Z01OM372700Purpureocillium lavendulum
GrassAsteHB0601OM372701Aspergillus terreus
HB07Wuhan, Hubei30.887 N, 114.462 EGrassMema sp. HB0701OM372702Metarhizium marquandii
HB0702--
PemiHB0703OM372703Penicillium mirabile
ArborAsnoHB07S01OM372704Aspergillus nomius
HB08Xiaogan, Hubei31.030 N, 113.938 ECrop----
GrassTapiHB0801OM372705Talaromyces pinophilus
HB0802--
PeciHB803OM372706Penicillium citrinum
IsjaHB0804OM372707Isaria javanica
HB09Xiaogan, Hubei31.325 N, 113.580 EFallow landGobuHB0901OM372708Gongronella butleri
HB0902--
Suizhou, Hubei31.665 N, 113.269 EArbor----
Grass----
HB11Xiangyang, Hubei31.948 N, 112.929 ECropHB11Y01--
PemiHB11Q01OM372709Penicillium mirabile
ClgrHB11Q02OM372710Clonostachys grammicospora
HB12Xiangyang, Hubei32.178 N, 112.211 E GrassHB12A01--
MeanHB12A02OM372711Metarhizium anisopliae
Arbor--
HB13Xiangyang, Hubei32.307 N, 111.614 E CropAsteHB13F01OM372712Aspergillus terreus
HB13F02--
ArborPuliHB13S01OM372713Purpureocillium lilacinum
HB14Shiyan, Hubei32.502 N, E111.100 E GrassPulaHB1401OM372714Purpureocillium lavendulum
ArborHB14S01--
HB15Shiyan, Hubei32.020 N, 110.679 EFallow land--
GrassHB1501--
PulaHB1502OM372715Purpureocillium lavendulum
FufaHB1503OM372716Fusarium falciforme
HB16Shennongjia, Hubei31.823 N, 110.508 EGrassMeanHB1601OM372717Metarhizium anisopliae
ArborCofaHB16S01OM372718Coniochaeta fasciculata
MeanHB16S02OM372719Metarhizium anisopliae
PesuHB16S03OM372720Penicillium subrubescens
HB17Shennongjia, Hubei31.514 N, 110.338 E GrassCofaHB1701OM372721Coniochaeta fasciculata
AsfuHB1702OM372722Aspergillus fumigatus
ArborCofaHB17S01OM372723Coniochaeta fasciculata
HB18Yichang, Hubei31.266 N, 110.686 EGrassHB1801--
HB19Enshi, Hubei30.007 N, 110.377 EGrassHB1901--
HB1902--
AcexAB1903OM372724Acremonium exuviarum
CropMeanHB20Y01OM372725Metarhizium anisopliae
HB20Enshi, Hubei30.556 N, 109.889 EGrassPeruHB2001OM372726Penicillium rubens
AsteHB2002OM372727Aspergillus terreus
CofaHB2003OM372728Coniochaeta fasciculata
ArborHB20S01--
HB20S02--
HB21Yichang, Hubei30.615 N, 110.513 EGrassMema sp. HB2101OM372729Metarhizium marquandii
PulaHB2102OM372730Purpureocillium lavendulum
CropArkaHB21Y01OM372731Arthrographis kalrae
AsfuHB21Y02OM372732Aspergillus fumigatus
HB22Yichang, Hubei30.582 N, 111.028 EFallow landTapiHB22Z01OM372733Talaromyces pinophilus
CropHB22Y01--
HB22Y02--
HB23Yichang, Hubei30.688 N, 111.517 ECropPeciHB23Y01OM372734Penicillium citrinum
OrchardTapiHB23G01OM372735Talaromyces pinophilus
ArborTapiHB23S01OM372736Talaromyces pinophilus
HB24Jingmen, Hubei30.904 N, 112.185 EArborAsteHB24S01OM372737Aspergillus terreus
AsudHB24S02OM372738Aspergillus udagawae
CropAsfuHB24N01OM372739Aspergillus fumigatus
HB24N02--
MuelHB24N03OM372740Mucor ellipsoideus
HB24N04--
HB25Jingmen, Hubei30.991 N, 112.854 EArborHB25S01--
Grass--
HB26Xiaogan, Hubei30.868 N, 113.576 EArborMema sp.HB26S01OM372741Metarhizium marquandii
PeciHB26S02OM372742Penicillium citrinum
AsteHB26S03OM372743Aspergillus terreus
PeciHB26S04OM372744Penicillium citrinum
GrassAsteHB2601OM372745Aspergillus terreus
IsjaHB2602OM372746Isaria javanica
PulaHB2603OM372747Purpureocillium lavendulum
HB27Wuhan, Hubei30.478 N, 113.874 EArborHB27S01--
AsnoHB27S02OM372748Aspergillus nomius
GrassHB2701--
HB2702--
MeanHB2703OM372749Metarhizium anisopliae
HB28Xiantao, Hubei30.350 N, 113.424 EGrassPeguHB2801OM372750Penicillium guttulosum
ArborAcnaHB28S01OM372751Acrophialophora nainiana
PulaHB28S02OM372752Purpureocillium lavendulum
MemaHB28S03OM372753Metarhizium marquandii
MemaHB28S04OM372754Metarhizium marquandii
LesaHB28S05OM372755Lecanicillium saksenae
HB29Qianjiang, Hubei30.373 N, 112.889 ECropTatrHB29Y01OM372756Talaromyces trachyspermus
AcnaHB29Y02OM372757Acrophialophora nainiana
HB29Y03--
MeanHB29Y04OM372758Metarhizium anisopliae
ArborAsnoHB29S01OM372759Aspergillus nomius
HB29S02--
PuliHB29S03OM372760Purpureocillium lilacinum
HB29S04--
HB30Jingzhou, Hubei30.352 N, 112.338 EGrassClroHB3001OM372761Clonostachys rosea
AspsHB3002OM372762Aspergillus pseudodeflectus
HB3003--
AsgrHB3004OM372763Aspergillus granulosus
Crop--
