Publications by authors named "Tom Hsiang"

91 Publications

Deep Sequencing, Nested PCR, and Denaturing Gradient Gel Electrophoresis Reveal a Wider Distribution of Chinese Caterpillar Mushroom, Ophiocordyceps sinensis (Ascomycetes), in Native Soil Types.

Int J Med Mushrooms 2021 ;23(4):93-104

State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; ITPB-IMCAS Key Joint Laboratory of Alpine Fungi, Lhasa, China.

Ophiocordyceps sinensis appears as stroma emerging from underground sclerotium enclosed by the skeleton of Thitarodes moth larvae. However, the actual distribution of the fungus in soil still remains unclarified. In this study, 40 soil samples were used for detection of O. sinensis to confirm its distribution in native habitats using denaturing gradient gel electrophoresis, nested internal transcribed spacer (ITS) PCR, and 454 pyrosequencing methods. The soil samples included six types: Os, where both stromata and host moth larvae were found; NL, representing no signs of stromata, but where moth larvae were found; NOs, where neither stroma nor moth larvae were found; BS, with bare soil without the presence of stroma of O. sinensis or moth larvae; AF, from soil surrounding the stroma; and MP, soil particles firmly wrapping the sclerotium of O. sinensis. Of 40 samples tested, 36 showed positive detection of O. sinensis by at least one of the three detection methods, with positive detection in all six sample types at all five sites. The results showed that traces of O. sinensis can be detected in locations with no macroscopically visible evidence of the fungus or its host and at least 100 m away from such locations.
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http://dx.doi.org/10.1615/IntJMedMushrooms.2021037759DOI Listing
January 2021

Evolutionary and genomic comparisons of hybrid uninucleate and nonhybrid Rhizoctonia fungi.

Commun Biol 2021 Feb 15;4(1):201. Epub 2021 Feb 15.

Key Laboratory of Pest Monitoring and Green Management, MOA; Joint Laboratory for International Cooperation in Crop Molecular Breeding; Department of Plant Pathology, China Agricultural University, Beijing, China.

The basidiomycetous fungal genus, Rhizoctonia, can cause severe damage to many plants and is composed of multinucleate, binucleate, and uninucleate species differing in pathogenicity. Here we generated chromosome-scale genome assemblies of the three nuclear types of Rhizoctonia isolates. The genomic comparisons revealed that the uninucleate JN strain likely arose by somatic hybridization of two binucleate isolates, and maintained a diploid nucleus. Homeolog gene pairs in the JN genome have experienced both decelerated or accelerated evolution. Homeolog expression dominance occurred between JN subgenomes, in which differentially expressed genes show potentially less evolutionary constraint than the genes without. Analysis of mating-type genes suggested that Rhizoctonia maintains the ancestral tetrapolarity of the Basidiomycota. Long terminal repeat-retrotransposons displayed a reciprocal correlation with the chromosomal GC content in the three chromosome-scale genomes. The more aggressive multinucleate XN strain had more genes encoding enzymes for host cell wall decomposition. These findings demonstrate some evolutionary changes of a recently derived hybrid and in multiple nuclear types of Rhizoctonia.
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http://dx.doi.org/10.1038/s42003-021-01724-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7884421PMC
February 2021

Comprehensive transcriptome profiling reveals abundant long non-coding RNAs associated with development of the rice false smut fungus, Ustilaginoidea virens.

Environ Microbiol 2021 Feb 15. Epub 2021 Feb 15.

Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, Wuhan, 430070, China.

Long non-coding RNAs (lncRNAs) play an important role in biological processes but regulation and function of lncRNAs remain largely unelucidated, especially in fungi. Ustilaginoidea virens is an economically important fungus causing a devastating disease of rice. By combining microscopic and RNA-seq analyses, we comprehensively characterized lncRNAs of this fungus in infection and developmental processes and defined four serial typical stages. RNA-seq analyses revealed 1724 lncRNAs in U. virens, including 1084 long intergenic non-coding RNAs (lincRNAs), 51 intronic RNAs (incRNAs), 566 natural antisense transcripts (lncNATs) and 23 sense transcripts. Gene Ontology enrichment of differentially expressed lincRNAs and lncNATs demonstrated that these were mainly involved in transport-related regulation. Functional studies of transport-related lncRNAs revealed that UvlncNAT-MFS, a cytoplasm localized lncNAT of a putative MFS transporter gene, UvMFS, could form an RNA duplex with UvMFS and was required for regulation of growth, conidiation and various stress responses. Our results were the first to elucidate the lncRNA profiles during infection and development of this important phytopathogen U. virens. The functional discovery of the novel lncRNA, UvlncNAT-MFS, revealed the potential of lncRNAs in regulation of life processes in fungi.
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http://dx.doi.org/10.1111/1462-2920.15432DOI Listing
February 2021

iTRAQ-based quantitative proteomics reveals ChAcb1 as a novel virulence factor in Colletotrichum higginsianum.

Phytopathology 2021 Feb 10. Epub 2021 Feb 10.

Huazhong Agricultural University, 47895, College of Plant Science & Technology, Wuhan, Hubei , China;

Colletotrichum higginsianum is an important hemibiotrophic fungal pathogen that causes anthracnose disease on various cruciferous plants. Discovery of new virulence factors could lead to strategies for effectively controlling anthracnose. Acyl-CoA binding proteins (ACBPs) are mainly involved in binding and trafficking acyl-CoA esters in eukaryotic cells. However, the functions of this important class of proteins in plant fungal pathogens remain unclear. In this study, we performed an iTRAQ-based quantitative proteomic analysis to identify differentially expressed proteins (DEPs) between a nonpathogenic mutant ΔCh-MEL1 and the wild-type. Based on iTRAQ data, DEPs in the ΔCh-MEL1 mutant were mainly associated with melanin biosynthesis, carbohydrate and energy metabolism, lipid metabolism, redox processes, and amino acid metabolism. Proteomic analysis revealed that many DEPs might be involved in growth and pathogenesis of C. higginsianum. Among them, an acyl-CoA binding protein, ChAcb1, was selected for further functional studies. Deletion of ChAcb1 caused defects in vegetative growth and conidiation. ChAcb1 is also required for response to hyperosmotic and oxidative stresses, and maintenance of cell wall integrity. Importantly, the ΔChAcb1 mutant exhibited reduced virulence, and microscopic examination revealed that it was defective in appressorial penetration and infectious growth. Furthermore, the ΔChAcb1 mutant was impaired in fatty acid and lipid metabolism. Taken together, ChAcb1 was identified as a new virulence gene in this plant pathogenic fungus.
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http://dx.doi.org/10.1094/PHYTO-01-21-0028-RDOI Listing
February 2021

ATAC-seq Data for Genome-Wide Profiling of Transcription Factor Binding Sites in the Rice False Smut Fungus Ustilaginoidea virens.