HB31Jingzhou, Hubei30.043 N, 112.158 EGrassAsfuHB3101OM372764Aspergillus fumigatus
HB3102--
Crop--
HN01Changsha, Hunan28.203 N, 113.303 ECropPulaHN01S01OM372765Purpureocillium lavendulum
AsteHN01S02OM372766Aspergillus terreus
MeanHN01S03OM372767Metarhizium anisopliae
CropAsfuHN0101OM372768Aspergillus fumigatus
IsjaHN0102OM372769Isaria javanica
HN02Changde, Hunan29.634 N, 111.840 EGrassMemaHN0201OM372770Metarhizium marquandii
PulaHN0202OM372771Purpureocillium lavendulum
ArborPeciHN02S01OM372772Penicillium citrinum
AsteHN02S02OM372773Aspergillus terreus
HN03Changde, Hunan29.131 N, 111.706 EGrassHN0301--
PesuHN0302OM372774Penicillium subrubescens
ArborMemaHN03S01OM372775Metarhizium marquandii
AsnoHN03S02OM372776Aspergillus nomius
HN04Zhangjiajie, Hunan29.424 N, 111.163 EOrchardTapiHN04Y01OM372777Talaromyces pinophilus
Grass----
HN05Zhangjiajie, Hunan29.348 N, 110.568 EArborHN05S01--
Grass----
HN06Xiangxi, Hunan29.034 N, 110.228 EArborPulaHN06S01OM372778Purpureocillium lavendulum
GrassTapiHN0601OM372779Talaromyces pinophilus
CropHN06Y01--
PuliHN06Y02OM372780Purpureocillium lilacinum
ChasHN06Y03OM372781Chloridium aseptatum
HN06Y04--
HN06Y05--
HN07Xiangxi, Hunan28.623 N, 109.547 EGrassHN0701--
Pula sp. HN0702OM372782Purpureocillium lavendulum
PeciHN0703OM372783Penicillium citrinum
ArborPulaHN07S01OM372784Purpureocillium lavendulum
AsscHN07S02OM372785Aspergillus sclerotiorum
HN08Huaihua, Hunan26.963 N, 109.747 EGrassMema sp. HN0801OM372786Metarhizium marquandii
ArborPesuHN08S01OM372787Penicillium subrubescens
PulaHN08S02OM372788Purpureocillium lavendulum
HN09Huaihua, Hunan26.614 N, 109.671 EGrassHataHN0901OM372789Hawksworthiomyces taylorii
PuliHN0902OM372790Purpureocillium lilacinum
PesuHN0903OM372791Penicillium subrubescens
ArborPulaHN09S01OM372792Purpureocillium lavendulum
HN09S02--
HN10Yongzhou, Hunan26.662 N, 111.493 EGrassHN1001--
PesuHN1002OM372793Penicillium subrubescens
HN1003--
ArborHN10S01--
HN11Yongzhou, Hunan26.063 N, 111.831 EArborFufaHN11S01OM372794Fusarium falciforme
Fallow land----
HN12Yongzhou, Hunan25.528 N, 112.111 EGrassPulaHN1201OM372795Purpureocillium lavendulum
CudeHN1202OM372796Cutaneotrichosporon dermatis
HN13Chenzhou, Hunan25.659 N, 112.729 EGrassTavaHN1301OM372797Talaromyces variabilis
BebaHN1302OM372798Beauveria bassiana
HN1303--
ArborMeteHN13S01OM372799Melanoctona tectonae
HN14Chenzhou, Hunan25.965 N, 113.042 EGrassBebaHN1401OM372800Beauveria bassiana
ArborPesuHN14S01OM372801Penicillium subrubescens
PuliHN14S02OM372802Purpureocillium lilacinum
HN15Hengyang, Hunan26.426 N, 112.889 EGrassAstaHN1501OM372803Aspergillus tanneri
AsscHN1502OM372804Aspergillus sclerotiorum
ArborAsscHN15S01OM372805Aspergillus sclerotiorum
Mema sp. HN15S02OM372806Metarhizium marquandii
ToalHN15S03OM372807Tolypocladium album
ToalHN15S04OM372808Tolypocladium album
FusoHN15S05OM372809Fusarium solani
HN16Hengyang, Hunan26.974 N, 112.425 EGrassMema sp. HN1601OM372810Metarhizium marquandii
OrchardAsscHN16Z01OM372811Aspergillus sclerotiorum
AsscHN16Z02OM372812Aspergillus sclerotiorum
HN17Loudi, Hunan27.440 N, 112.132 EGrassPesuHN1701OM372813Penicillium subrubescens
ArborMemaHN17S01OM372814Metarhizium marquandii
XepiHN17S02OM372815Xenopolyscytalum pinea
CuelHN17S03OM372816Cunninghamella elegans
HN18Loudi, Hunan27.821 N, 111.763 EGrassMemaHN1801OM372817Metarhizium marquandii
HN1802
Fallow landPesuHN18Z01OM372818Penicillium subrubescens
HN19Yiyang, Hunan28.264 N, 111.712 EArborMeanHN19S01OM372819Metarhizium anisopliae
HN19S02
HN19S03
GrassFufaHN1901OM372820Fusarium falciforme
Mema sp. HN1902OM372821Metarhizium marquandii
HN20Yiyang, Hunan28.525 N, 112.045 E GrassBebaHN2001OM372822Beauveria bassiana
PulaHN2002OM372823Purpureocillium lavendulum
PesuHN2003OM372824Penicillium subrubescens
Fallow landHN20Z01--
BebaHN20Z02OM372825Beauveria bassiana
Mema sp. HN20Z03OM372826Metarhizium marquandii
HN21Changsha, Hunan28.222 N, 112.567 ECropMeanHN21G01OM372829Metarhizium anisopliae
Pula sp. HN21G02OM372830Purpureocillium lavendulum
TapiHN21G03OM372831Talaromyces pinophilus
ArborPulaHN21S01OM372827Purpureocillium lavendulum
Mema sp. HN21S02OM372828Metarhizium marquandii
HN22Xiangtan, Hunan27.806 N, 112.511 EFallow landPula sp. HN22Z01OM372832Purpureocillium lavendulum
Arbor----
HN23Xiangtan, Hunan27.846 N, 113.017 EGrassMema sp. HN2301OM372833Metarhizium marquandii
PulaHN2302OM372834Purpureocillium lavendulum
PeciHN2303OM372835Penicillium citrinum
ArborPula sp. HN23S01OM372836Purpureocillium lavendulum
HN24Hengyang, Hunan27.229 N, 112.897 EGrassTavaHN2401OM372837Talaromyces variabilis
ApcaHN2402OM372838Apiotrichum cacaoliposimilis
PesuHN2403OM372839Penicillium subrubescens
ArborMeanHN24S01OM372840Metarhizium anisopliae
HN24S02--
HN25Zhuzhou, Hunan26.893 N, 113.374 EGrassMema sp. HN2501OM372841Metarhizium marquandii
OrchardMeanHN25B01OM372842Metarhizium anisopliae
HN26Zhuzhou, Hunan27.496 N, 113.486 EArborMemaHN26S01OM372843Metarhizium marquandii
HN26S02--
Fallow landMeanHN26Z01OM372844Metarhizium anisopliae
HN27Xiangxi, Hunan27.914 N, 109.385 EGrassPulaHN2701OM372845Purpureocillium lavendulum
PhliHN2702OM372846Phialophora livistonae
HN28Huaihua, Hunan27.896 N, 109.702 EOrchardHN28J01--
PuliHN28J02OM372847Purpureocillium lilacinum
PeruHN28J03OM372848Penicillium rubens
HN29Huaihua, Hunan27.367 N, 109.935 EFallow landPulaHN29B01OM372849Purpureocillium lavendulum
MeanHN29B02OM372850Metarhizium anisopliae
GrassArhiHN2901OM372851Arthropsis hispanica
HN30Huaihua, Hunan27.216 N, 110.420 EArborSimiHN3001OM372852Simplicillium minatense
IsjaHN3002OM372853Isaria javanica
HN31Shaoyang, Hunan26.941 N, 110.638 EArborXepiHN3101OM372854Xenopolyscytalum pinea
HN32Shaoyang, Hunan26.322 N, 110.837 EGrass----
HE01Xingtai, Hebei36.905 N, 114.559 ECropMeanHE01A01OM372855Metarhizium anisopliae
LecoHE01A02OM372856Lecanicillium coprophilum
GrassMeanHE01B01OM372857Metarhizium anisopliae
NemaHE01B02OM372858Nectria mauritiicola
LecoHE01B03OM372859Lecanicillium coprophilum
HE02Shijiazhuang, Hebei35.994 N, 113.758 EArborLecoHE02A01OM372860Lecanicillium coprophilum
MeanHE02A02OM372861Metarhizium anisopliae
HE02A03--
HE03Baoding, Hebei39.138 N, 115.536 ECropLecoHE03A01OM372862Lecanicillium coprophilum
MemaHE03A02OM372863Metarhizium marquandii
GrassHE03B01--
LecoHE03B02OM372864Lecanicillium coprophilum
PoplarClgrHE03C01OM372865Clonostachys grammicospora
MeanHE03C02OM372866Metarhizium anisopliae
TatrHE03C03OM372867Talaromyces trachyspermus
HE04Zhangjiakou, Hebei39.273 N, 115.455 EPoplarAualHE04A01OM372868Auxarthron alboluteum
ClgrHE04A02OM372869Clonostachys grammicospora
CropHE04B01--
LecoHE04B02OM372870Lecanicillium coprophilum
Mema sp. HE04B03OM372871Metarhizium marquandii
HE05Zhangjiakou, Hebei39.375 N, 114.866 EPoplarHE05A01--
LecoHE05A02OM372872Lecanicillium coprophilum
CropMema sp. HE05B01OM372873Metarhizium marquandii
MeanHE05B02OM372874Metarhizium anisopliae
HE06Zhangjiakou, Hebei40.488 N, 114.838 EOrchardMeanHE06A01OM372875Metarhizium anisopliae
TrteHE06A02OM372876Trichurus terrophilus
AssyHE06A03OM372877Aspergillus sydowii
BebaHE06A04OM372878Beauveria bassiana
CropMema sp. HE06B01OM372879Metarhizium marquandii
PuliHE06B02OM372880Purpureocillium lilacinum
HE07Zhangjiakou, Hebei41.267 N, 114.785 ECropHE07A01--
AscrHE07C01OM372882Aspergillus crustosus
GrassLecoHE07B01OM372881Lecanicillium coprophilum
PoplarLecoHE07D01OM372883Lecanicillium coprophilum
HE08Zhangjiakou, Hebei41.073 N, 115.389 EGrassHE08A01--
HE08A02--
CropAualHE08B01OM372884Auxarthron alboluteum
AsfuHE08C01OM372885Aspergillus fumigatus
HE09Chengde, Hebei41.581 N, 116.023 EGrassMeanHE09A01OM372886Metarhizium anisopliae
PulaHE09A02OM372887Purpureocillium lavendulum
ElmAsfuHE09B01OM372888Aspergillus fumigatus
CropHE09C01--
OifuHE09C02OM372889Oidiodendron fuscum
HE10Chengde, Hebei42.001 N, 116.975 EGrassTapuHE10A01OM372890Talaromyces purpureogenus
Crop----
HE11Chengde, Hebei42.253 N, 117.143 EGrassPulaHE11A01OM372891Purpureocillium lavendulum
PesuHE11A02OM372892Penicillium subrubescens
PineCofaHE11C01OM372893Coniochaeta fasciculata
CropAssyHE11D01OM372894Aspergillus sydowii
HE12Chengde, Hebei41.997 N, 117.655 EOrchardAsfuHE12A01OM372895Aspergillus fumigatus