Mol Plant Microbe Interact 2021 Feb 8. Epub 2021 Feb 8.

Huazhong Agricultural University, 47895, College of Plant Science & Technology, No. 1 Shizishan Street, Hongshan District, Wuhan, China, 430070;

Identification of transcription factor binding-sites is one of the most important steps in understanding the function of transcription factors and regulatory networks in organisms. The Assay for Transposase Accessible Chromatin Sequencing (ATAC-seq) is a simple protocol for detection of open chromatin, which could be a powerful tool to advance studies of protein:DNA interactions. Although ATAC-seq has been used in systematic identification of cis-regulatory regions in animal and plant genomes, this method has been rarely applied in fungi. Here, we describe a valuable ATAC-seq resource in the genome of an economically important phytopathogen, the rice false smut fungus, Ustilaginoidea virens. The ATAC-seq data of U. virens mycelia collected from potato sucrose broth (PSB) and PSB supplied with rice spikelet extract (RSE) were both generated. This is the first genome-wide profiling of open chromatin and transcription factor binding sites in U. virens.
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http://dx.doi.org/10.1094/MPMI-01-21-0006-ADOI Listing
February 2021

Biocontrol Using PP19 Against Litchi Downy Blight Caused by .

Front Microbiol 2020 12;11:619423. Epub 2021 Jan 12.

Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization (MOA), Guangdong Province Key Laboratary of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, China.

has been widely used in the agriculture, food, and medicine industries. Isolate PP19 was obtained from the litchi fruit carposphere and showed biocontrol efficacy against litchi downy blight (LDB) whether applied preharvest or postharvest. To further understand the underlying regulatory mechanisms, the genome of PP19 was sequenced and analyzed. The genome comprised a 3,847,565 bp circular chromosome containing 3990 protein-coding genes and 121 RNA genes. It has the smallest genome among 36 sequenced strains of except for RD7-7. In whole genome phylogenetic analysis, PP19 was clustered into a group with known industrial applications, indicating that it may also produce high-yield metabolites that have yet to be identified. A large chromosome structural variation and large numbers of single nucleotide polymorphisms (SNPs) between PP19 (industrial strain) and UMAF6639 (plant-associated strain) were detected through comparative analysis, which may shed light on their functional differences. Preharvest treatment with PP19 enhanced resistance to LDB, by decreasing the plant HO content and increasing the SOD activity. This is the first report of an industrial strain of showing a plant-associated function and with major potential for the biocontrol of LDB.
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http://dx.doi.org/10.3389/fmicb.2020.619423DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835641PMC
January 2021

Fusarium species associated with leaf spots of mango in China.

Microb Pathog 2021 Jan 13;150:104736. Epub 2021 Jan 13.

Plant Breeding Institute, University of Sydney, Cobbitty, NSW, 2570, Australia.

Mango is one of the important commercially cultivated fruit crops in southern China. In continuing research on foliar diseases of mango in south of China during 2016-2017, leaf spot disease was common at all mango orchards investigated. The purpose of this study was to investigate Fusarium species associated with leaf spots of mango in the main production areas of China, and to identify them to species. Twenty-two Fusarium isolates were obtained from diseased leaves from seven provinces (Fujian, Guangdong, Guangxi, Guizhou, Hainan, Sichuan and Yunnan), and then identified using morphological characteristics and phylogenetic analysis. These isolates were from seven species: F. concentricum, F. hainanense, F. mangiferae, F. pernambucanum, F. proliferatum, F. sulawesiense, and F. verticillioides. We found all 22 isolates to be capable of causing leaf spot symptoms on artificially wounded leaves. To our knowledge, this is the first report of F. concentricum, F. hainanense, F. mangiferae, F. pernambucanum, F. sulawesiense and F. verticillioides associated with leaf spots on mango in China, and the first for F. concentricum, F. hainanense, F. pernambucanum, F. sulawesiense from mango worldwide. This is one of the few reports on Fusarium species as potential causal agents of mango leaf spots.
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http://dx.doi.org/10.1016/j.micpath.2021.104736DOI Listing
January 2021

Comprehensive identification of lysine 2-hydroxyisobutyrylated proteins in Ustilaginoidea virens reveals the involvement of lysine 2-hydroxyisobutyrylation in fungal virulence.

J Integr Plant Biol 2021 Feb;63(2):409-425

Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, Wuhan, 430070, China.

Lysine 2-hydroxyisobutyrylation (K ) is a newly identified post-translational modification (PTM) that plays important roles in transcription and cell proliferation in eukaryotes. However, its function remains unknown in phytopathogenic fungi. Here, we performed a comprehensive assessment of K in the rice false smut fungus Ustilaginoidea virens, using Tandem Mass Tag (TMT)-based quantitative proteomics approach. A total of 3 426 K sites were identified in 977 proteins, suggesting that K is a common and complex PTM in U. virens. Our data demonstrated that the 2-hydroxyisobutyrylated proteins are involved in diverse biological processes. Network analysis of the modified proteins revealed a highly interconnected protein network that included many well-studied virulence factors. We confirmed that the Zn-binding reduced potassium dependency3-type histone deacetylase (UvRpd3) is a major enzyme that removes 2-hydroxyisobutyrylation and acetylation in U. virens. Notably, mutations of K sites in the mitogen-activated protein kinase (MAPK) UvSlt2 significantly reduced fungal virulence and decreased the enzymatic activity of UvSlt2. Molecular dynamics simulations demonstrated that 2-hydroxyisobutyrylation in UvSlt2 increased the hydrophobic solvent-accessible surface area and thereby affected binding between the UvSlt2 enzyme and its substrates. Our findings thus establish K as a major post-translational modification in U. virens and point to an important role for K in the virulence of this phytopathogenic fungus.
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http://dx.doi.org/10.1111/jipb.13066DOI Listing
February 2021

A novel mycovirus infecting Aspergillus nidulans that is closely related to viruses in a new genus of the family Partitiviridae.