GrassPulaHE12B01OM372896Purpureocillium lavendulum
MeanHE12B02OM372897Metarhizium anisopliae
HE13Chengde, Hebei41.302 N, 118.038 ECropHE13A01--
MeanHE13B01OM372898Metarhizium anisopliae
MeanHE13B02OM372899Metarhizium anisopliae
PoplarAsudHE13C01OM372900Aspergillus udagawae
PulaHE13C02OM372901Purpureocillium lavendulum
MeanHE13C03OM372902Metarhizium anisopliae
HE14Chengde, Hebei40.578 N, 117.704 ECropTatrHE14A01OM372903Talaromyces trachyspermus
Grass----
HE15Tangshan, Hebei40.108 N, 117.985 ECropMeanHE15A01OM372904Metarhizium anisopliae
Sicy sp. HE15A02OM372905Simplicillium cylindrosporum
ArborMeanHE15B01OM372906Metarhizium anisopliae
PemiHB15B02OM372907Penicillium mirabile
GrassSicyHE15C01OM372908Simplicillium cylindrosporum
SimiHE15C02OM372909Simplicillium minatense
MeanHE15C03OM372910Metarhizium anisopliae
HE16Tangshan, Hebei39.584 N, 118.264 EGrassMeanHE16A01OM372911Metarhizium anisopliae
HE17Tangshan, Hebei39.490 N, 118.682 EGrassPeciHE17A01OM372912Penicillium citrinum
SicyHE17A02OM372913Simplicillium cylindrosporum
PulaHE17A03OM372914Purpureocillium lavendulum
OrchardPula sp. HE17B01OM372915Purpureocillium lavendulum
SicyHE17B02OM372916Simplicillium cylindrosporum
BebaHE17B03OM372917Beauveria bassiana
PoplarSimiHE17C01OM372918Simplicillium minatense
MemaHE17C02OM372919Metarhizium marquandii
HE18Tangshan, Hebei39.408 N, 117.954 ECropPulaHE18A01OM372920Purpureocillium lavendulum
TatrHE18B01OM372921Talaromyces trachyspermus
Pula sp. HE18B02OM372922Purpureocillium lavendulum
TrteHE18B03OM372923Trichurus terrophilus
PoplarMeanHE18C01OM372924Metarhizium anisopliae
HE19Tianjin, Hebei38.768 N, 117.184 ECropMeanHE19A01OM372925Metarhizium anisopliae
NemaHE19A02OM372926Nectria mauritiicola
OrchardPula sp. HE19B01OM372927Purpureocillium lavendulum
MeanHE19B02OM372928Metarhizium anisopliae
HE20Cangzhou, Hebei38.151 N, 115.740 ECropPulaHE20A01OM372929Purpureocillium lavendulum
MemaHE20A02OM372930Metarhizium marquandii
GrassMeanHE20B01OM372931Metarhizium anisopliae
HE21Hengshui, Hebei37.719 N, 115.193 ECropPemiHB21A01OM372932Penicillium mirabile
GrassPechHE21B01OM372933Penicillium chrysogenum
Pula sp. HE21B02OM372934Purpureocillium lavendulum
MemaHE21B03OM372935Metarhizium marquandii
HE22Handan, Hebei36.804 N, 115.193 ECropClroHE22A01OM372936Clonostachys rosea
MemaHe22B01OM372937Metarhizium marquandii
HA01Xinxiang, Henan35.268 N, 113.974 EOrchardHA01A01--
CropMemaHA01B01OM372938Metarhizium marquandii
Grass----
HA02Linzhou, Henan35.994 N, 113.758 NCropPulaHA02A01OM372939Purpureocillium lavendulum
MeanHA02B01OM372940Metarhizium anisopliae
ArborPulaHA02C01OM372941Purpureocillium lavendulum
HA03Linzhou, Henan35.928 N, 113.655 ECrop----
HA04Puyang, Henan36.090 N, 115.124 ECropTrteHA04A01OM372942Trichurus terrophilus
MemaHA04B01OM372943Metarhizium marquandii
HA04B02--
GrassPula sp. HA04C01OM372944Purpureocillium lavendulum
HA05Kaifeng, Henan34.790 N, 114.485 ECrop----
GrassPulaHA05B01OM372945Purpureocillium lavendulum
BebaHA05B02OM372946Beauveria bassiana
CropMema sp. HA05C01OM372947Metarhizium marquandii
TavaHA05C02OM372948Talaromyces variabilis
HA06Kaifeng, Henan34.895 N, 114.328 ECropMemaHA06A01OM372949Metarhizium marquandii
PulaHA06A02OM372950Purpureocillium lavendulum
HA06A03--
PoplarOifuHA06B01OM372951Oidiodendron fuscum
HA06B02--
GrassPulaHA06C01OM372952Purpureocillium lavendulum
ChloHA06C02OM372953Chrysosporium lobatum
MeanHA06C03OM372954Metarhizium anisopliae
HA07Zhengzhou, Henan34.481 N, 113.030 EArborMemaHA07A01OM372955Metarhizium marquandii
OrchardPeciHA07B01OM372956Penicillium citrinum
Pula sp. HA07B02OM372957Purpureocillium lavendulum
CropPeguHA07C01OM372958Penicillium guttulosum
HA08Luoyang, Henan34.555 N, 112.873 ECropPulaHA08A01OM372959Purpureocillium lavendulum
MemaHA08A02OM372960Metarhizium marquandii
PulaHA08B01OM372961Purpureocillium lavendulum
MeanHA08B02OM372962Metarhizium anisopliae
MemaHA08B03OM372963Metarhizium marquandii
PulaHA08C01OM372964Purpureocillium lavendulum
MemaHA08C02OM372965Metarhizium marquandii
HA09Luoyang, Henan34.768 N, 112.093 ECropPulaHA09A01OM372966Purpureocillium lavendulum
MeanHA09A02OM372967Metarhizium anisopliae
PoplarMemaHA09B01OM372968Metarhizium marquandii
MeanHA09B02OM372969Metarhizium anisopliae
PulaHA09B03OM372970Purpureocillium lavendulum
HA10Sanmenxia, Henan34.797 N, 111.243 ECropPulaHA10A01OM372971Purpureocillium lavendulum
MeanHA10A02OM372972Metarhizium anisopliae
Pula sp. HA10B01OM372973Purpureocillium lavendulum
MemaHA10B02OM372974Metarhizium marquandii
MeanHA10B03OM372975Metarhizium anisopliae
HA11Sanmenxia, Henan34.626 N, 110.914 ECropMemaHA11A01OM372976Metarhizium marquandii
MeanHA11A02OM372977Metarhizium anisopliae
PulaHA11A03OM372978Purpureocillium lavendulum
PulaHA11B01OM372979Purpureocillium lavendulum
Grass----
HA12Nanyang, Henan33.566 N, 111.185 ECropPula sp. HA12A01OM372980Purpureocillium lavendulum
Mema sp. HA12A02OM372981Metarhizium marquandii
BebaHA12B01OM372982Beauveria bassiana
PuliHA12B02OM372983Purpureocillium lilacinum
TrteHA12B03OM372984Trichurus terrophilus
GrassPulaHA12C01OM372985Purpureocillium lavendulum
HA13Nanyang, Henan33.072 N, 111.792 ECrop------
PuliHA13B01OM372986Purpureocillium lilacinum
HA13B02----
HA14Nanyang, Henan32.780 N, 112.707 ECropPulaHA14A01OM372987Purpureocillium lavendulum
NemaHA14B01OM372988Nectria mauritiicola
GrassMemaHA14C01OM372989Metarhizium marquandii
HA15Xinyang, Henan32.401 N, 113.931 ECropPulaHA15A01OM372990Purpureocillium lavendulum
ChasHA15A02OM372991Chloridium aseptatum
GrassPulaHA15C01OM372992Purpureocillium lavendulum
HA16Xinyang, Henan32.338 N, 114.128 ECropPulaHA16A01OM372993Purpureocillium lavendulum
MaauHA16A02OM372994Malbranchea aurantiaca
GrassPulaHA16C01OM372995Purpureocillium lavendulum
HA17Zhumadian, Henan32.707 N, 114.109 ECropPulaHA17A01OM372996Purpureocillium lavendulum
MemaHA17B01OM372997Metarhizium marquandii
PulaHA17B02OM372998Purpureocillium lavendulum
GrassHA17C01----
PulaHA17C02OM372999Purpureocillium lavendulum
HA18Luohe, Henan33.510 N, 113.980 ECropPulaHA18A01OM373000Purpureocillium lavendulum
Pula sp. HA18B01OM373001Purpureocillium lavendulum
HA18B02--
GrassMeanHA18C01OM373002Metarhizium anisopliae
PulaHA18C02OM373003Purpureocillium lavendulum
MemaHA18C03OM373004Metarhizium marquandii
HA19Pingdingshan, Henan33.652 N, 113.370 ECropMeanHA19A01OM373005Metarhizium anisopliae
PulaHA19A02OM373006Purpureocillium lavendulum
MeanHA19B01OM373007Metarhizium anisopliae
PulaHA19B02OM373008Purpureocillium lavendulum
GrassMemaHA19C01OM373009Metarhizium marquandii
Pula sp. HA19C02OM373010Purpureocillium lavendulum
AssyHA19C03OM373011Aspergillus sydowii
HA20Xuchang, Henan34.052 N, 113.709 ECropMemaHA20A01OM373012Metarhizium marquandii
MemaHA20B01OM373013Metarhizium marquandii
GrassPulaHA20C01OM373014Purpureocillium lavendulum
MemaHA20C02OM373015Metarhizium marquandii
BebaHA20C03OM373016Beauveria bassiana
HA21Zhoukou, Henan33.978 N, 114.867 ECropPulaHA21A01OM373017Purpureocillium lavendulum
MemaHA2102OM373018Metarhizium marquandii
GrassPula sp. HA21B01OM373019Purpureocillium lavendulum
PeciHA21B02OM373020Penicillium citrinum
HA22Shangqiu, Henan34.350 N, 115.572 ECropHA22A01--
BebaHA22A02OM373021Beauveria bassiana
PuliHA22B01OM373022Purpureocillium lilacinum
GrassPuliHA22C01OM373023Purpureocillium lilacinum
HA23Shangqiu, Henan34.596 N, 115.109 ECropTapuHA23A01OM373024Talaromyces purpureogenus
MemaHA23B01OM373025Metarhizium marquandii
HA23B02--
OrchardPemiHA23C01OM373026Penicillium mirabile
HA24Kaifeng, Henan34.771 N, 114.806 ECropMemaHA24A01OM373027Metarhizium marquandii
PulaHA24A02OM373028Purpureocillium lavendulum
PuliHA24B01OM373029Purpureocillium lilacinum
HA25Zhengzhou, Henan34.838 N, 114.036 ECropPeciHA25A01OM373030Penicillium citrinum
MeanHA25A02OM373031Metarhizium anisopliae
GrassMeanHA25B01OM373032Metarhizium anisopliae
PuliHA25B02OM373033Purpureocillium lilacinum
CropMeanHA25C01OM373034Metarhizium anisopliae
PoplarMemaHA25D01OM373035Metarhizium marquandii
HA25D02--

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Diversity 14 00464 g001 550
Figure 1. Phylogenetic tree of Purpureocillium spp. (A) and Metarhizium spp. (B) isolates.