Arch Virol 2021 Feb 6;166(2):659-664. Epub 2021 Jan 6.

School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada.

The bisegmented genome of a novel double-stranded (ds) RNA mycovirus, named "Aspergillus nidulans partitivirus 1" (AnPV1), isolated from the fungus Aspergillus nidulans strain HJ5-47, was sequenced and analyzed. AnPV1 contains two segments, AnPV1-1 and AnPV1-2. AnPV1-1 has 1837 bp with an open reading frame (ORF) that potentially encodes a putative RNA-dependent RNA polymerase (RdRp) of 572 amino acids (aa). AnPV1-2 has 1583 bp with an ORF encoding a putative capsid protein (CP) of 488 aa. Phylogenetic analyses indicated that AnPV1 and related viruses clustered in a group that could represent a new unclassified genus in the family Partitiviridae.
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http://dx.doi.org/10.1007/s00705-020-04930-xDOI Listing
February 2021

Detection of Fungi and Oomycetes by Volatiles Using E-Nose and SPME-GC/MS Platforms.

Molecules 2020 Dec 5;25(23). Epub 2020 Dec 5.

Institute of Biological Sciences, Cardinal Stefan Wyszynski University in Warsaw, Wóycickiego 1/3 Street, 01-938 Warsaw, Poland.

Fungi and oomycetes release volatiles into their environment which could be used for olfactory detection and identification of these organisms by electronic-nose (e-nose). The aim of this study was to survey volatile compound emission using an e-nose device and to identify released molecules through solid phase microextraction-gas chromatography/mass spectrometry (SPME-GC/MS) analysis to ultimately develop a detection system for fungi and fungi-like organisms. To this end, cultures of eight fungi (, , , , , , , ) and four oomycetes (, , , ) were tested with the e-nose system and investigated by means of SPME-GC/MS. Strains of , and appeared to be the most odoriferous. All investigated fungal species (except ) produced sesquiterpenes in variable amounts, in contrast to the tested oomycetes strains. Other molecules such as aliphatic hydrocarbons, alcohols, aldehydes, esters and benzene derivatives were found in all samples. The results suggested that the major differences between respective VOC emission ranges of the tested species lie in sesquiterpene production, with fungi emitting some while oomycetes released none or smaller amounts of such molecules. Our e-nose system could discriminate between the odors emitted by , , and , which accounted for over 88% of the PCA variance. These preliminary results of fungal and oomycete detection make the e-nose device suitable for further sensor design as a potential tool for forest managers, other plant managers, as well as regulatory agencies such as quarantine services.
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http://dx.doi.org/10.3390/molecules25235749DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7730677PMC
December 2020

The 'pears and lemons' protein UvPal1 regulates development and virulence of Ustilaginoidea virens.

Environ Microbiol 2020 12 23;22(12):5414-5432. Epub 2020 Nov 23.

The Key Lab of Plant Pathology of Hubei Province, Huazhong Agricultural University, Wuhan, 430070, China.

Ustilaginoidea virens is an economically important fungus causing a devastating grain disease, rice false smut. An insertional mutagenesis screen was used to explore biological mechanisms underlying infection process of U. virens. T184, a new mutant was identified, with abnormal conidial morphology and deficient virulence. Analysis of the T-DNA inserted gene UvPal1 in the mutant confirmed it as a putative homologue of a cellular morphogenetic protein in yeast, Pal1, whose function has not been well characterized. Deletion of UvPal1 affected hyphal growth, cell morphology, stress adaptation and virulence. UvPal1 could interact with the endocytic proteins, UvEde1 and UvSla2, but was not required for receptor-mediated endocytosis. A yeast two-hybrid (Y2H) analysis was further carried out to screen the UvPal1-interacting proteins, resulting in the identification of 16 putative interacting proteins. Interestingly, UvPal1 interacted with a septin protein, UvCdc11 in vivo and in vitro, and also affected subcellular localization of UvCdc11 protein. Deletion of the four core septins impaired the growth, morphogenesis, stress response and virulence. Collectively, effects on cell morphology, oxidative stress response and virulence are similar to those of UvPal1, suggesting that UvPal1 physically interacts with UvCdc11 to mediate the septin complex to maintain the cellular morphology and virulence of U. virens.
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http://dx.doi.org/10.1111/1462-2920.15284DOI Listing
December 2020

Delineating yeast species with genome average nucleotide identity: a calibration of ANI with haplontic, heterothallic Metschnikowia species.

Antonie Van Leeuwenhoek 2020 Dec 13;113(12):2097-2106. Epub 2020 Oct 13.

School of Environmental Sciences, University of Guelph, Guelph, Ontario, N1G 2W1, Canada.

We determined pairwise average nucleotide identity (ANI) values for the genomes of 71 strains assigned to 36 Metschnikowia species, 28 of which were represented by multiple isolates selected to represent the range of genetic diversity of the species, and most of which were defined on the basis of reproductive isolation. Similar to what has been proposed for prokaryote species delineation, an ANI value of 95% emerged as a good guideline for the delineation of yeast species, although some overlap exists, whereby members of a reproductive community could have slightly lower values (e.g., 94.3% for M. kamakouana), and representatives of distinct sister species could give slightly higher values (e.g., 95.2% for the sister species M. drakensbergensis and M. proteae). Unlike what is observed in prokaryotes, a sizeable gap between intraspecific and interspecific ANI values was not encountered. Given the ease with which yeast draft genomes can now be obtained, ANI values are poised to become the new standard upon which yeast species may be delineated on genetic distance. As borderline cases exist, however, the delineation of yeast species will continue to require careful evaluation of all available data. We also explore the often-neglected distinction between phylogenetic relatedness and sequence identity through the analysis of a tree constructed from ANI' (100 - ANI) values.
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http://dx.doi.org/10.1007/s10482-020-01480-9DOI Listing
December 2020

First report of causing anthracnose on in China.