Figure 1. Phylogenetic tree of Purpureocillium spp. (A) and Metarhizium spp. (B) isolates.
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Diversity 14 00464 g002 550
Figure 2. Phylogenetic tree of Penicillium spp. (A) and Aspergillus spp. (B) isolates.
Figure 2. Phylogenetic tree of Penicillium spp. (A) and Aspergillus spp. (B) isolates.
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Diversity 14 00464 g003 550
Figure 3. Phylogenetic tree of Talaromyces spp. (A) and Beauveria/Isaria (B) isolates.
Figure 3. Phylogenetic tree of Talaromyces spp. (A) and Beauveria/Isaria (B) isolates.
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Diversity 14 00464 g004 550
Figure 4. Phylogenetic tree of Lecanicillium/Simplicillium spp. (A) and Fusarium/Coniochaeta/Clonostachys (B) isolates.
Figure 4. Phylogenetic tree of Lecanicillium/Simplicillium spp. (A) and Fusarium/Coniochaeta/Clonostachys (B) isolates.
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Diversity 14 00464 g005 550
Figure 5. Phylogenetic tree of other isolates.
Figure 5. Phylogenetic tree of other isolates.
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Diversity 14 00464 g006 550
Figure 6. The attachment of conidia of I. javanica on the body surface after inoculation for 2 h. (A) Chest internode; (B) hind foot internode; (C) foot end.
Figure 6. The attachment of conidia of I. javanica on the body surface after inoculation for 2 h. (A) Chest internode; (B) hind foot internode; (C) foot end.
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Diversity 14 00464 g007 550
Figure 7. SEM observations of the inoculation of I. javanica for 12–24 h. (A) Spores germinate to form a short dental canal; (B) apical expansion to form an adherent cell; (C) adnexal extension; (D) bud tube invades the body wall.
Figure 7. SEM observations of the inoculation of I. javanica for 12–24 h. (A) Spores germinate to form a short dental canal; (B) apical expansion to form an adherent cell; (C) adnexal extension; (D) bud tube invades the body wall.
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Diversity 14 00464 g008 550
Figure 8. SEM observations of the inoculation of I. javanica for 48–72 h. (A) At 48 h, hyphae grew between the foot nodes, and new conidiophores and new conidia were formed. (B) At 60 h, conidia germination in vitro produced new hyphae covering the hindfoot. (C) At 72 h, the end of the foot was covered with mycelia. (D) At 72 h, the hind foot was covered with mycelia.
Figure 8. SEM observations of the inoculation of I. javanica for 48–72 h. (A) At 48 h, hyphae grew between the foot nodes, and new conidiophores and new conidia were formed. (B) At 60 h, conidia germination in vitro produced new hyphae covering the hindfoot. (C) At 72 h, the end of the foot was covered with mycelia. (D) At 72 h, the hind foot was covered with mycelia.
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Diversity 14 00464 g009 550
Figure 9. Mycelial growth of Phyllotreta striolata infected by I. javanica. (A) 3 d; (B) 4 d; (C) 5 d; (D) 6 d; (E) 7 d.
Figure 9. Mycelial growth of Phyllotreta striolata infected by I. javanica. (A) 3 d; (B) 4 d; (C) 5 d; (D) 6 d; (E) 7 d.
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Table
Table 1. The information of referred fungal strains.
Table 1. The information of referred fungal strains.
Strain/VoucherGenBank Accession NumberGeographic OriginReference
Acremonium exuviarumNR_077167Canada[30]
Acrophialophora nainiana CBS 417.67MK926894ChinaUnpublished
Apiotrichum cacaoliposimilis ATCC 20505NR_154671USA[31]
Arthrographis kalraeAB506810Japan[32]
Arthropsis hispanica CBS 351.92THE965759Spain[33]
Aspergillus auricomus NRRL 391NR_135388USA[34]
Aspergillus crustosus NRRL 4988NR_135366USA[34]
Aspergillus fumigatus ATCC 1022NR_121481USA[30]
Aspergillus granulosus NRRL 1932NR_135348USA[30]
Aspergillus niger ATCC 16888NR_111348USA[30]
Aspergillus nomius NRRL 13137NR_121218USA[30]
Aspergillus pseudodeflectus NRRL 6135NR_135372USA[34]
Aspergillus sclerotiorum NRRL 415NR_131294USA[34]
Aspergillus sydowii CBS 593.65NR_131259JapanUnpublished
Aspergillus tanneri ATCC MYA-4905NR_111840USA[30]
Aspergillus terreus var. subfloccosus CBS 117.37NR_149331Netherlands[35]
Aspergillus udagawae CBM FA-0702NR_137442JapanUnpublished
Auxarthron alboluteum UAMH 2846NR_111137Canada[30]
Beauveria bassiana ARSEF 1564NR_111594USA[30]
Beauveria bassiana ARSEF 8187HQ444271Canada[30]
Beauveria bassiana CBS 465.70MH859798Netherlands[36]