Plant Dis 2020 Oct 7. Epub 2020 Oct 7.

University of Guelph, Environmental Sciences, 50 Stone Road East, Guelph, Ontario, Canada, N1G2W1;

(Kunth) Baehni (= A. DC.) is a fruit crop planted in southern China (Gao et al. 2019). It is originally from Central America, and also grown there commercially as well as in some American states (Fadzilah et al. 2018). In March 2019, a leaf spot disease was found on in Baoshan, Yunnan, China. Field surveys were done in a 0.06 ha orchard in Yunnan Province. Leaf spots were found on 90% of six-year-old plants in this field and were observed in other planting areas. The symptoms initially appeared as small, round, brown spots. As the disease developed, the center of the lesions was sunken with a dark brown border (Fig. 1). Under severe conditions, some spots were joined into larger irregular spots, and even whole leaves died. The disease severity of different plants varied, and some leaves showed only a few brown spots while others showed many spots. Small fragments of diseased tissues (3×3 mm) were disinfected in 75% ethanol for 10 s, 1% NaClO for 1 min, and rinsed three times in sterilized water. Then, tissues were placed onto potato dextrose agar (PDA), and incubated at 25°C in the dark for 5 days. Fungal isolates with similar morphology were consistently recovered from diseased tissues. The 25 colonies were initially cottony, pale white to pale gray on the upper side and greyish-green with black zonation on the underside of plates. Conidia were single-celled and hyaline, aseptate, straight, and cylindrical, with rounded ends (Fig. 1B). The length and width of 200 conidia were measured for two representative isolates, DHG-1 and DHG-2, and these averaged 14.48 × 5.59 μm and 14.92 × 5.57 μm. Appressoria were ovoid, sometimes clavate, brown, averaged 7.47 × 5.86 μm and 7.25 × 5.85 μm (n=30). Brown and globose ascocarp were observed on the leaves of . Asci were unitunicate, thin-walled, 6-8 spored, clavate, averaged 51.53×13.01 μm and 50.21 × 13.32 μm (n=30). Ascospores were hyaline, one-celled, slightly curved to curved with obtuse to slightly rounded ends, averaged 14.64×5.97 μm and 15.19 × 6.23 μm (n=30). These two isolates were selected for molecular identification. DNA was extracted from mycelia with the DNA secure Plant Kit (TIANGEN, Biotech, China). For further molecular identification, the internal transcribed spacer (ITS), partial actin (ACT), calmodulin (CAL), chitin synthase (CHS-1), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), beta-tubulin (TUB2), and the Apn2-Mat1-2 intergenic spacer and partial mating type (Mat1-2) gene (ApMat) genes of the strains (DHG-1, DHG-2) were amplified using the primer pairs ITS1/ITS4, ACT-512F/ACT-783R, CL1C/CL2C, CHS-79F/CHS-345R, GDF1/GDR1, T1/Bt-2b, and AM-F/AM-R (Weir et al. 2012; Silva et al. 2012), respectively.The sequences were obtained and compared with GenBank and they all showed over 99% identity to the type strain of ICMP 18581 (Accession nos. JX010165, JX010033, JQ807838, FJ907426, JX010405, JX009866, and FJ917508) (Weir et al. 2012). A phylogenetic tree based on the combined ITS, ACT, CAL, CHS-1, TUB2, GAPDH and ApMat sequences using the Neighbor-joining algorithm revealed that the isolates were (Fig. 2). The sequences were deposited into GenBank with accession MN955541, MN955542, and MN966581 to MN966592. Pathogenicity tests were conducted on eighteen healthy and tender leaves of six 1-year-old plants in a greenhouse. The experiment was repeated twice. The length and width of the inoculated leaves were between 8-13 cm × 2.5-3.6 cm. The epidermis of each tested leaf was lightly scratched in six separate areas with a sterilized needle. Each isolate was inoculated onto at least three wounded leaves by placing 20 μL of a conidial suspension (10 conidia/mL) on the wound sites. Control leaves were also wounded and inoculated with distilled water. All the plants were then sprayed with distilled water and covered with plastic bags. After 10 days, initial symptoms appeared as circular and deep yellow spots. After a few more days, the spots became brown, enlarged to up to 4.0 mm which was similar to symptoms observed in the field, whereas controls remained symptomless. Koch's postulates were fulfilled by re-isolation of from diseased leaves, and identification confirmed by sequencing. has been associated with anthracnose on mango, apple, pear and cassava (Oliveira et al. 2018). To our knowledge, this is the first report of associated with anthracnose of worldwide. These results will provide crucial information for future epidemiological studies and for management of this disease.
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http://dx.doi.org/10.1094/PDIS-02-20-0253-PDNDOI Listing
October 2020

Draft Genome Sequence of Cumin Blight Pathogen .

Plant Dis 2021 Mar 9:PDIS02200224A. Epub 2021 Mar 9.

State Key Laboratory of Crop Stress Biology in Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, Shaanxi Province 712100, China.

The fungal genus consists of highly diverse species. They can be isolated readily from soil, water, and many plants, and even from animals and humans. is a small-spored species of section . It has been reported as a pathogen, an endophyte, and a saprophyte, and can also be found in indoor air. It causes cumin blight, a destructive disease on cumin (), and also causes other serious diseases, such as pumpkin seed rot, date palm leaf spot, wheat leaf spot, and gray spot of . In this study, we sequenced and assembled the first genome of isolate CBS 107.38. The draft genome can be used as a reference for the further study of related pathogens and comparative genomics of species.
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http://dx.doi.org/10.1094/PDIS-02-20-0224-ADOI Listing
March 2021

Molecular networking assisted discovery and biosynthesis elucidation of the antimicrobial spiroketals epicospirocins.