Beauveria bassiana CBS 110.25MH854802Sri Lanka[36]
Beauveria pseudobassiana ARSEF 3405NR_111598USA[30]
Chloridium aseptatum MFLU 11-1051NR_158365China[37]
Chrysosporium lobatum CBS 666.78NR_111087Spain[30]
Clonostachys grammicospora CBS 209.93NR_137650Netherlands[38]
Clonostachys rosea f. catenulata CBS 154.27NR_145021Netherlands[38]
Coniochaeta fasciculata CBS 205.38NR_154770SpainUnpublished
Cordyceps cateniannulata CBS 152.83NR_111169Thailand[30]
Cunninghamella elegans CBS 160.28NR_154747China[39]
Cutaneotrichosporon dermatis CBS 2043NR_130667USAUnpublished
Fusarium falciforme CBS 475.67NR_164424Netherlands[40]
Fusarium keratoplasticum FRC S-2477NR_130690USA[41]
Fusarium solani CBS 140079NR_163531Slovenia[42]
Gongronella butleri CBS 102.44JN206284Netherlands[43]
Gongronella butleri CBS 157.25JN206607Netherlands[43]
Hawksworthiomyces taylorii CMW 20741NR_155176South Africa[44]
Isaria cateniannulata ARSEF 6242GU734760Brazil[45]
Isaria farinosa ARSEF 4029HQ880828USA[46]
Isaria farinosa CBS 262.58AY624179Thailand[47]
Isaria fumosorosea ARSEF 887EU553334Brazil[48]
Isaria fumosorosea CBS 244.31AY624182Thailand[47]
Isaria fumosorosea CBS 337.52EF411219ThailandUnpublished
Isaria javanica CBS 134.22DQ403723USA[49]
Isaria javanica CHE-CNRCB 303/2KM234213Mexico[50]
Lecanicillium coprophilum CGMCC 3.18986NR_163303China[51]
Lecanicillium saksenae IMI 179841NR_111102United Kingdom[30]
Malbranchea aurantiaca CBS 127.77AB040704Japan[52]
Melanoctona tectonae MFLUCC 12-0389NR_154194ThailandUnpublished
Metarhizium anisopliae CBS 657.67MH859066Netherlands[36]
Metarhizium flavoviride CBS 218.56MH857590Czech[36]
Metarhizium marquandii CBS 282.53MH857200Netherlands[36]
Metarhizium marquandii CBS 182.27NR_131994Thailand[47]
Metarhizium carneum CBS 239.32NR_131993Thailand[47]
Metapochonia bulbillosa 38G272EU999952USA[53]
Metapochonia bulbillosa CBS 145.70AJ292397UK[54]
Metapochonia bulbillosa FKI-4395AB709836Japan[55]
Mucor ellipsoideus ATCC MYA-4767NR_111683USA[55]
Nectria mauritiicola NHRC-FC048AJ558115RussiaUnpublished
Oidiodendron fuscum UAMH 8511NR_111035Canada[30]
Paecilomyces formosus CBS 990.73BNR_149329Netherlands[56]
Paecilomyces variotii CBS 338.51FJ389930Netherlands[56]
Penicillium chrysogenum CBS 306.48NR_077145USA[30]
Penicillium subrubescens CBS 132785NR_111863Netherlands[30]
Penicillium rubens CBS 319.59MH857874Netherlands[30]
Penicillium rubens CBS 129667NR_111815Netherlands[30]
Penicillium guttulosum NRRL 907NR_144820USA[57]
Penicillium citrinum NRRL 1841NR_121224USA[30]
Penicillium mirabile CBS 624.72JN899322Netherlands[58]
Phialophora livistonae CPC 19433NR_111824Netherlands[30]
Purpureocillium lilacinum CBS 284.36 NR_111432 USA[30]
Purpureocillium lavendulum FMR 10376NR_111433Spain[30]
Simplicillium cylindrosporum JCM 18169NR_111023Japan[30]
Simplicillium minatense JCM 18176NR_111025Japan[30]
Talaromyces pinophilus CBS 631.66NR_111691Netherlands[30]
Talaromyces purpureogenus CBS 286.36NR_121529Netherlands[30]
Talaromyces trachyspermus CBS 373.48NR_147425Netherlands[30]
Talaromyces variabilis CBS 385.48NR_103670Netherlands[30]
Tolypocladium album CBS 869.73NR_155018JapanUnpublished
Trichurus terrophilus CBS 368.53LN850976SpainUnpublished
Table
Table 2. The fungi isolation and biodiversity of different regions.
Table 2. The fungi isolation and biodiversity of different regions.
RegionSoil Sample
Numbers		Isolate NumberIsolation Rate (%)EPF
Species		SHEI
FungiEPFFungiEPF
Hunan54973985.1962.9690.87
Hubei50582480.0040.0080.88
Henan63738398.4190.4870.84
Hebei59744271.1954.2480.78
Total22630218883.70 *61.92 *11--
* The mean isolation rate (%) of all regions. EPF: Entomopathogenic fungi; SHEI: Shannon evenness index.
Table
Table 3. The fungi isolation and biodiversity of different samples.
Table 3. The fungi isolation and biodiversity of different samples.
RegionSoil Sample
Numbers		Isolate NumberIsolation Rate (%)EPF
Species		SHEI
FungiEPFFungiEPF
Arbor64794579.6959.3890.86
Crop851148384.7169.4190.76
Fallow land9126100.0055.5661.00
Grass68975485.2960.2990.81
Total22630218887.42 *61.16 *11--
* The mean isolation rate (%) of all vegetation types sampled. EPF: Entomopathogenic fungi, SHEI: Shannon evenness index. Arbor: lands covered with arbor forests; cropland: farming lands planted with crops; fallow land: farming lands with no crops; grass: lands covered with grass.
Table
Table 4. The pathogenicity of fungal isolates against adults of P. striolata.
Table 4. The pathogenicity of fungal isolates against adults of P. striolata.