Chem Commun (Camb) 2020 Sep 4;56(70):10171-10174. Epub 2020 Aug 4.

State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China.

Two pairs of dibenzospiroketal racemates, (±)-epicospirocin A (1a/1b) and (±)-1-epi-epicospirocin A (2a/2b), and two (+)-enantiomers of aspermicrones, ent-aspermicrone B (3b) and ent-aspermicrone C (4b), together with two hemiacetal epimeric mixtures, epicospirocin B/1-epi-epicospirocin B (5/6) and epicospirocin C/1-epi-epicospirocin C (7/8), were investigated from the phytopathogenic fungus Epicoccum nigrum 09116 via MS/MS molecular networking guided isolation and chiral separation for the first time. A plausible epicospirocin biosynthetic pathway was elucidated through in silico gene function annotation together with knock-out experiments. This is the first report that has applied MS/MS molecular networking to identify intermediates correlated with a biosynthetic pathway.
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http://dx.doi.org/10.1039/d0cc03990jDOI Listing
September 2020

Chemical Composition and Attractant Activity of Volatiles from to The Spring Aphid .

Molecules 2020 Jul 28;25(15). Epub 2020 Jul 28.

Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education, College of Agriculture, Yangtze University, Jingmi Road 88, Jingzhou 434025, China.

Maxim, a type of sumac, is an economically important tree widely cultivated in mountainous areas of western and central China. A gall, called the bellied gallnut, induced by the aphid, Takagi, is important in the food, medical, and chemical industries in China. Volatiles from were found to attract , but little is known about them. The chemical composition of these volatiles was investigated using GC-MS analysis and Y-tube olfactometer methods. Twenty-five compounds accounting for 55.3% of the volatiles were identified, with the highest proportion of 1-(4-ethylphenyl)ethanone (11.8%), followed by 1-(4-hydroxy-3-methylphenyl)ethanone (11.2%) and -cymen-7-ol (7.1%). These findings provide a theoretical basis for the preparation of attractants and could eventually lead to increased bellied gallnut yield.
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http://dx.doi.org/10.3390/molecules25153412DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7435823PMC
July 2020

The strange mitochondrial genomes of Metschnikowia yeasts.

Curr Biol 2020 Jul;30(14):R800-R801

Department of Biology, University of Western Ontario, London, ON N6A 1W8, Canada. Electronic address:

While sequencing and characterizing the mitochondrial genomes of 71 strains from the yeast genus Metschnikowia [1] (close cousin to the model species Candida albicans), we uncovered one of the most extreme examples of mitochondrial genome architectural diversity observed to date. These Metschnikowia mitochondrial DNAs (mtDNAs) capture nearly the entire known gene-size and intron-content range for cox1 and cob across all eukaryotic life and show remarkable differences in structure and noncoding content. This genomic variation can be seen both among species and between strains of the same species, raising the question: why are Metschnikowia mitogenomes so malleable?
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http://dx.doi.org/10.1016/j.cub.2020.05.075DOI Listing
July 2020

Intra-specific comparison of mitochondrial genomes reveals host gene fragment exchange via intron mobility in Tremella fuciformis.

BMC Genomics 2020 Jun 24;21(1):426. Epub 2020 Jun 24.

Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.

Background: Mitochondrial genomic sequences are known to be variable. Comparative analyses of mitochondrial genomes can reveal the nature and extent of their variation.

Results: Draft mitochondrial genomes of 16 Tremella fuciformis isolates (TF01-TF16) were assembled from Illumina and PacBio sequencing data. Mitochondrial DNA contigs were extracted and assembled into complete circular molecules, ranging from 35,104 bp to 49,044 bp in size. All mtDNAs contained the same set of 41 conserved genes with identical gene order. Comparative analyses revealed that introns and intergenic regions were variable, whereas genic regions (including coding sequences, tRNA, and rRNA genes) were conserved. Among 24 introns detected, 11 were in protein-coding genes, 3 in tRNA genes, and the other 10 in rRNA genes. In addition, two mobile fragments were found in intergenic regions. Interestingly, six introns containing N-terminal duplication of the host genes were found in five conserved protein-coding gene sequences. Comparison of genes with and without these introns gave rise to the following proposed model: gene fragment exchange with other species can occur via gain or loss of introns with N-terminal duplication of the host genes.

Conclusions: Our findings suggest a novel mechanism of fungal mitochondrial gene evolution: partial foreign gene replacement though intron mobility.
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http://dx.doi.org/10.1186/s12864-020-06846-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7315562PMC
June 2020

Lasiodiplodia theobromae-induced alteration in ROS metabolism and its relation to gummosis development in Prunus persica.

Plant Physiol Biochem 2020 Sep 22;154:43-53. Epub 2020 May 22.

Key Laboratory of Horticultural Plant Biology-Ministry of Education, College of Horticulture and Forest Sciences, Huazhong Agricultural University, Wuhan, 430070, Hubei Province, China. Electronic address:

Peach gummosis caused by Lasiodiplodia theobromae is one of the most detrimental diseases to peaches in southern China. Reactive oxygen species (ROS) play major roles in plant-pathogen interactions, however, their roles in the pathogenesis of peach gummosis, especially shoot disease in perennials, are largely unknown. In this study, the effects of L. theobromae on ROS production-scavenging systems and on signalling transduction during L. theobromae-induced gummosis in current-year peach shoots were investigated. The infection by L. theobromae led to a ROS burst and activated the plant antioxidant enzyme-dependent scavenging system. With disease progression, the capacity of the plant antioxidant machinery declined, and allowed for ROS accumulation and eventual malondialdehyde production. As for the fungus L. theobromae, the transcripts of genes related to ROS production were significantly repressed, and concomitantly the expression of genes related to antioxidant systems and oxidative stress resistance was markedly upregulated, perhaps to alleviate oxidative stress for successful colonisation. Moreover, genes involved in phytohormones biosynthesis and pathogenesis-related proteins were all markedly promoted, which could contribute to the restriction of disease development in peach shoots. Overall, the results showed that the ROS production-scavenging system in P. persica might affect disease development during peach-L. theobromae interaction. Our findings lay the foundations for future in-depth investigations of the molecular mechanisms and regulatory networks underlying L. theobromae-mediated shoot diseases in terms of ROS production-scavenging systems.
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http://dx.doi.org/10.1016/j.plaphy.2020.05.018DOI Listing
September 2020

Effects of Cultured Root and Soil Microbial Communities on the Disease of Caused by .

Front Microbiol 2020 15;11:929. Epub 2020 May 15.

College of Plant Protection, Hunan Agricultural University, Changsha, China.

Background: Black shank, caused by the oomycete pathogen , is responsible for huge economic losses worldwide. Research has focused on biocontrol to prevent disease and to minimize the use of synthetic fungicides.

Methods: We explored and compared the efficacy of suppressive microflora cultured from soil and roots on the growth of for controlling the incidence of black shank.

Results: We found that 31 microfloral communities, enriched from 40 root samples but only 18 microfloral communities from soil samples, were antagonistic to In the field experiment, the root functional microflora (RFM) showed a greater suppressiveness of black shank than the soil functional microflora (SFM), while both RFM and SFM altered diversity, composition, structure, and interaction of soil bacterial communities during plant growth. Although the inoculation of RFM onto roots significantly ( < 0.05) decreased microbial diversity, molecular ecological network analysis indicated more possible interactions among soil microbes, while an opposite trend was observed with SFM inoculation. Linear regression analysis revealed that diversity indices were negatively correlated with suppression on the black shank, suggesting that specific taxa (e.g., OTU_322 and OTU_6478) could colonize and be active during plant growth at the expense of microbial diversity. In addition, 18 functional strains, isolated and screened from 3 RMF (12 strains) and 3 SMF (6 strains), were identified as bacterial genera (12), (1), (1), (2), and (2). Spearman's ranked correlation tests revealed that relative abundances of some OTUs affiliated with genera , , and were significantly ( < 0.05) and positively correlated with the level of disease suppression.

Conclusion: Microfloral communities or key functional species isolated from plant roots might be more effective in controlling black shank than those from soil, and they may be developed for disease control.
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http://dx.doi.org/10.3389/fmicb.2020.00929DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243367PMC
May 2020

Regulates Infection-Related Morphogenesis and Pathogenicity of the Crucifer Anthracnose Fungus .

Front Microbiol 2020 8;11:763. Epub 2020 May 8.

The Key Lab of Plant Pathology of Hubei Province, Huazhong Agricultural University, Wuhan, China.

The fungal pathogen, , causes a disease called anthracnose on various cruciferous plants. Here, we characterized a 25 ortholog in , named (CH063_04363). The deletion mutants were defective in mycelial growth, conidiation, conidial germination, appressorial formation, and invasive hyphal growth on leaves, resulting in loss of virulence. Furthermore, deletion of led to increased sensitivity to cell wall stress and resulted in resistance to osmotic stress. Exogenous cyclic adenosine monophosphate (cAMP) and IBMX treatments were able to induce appressorial formation in the mutants, but abnormal germ tubes were still formed. The results implied that is involved in pathogenicity by regulation of cAMP signaling pathways in . More importantly, we found that ChCDC25 may interact with Ras2 and affects Ras2 protein abundance in . Taken together, regulates infection-related morphogenesis and pathogenicity of This is the first report to reveal functions of a 25 ortholog in a hemibiotrophic phytopathogen.
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http://dx.doi.org/10.3389/fmicb.2020.00763DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7227425PMC
May 2020

A chromosome-scale assembly of the smallest Dothideomycete genome reveals a unique genome compaction mechanism in filamentous fungi.

BMC Genomics 2020 Apr 23;21(1):321. Epub 2020 Apr 23.

State Key Laboratory of Crop Stress Biology in Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, Shaanxi Province, China.

Background: The wide variation in the size of fungal genomes is well known, but the reasons for this size variation are less certain. Here, we present a chromosome-scale assembly of ectophytic Peltaster fructicola, a surface-dwelling extremophile, based on long-read DNA sequencing technology, to assess possible mechanisms associated with genome compaction.

Results: At 18.99 million bases (Mb), P. fructicola possesses one of the smallest known genomes sequence among filamentous fungi. The genome is highly compact relative to other fungi, with substantial reductions in repeat content, ribosomal DNA copies, tRNA gene quantity, and intron sizes, as well as intergenic lengths and the size of gene families. Transposons take up just 0.05% of the entire genome, and no full-length transposon was found. We concluded that reduced genome sizes in filamentous fungi such as P. fructicola, Taphrina deformans and Pneumocystis jirovecii occurred through reduction in ribosomal DNA copy number and reduced intron sizes. These dual mechanisms contrast with genome reduction in the yeast fungus Saccharomyces cerevisiae, whose small and compact genome is associated solely with intron loss.

Conclusions: Our results reveal a unique genomic compaction architecture of filamentous fungi inhabiting plant surfaces, and broaden the understanding of the mechanisms associated with compaction of fungal genomes.
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http://dx.doi.org/10.1186/s12864-020-6732-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7181583PMC
April 2020

Genome-based mining of new antimicrobial meroterpenoids from the phytopathogenic fungus Bipolaris sorokiniana strain 11134.

Appl Microbiol Biotechnol 2020 May 26;104(9):3835-3846. Epub 2020 Mar 26.

Griffith Institute for Drug Discovery, Griffith University, Brisbane, QLD, 4111, Australia.