Isolated StrainSpeciesAdjusted Mortality (%)
ApcaHN2402Apiotrichum cacaoliposimilis12.96 ± 0.56
AsgrHB3004Aspergillus granulosus26.19 ± 0.24
AsnoHB27S02Aspergillus nomius21.05 ± 0.72
AsnoHN03S02Aspergillus nomius12.96 ± 0.57
AspsHB3002Aspergillus pseudodeflectus21.88 ± 0.85
AsscHN1502Aspergillus sclerotiorum7.55 ± 0.35
AssyHE06A03Aspergillus sydowii19.30 ± 0.38
AstaHN1501Aspergillus tanneri45.24 ± 0.39
AsteHN01S02Aspergillus terreus15.71 ± 0.73
AsudHE13C01Aspergillus udagawae16.00 ± 0.44
BebaHA22A02Beauveria bassiana10.70 ± 0.19
ChasHA15A02Chloridium aseptatum1.28 ± 0.51
CudeHN1202Cutaneotrichosporon dermatis2.83 ± 0.10
FufaHN1901Fusarium falciforme28.07 ± 0.68
IsjaHB2602Isaria javanica9.52 ± 0.30
IsjaHN3002Isaria javanica67.86 ± 0.61
LecoHE07B01Lecanicillium coprophilum18.18 ± 0.33
LesaHB28S05Lecanicillium saksenae26.32 ± 0.45
MeanHE15B01Metarhizium anisopliae23.56 ± 0.37
MeanHE20B01Metarhizium anisopliae19.62 ± 0.45
MemaHA24A01Metarhizium marquandii4.55 ± 0.42
MemaHN26S01Metarhizium marquandii22.81 ± 0.91
Mema sp. HN2501Metarhizium marquandii5.63 ± 0.41
MeteHN13S01Melanoctona tectonae15.00 ± 1.12
MuelHB24N03Mucor ellipsoideus15.00 ± 0.60
NemaHA14B01Nectria mauritiicola16.33 ± 0.30
OifuHA06B01Oidiodendron fuscum1.85 ± 0.19
PeciHA25A01Penicillium citrinum9.74 ± 0.29
PesuHN1002Penicillium subrubescens6.67 ± 0.27
PhliHN2702Phialophora livistonae16.33 ± 0.57
PulaHA08C01Purpureocillium lavendulum3.92 ± 0.30
SicyHE17A02Simplicillium cylindrosporum15.00 ± 0.27
SimiHE17C01Simplicillium minatense8.16 ± 0.23
TapiHB23G01Talaromyces pinophilus7.02 ± 0.16
TapiHB23S01Talaromyces pinophilus31.58 ± 0.32
TatrHE03C03Talaromyces trachyspermus11.11 ± 0.20
TatrHE14A01Talaromyces trachyspermus6.56 ± 0.44
TatrHE18B01Talaromyces trachyspermus8.33 ± 0.21
ToalHN15S03Tolypocladium album11.67 ± 0.65
HA13B02–2.27 ± 0.31
HA17C01–11.43 ± 0.18
HB3003–23.81 ± 0.34
HB3102–8.87 ± 0.69
HE07A01–14.81 ± 0.32
HN06Y05–14.81 ± 0.41
HN20Z01–7.41 ± 0.23
HN28J01–1.96 ± 0.22
Control–3.33 ± 0.45
Data in the table are mean values ± standard error. For each test, 20 P. striolata samples were used in each treatment, and the concentration of the fungal spore suspension was 1.0 × 108 spores/mL. The experiment was repeated three times.
Table
Table 5. Pathogenicity of I. javanica in different concentrations against P. striolata.
Table 5. Pathogenicity of I. javanica in different concentrations against P. striolata.
Concentration
(Spores/mL)		Accumulated Mortality (%) Muscardine Cadaver Rate (%)
1 d3 d7 d1 d3 d7 d
CK3.33 ± 2.36 c6.67 ± 2.36 c10.00 ± 4.08 d000
1.0 × 10410.00 ± 4.08 bc18.33 ± 2.36 b40.00 ± 4.08 c006.67 ± 4.71 c
1.0 × 10515.00 ± 0 ab23.33 ± 2.36 b41.67 ± 2.36 c0011.67 ± 4.71 c
1.0 × 10613.33 ± 6.23 abc20.00 ± 4.08 b53.33 ± 4.71 b01.67 ± 2.36 b21.67 ± 6.23 b
1.0 × 10721.67 ± 8.5 a33.33 ± 6.23 a61.67 ± 4.71 b03.33 ± 2.36 b26.67 ± 2.36 b
1.0 × 10823.33 ± 2.36 a36.67 ± 4.71 a80.00 ± 4.08 a08.33 ± 2.36 a41.67 ± 2.36 a
Muscardine cadavers were dead insects that grew mycelium. Accumulated mortality includes all dead insects. The data are the mean ± SE on different days after treatment. Different letters indicate a significant difference (p < 0.05) determined by DMRT.
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Zhang, K.; Zhang, X.; Hu, Q.; Weng, Q. Entomopathogenic Fungi in the Soils of China and Their Bioactivity against Striped Flea Beetles Phyllotretastriolata. Diversity 2022, 14, 464. https://doi.org/10.3390/d14060464

AMA Style

Zhang K, Zhang X, Hu Q, Weng Q. Entomopathogenic Fungi in the Soils of China and Their Bioactivity against Striped Flea Beetles Phyllotretastriolata. Diversity. 2022; 14(6):464. https://doi.org/10.3390/d14060464

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Zhang, Ke, Xiaofeng Zhang, Qiongbo Hu, and Qunfang Weng. 2022. "Entomopathogenic Fungi in the Soils of China and Their Bioactivity against Striped Flea Beetles Phyllotretastriolata" Diversity 14, no. 6: 464. https://doi.org/10.3390/d14060464

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