Polyketide-terpenoid hybrid compounds are one of the largest families of meroterpenoids, with great potential for drug development for resistant pathogens. Genome sequence analysis of secondary metabolite gene clusters of a phytopathogenic fungus, Bipolaris sorokiniana 11134, revealed a type I polyketide gene cluster, consisting of highly reducing polyketide synthase, non-reducing polyketide synthase, and adjacent prenyltransferase. MS- and UV-guided isolations led to the isolation of ten meroterpenoids, including two new compounds: 19-dehydroxyl-3-epi-arthripenoid A (1) and 12-keto-cochlioquinone A (2). The structures of 1-10 were elucidated by the analysis of NMR and high-resolution electrospray ionization mass spectroscopy data. Compounds 5-8 and 10 showed moderate activity against common Staphylococcus aureus and methicillin-resistant S. aureus, with minimum inhibitory concentration (MIC) values of 12.5-100 μg/mL. Compound 5 also exhibited activity against four clinical resistant S. aureus strains and synergistic antifungal activity against Candida albicans with MIC values of 12.5-25 μg/mL. The biosynthetic gene cluster of the isolated compounds and their putative biosynthetic pathway are also proposed. KEY POINTS: • Ten meroterpenoids were identified from B. sorokiniana, including two new compounds. • Cochlioquinone B (5) showed activity against MRSA and synergistic activity against C. albicans. • The biosynthetic gene cluster and biosynthetic pathway of meroterpenoids are proposed. • Genome mining provided a new direction to uncover the diversity of meroterpenoids.
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http://dx.doi.org/10.1007/s00253-020-10522-1DOI Listing
May 2020

Catching speciation in the act-act 2: Metschnikowia lacustris sp. nov., a sister species to Metschnikowia dekortorum.

Antonie Van Leeuwenhoek 2020 Jun 25;113(6):753-762. Epub 2020 Feb 25.

Department of Biology, University of Western Ontario, London, ON, N6A 5B7, Canada.

The isolation of a single yeast strain in the clade containing Metschnikowia dekortorum, in the Amazon biome of Brazil, incited us to re-examine the species boundaries within the clade. The strain (UFMG-CM-Y6306) was difficult to position relative to neighbouring species using standard barcode sequences (ITS-D1/D2 rRNA gene region). Mating took place freely with α strains of M. bowlesiae, M. dekortorum, and M. similis, but two-spored asci, indicative of a fertile meiotic progeny, were formed abundantly only with certain strains of M. dekortorum. Accordingly, we examined mating success among every phylotype in the clade and constructed a phylogeny based on a concatenation of 100 of the largest orthologous genes annotated in draft genomes. The analyses confirmed membership of the Amazonian isolate in M. dekortorum, but also indicated that the species should be subdivided into two. As a result, we retain three original members of M. dekortorum in the species, together with the new isolate, and reassign six isolates recovered from Mesoamerican lacustrine habitats to Metschnikowia lacustris sp. nov. The type is UWOPS 12-619.2 (isotype CBS 16250). MycoBank: MB 833751.
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http://dx.doi.org/10.1007/s10482-020-01395-5DOI Listing
June 2020

Identification and Characterization of Pestalotioid Fungi Causing Leaf Spots on Mango in Southern China.

Plant Dis 2020 Apr 15;104(4):1207-1213. Epub 2020 Feb 15.

Plant Breeding Institute, The University of Sydney, Cobbitty, NSW 2570, Australia.

Mango is an economically important fruit crop in southern China. However, leaf spots restrict the development of mango trees, reducing the yield and production. Pestalotioid fungi are one of the major agents causing leaf spots on mango. During 2016 and 2017, 21 isolates of pestalotioid fungi associated with leaf spots on mango leaves were collected from five provinces in southern China: Guangxi, Hainan, Yunnan, Guangdong, and Fujian. All 21 isolates were subjected to morphological characterization and DNA sequence analysis. The morphological data were combined with analyses of concatenated sequences of the ITS (internal transcribed spacer), TEF 1-α (translation elongation factor), and TUB2 (β-tubulin) for higher resolution of the species identity of these isolates. The results showed that these isolates belong to , , , , , , , and Pathogenicity test results showed that all these species could cause symptoms. On detached mango leaves (cv. Tainong), early foliar symptoms on leaves were small yellow-to-brown lesions. Later, these spots expanded with uneven borders, turned white to gray, and coalesced to form larger gray patches. To our knowledge, this is the first description of , , , , , , or as causal agents for leaf spots on mango worldwide.
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http://dx.doi.org/10.1094/PDIS-03-19-0438-REDOI Listing
April 2020

Two New Biocontrol Agents Against Clubroot Caused by .

Front Microbiol 2019 21;10:3099. Epub 2020 Jan 21.

The Key Lab of Plant Pathology of Hubei Province, Huazhong Agricultural University, Wuhan, China.

Clubroot disease caused by can lead to serious yield losses in crucifers such as . In this study, 323 bacterial strains were isolated from the rhizosphere of severely diseased in Dangyang county, Hubei province, China. Antagonistic strains were first identified based on dual culture inhibition zones with and . These were then further screened in germination inhibition and viability assays of resting spores of . Finally, eight of the antagonistic strains were found to significantly reduce the disease severity of clubroot by more than 40% under greenhouse conditions, and two strains, F85 and T113, were found to have efficacy of more than 80%. Root hair infection experiments showed that F85 and T113 can inhibit early infection of root hairs, reduce the differentiation of primary plasmodia of , and inhibit formation of secondary zoosporangia. Based on sequence analysis of 16S rDNA gene, gene and 22 housekeeping genes as well as carbon source utilization analysis, the F85 was identified as and T113 as . Genome analysis, PCR and RT-PCR detection revealed that both F85 and T113 harbor various antibiotic biosynthesis gene clusters required to form peptides with antimicrobial activity. To our knowledge, this is the first report of as a biocontrol agent against clubroot disease.
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http://dx.doi.org/10.3389/fmicb.2019.03099DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986203PMC
January 2020

The yeast community of Conotelus sp. (Coleoptera: Nitidulidae) in Brazilian passionfruit flowers (Passiflora edulis) and description of Metschnikowia amazonensis sp. nov., a large-spored clade yeast.

Yeast 2020 03 3;37(3):253-260. Epub 2020 Feb 3.

Department of Biology, University of Western Ontario, London, Ontario, Canada.

Species of the nitidulid beetle Conotelus found in flowers of Convolvulaceae and other plants across the New World and in Hawaii consistently harbour a yeast community dominated by one or more large-spored Metschnikowia species. We investigated the yeasts found in beetles and flowers of cultivated passionfruit in Rondônia state, in the Amazon biome of Brazil, where a Conotelus species damages the flowers and hinders fruit production. A sample of 46 beetles and 49 flowers yielded 86 and 83 yeast isolates, respectively. Whereas the flower community was dominated by Kodamaea ohmeri and Kurtzmaniella quercitrusa, the major yeasts recovered from beetles were Wickerhamiella occidentalis, which is commonly isolated from this community, and a novel species of large-spored Metschnikowia in the arizonensis subclade, which we describe here as Metschnikowia amazonensis sp. nov. Phylogenetic analyses based on barcode sequences (ITS-D1/D2) and a multigene alignment of 11,917 positions (genes ura2, msh6, and pmt2) agreed to place the new species as a sister to Metschnikowia arizonensis, a rare species known only from one locality in Arizona. The two form sterile asci when mated, which is typical of related members of the clade. The α pheromone of the new species is unique but typical of the subclade. The type of M. amazonensis sp. nov. is UFMG-CM-Y6309 (ex-type CBS 16156 , mating type a), and the designated allotype (mating type α) is UFMG-CM-Y6307 (CBS 16155 ). MycoBank MB 833560.
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http://dx.doi.org/10.1002/yea.3453DOI Listing
March 2020

A new abyssomicin polyketide with anti-influenza A virus activity from a marine-derived Verrucosispora sp. MS100137.

Appl Microbiol Biotechnol 2020 Feb 2;104(4):1533-1543. Epub 2020 Jan 2.

State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai, 200237, China.

Marine microorganisms live in dramatically different environments and have attracted much attention for their structurally unique natural products with potential strong biological activity. Based on the one strain-many compounds (OSMAC) strategy and liquid chromatography mass spectrometry (LC-MS) methods, our continuing efforts on the investigation of novel active compounds from marine Verrucosispora sp. MS100137 has led to the identification of a new polycyclic metabolite, abyssomicin Y (1), together with six known abyssomicin and proximicin analogs (2-7). Abyssomicin Y is a type I abyssomicin with an epoxide group at C-8 and C-9. Compounds 1-3 showed potent inhibitory effects against the influenza A virus; their observed inhibition rates were 97.9%, 98.3%, and 95.9%, respectively, at a concentration of 10 μM, and they displayed lower cytotoxicity than 4. The structures were determined by different NMR techniques and HRMS experiments. This investigation revealed that OSMAC could serve as a useful method for enabling the activation of the silent genes in the microorganism and for the formation of previously unreported active secondary metabolites.
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http://dx.doi.org/10.1007/s00253-019-10217-2DOI Listing
February 2020

In vitro antifungal activity of dimethyl trisulfide against Colletotrichum gloeosporioides from mango.

World J Microbiol Biotechnol 2019 Dec 12;36(1). Epub 2019 Dec 12.

School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada.

Colletotrichum gloeosporioides, one of the main agents of mango anthracnose, causes latent infections in unripe mango, and leads to huge economic losses during storage and transport. Dimethyl trisulfide (DMTS), one of the main volatile compounds produced by some microorganisms or plants, has shown antifungal activity against some phytopathogens in previous studies, but its effects on C. gloeosporioides and mechanisms of action have not been well characterized. In fumigation trials of conidia and mycelia of C. gloeosporioides for 2, 4, 6, 8, or 10 h, at a concentration of 100 μL/L of air space in vitro, DMTS caused serious damage to the integrity of plasma membranes, which significantly reduced the survival rate of spores, and resulted in abnormal hyphal morphology. Moreover, DMTS caused deterioration of subcellular structures of conidia and mycelia, such as cell walls, plasma membranes, Golgi bodies, and mitochondria, and contributed to leakage of protoplasm, thus promoting vacuole formation. In addition, to better understand the molecular mechanisms of the antifungal activity, the global gene expression profiles of isolate C. gloeosporioides TD3 treated in vitro with DMTS at a concentration of 100 μL/L of air for 0 h (Control), 1 h, or 3 h were investigated by RNA sequencing (RNA-seq), and over 62 Gb clean reads were generated from nine samples. Similar expressional patterns for nine differentially expressed genes (DEGs) in both RNA-seq and qRT-PCR assays showed the reliability of the RNA-seq data. In comparison to the non-treated control groups, we found DMTS suppressed expression of β-1, 3-D-glucan, chitin, sterol biosynthesis-related genes, and membrane protein-related genes. These genes related to the formation of fungal cell walls and plasma membranes might be associated with the toxicity of DMTS against C. gloeosporioides. This is the first study demonstrating antifungal activity of DMTS against C. gloeosporioides on mango by direct damage of conidia and hyphae, thus providing a novel tool for postharvest control of mango anthracnose.
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http://dx.doi.org/10.1007/s11274-019-2781-zDOI Listing
December 2019

Colletotrichum species associated with mango in southern China.

Sci Rep 2019 12 11;9(1):18891. Epub 2019 Dec 11.

Environmental Sciences, University of Guelph, Guelph, Ontario, Canada.

Mango (Mangifera indica L.) is an economically significant fruit crop in provinces of southern China including Hainan, Yunnan, Sichuan, Guizhou, Guangdong and Fujian. The objective of this study was to examine the diversity of Colletotrichum species infecting mango cultivars in major growing areas in China, using morphological and molecular techniques together with pathogenicity tests on detached leaves and fruits. Over 200 Colletotrichum isolates were obtained across all mango orchards investigated, and 128 of them were selected for sequencing and analyses of actin (ACT), chitin synthase (CHS-1), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), the internal transcribed spacer (ITS) region, β-tubulin (TUB2) genomic regions. Our results showed that the most common fungal isolates associated with mango in southern China involved 13 species: Colletotrichum asianum, C. cliviicola, C. cordylinicola, C. endophytica, C. fructicola, C. gigasporum, C. gloeosporioides, C. karstii, C. liaoningense, C. musae, C. scovillei, C. siamense and C. tropicale. The dominant species were C. asianum and C. siamense each accounting for 30%, and C. fructicola for 25%. Only C. asianum, C. fructicola, C. scovillei and C. siamense have previously been reported on mango, while the other nine Colletotrichum species listed above were first reports associated with mango in China. From this study, five Colletotrichum species, namely C. cordylinicola, C. endophytica, C. gigasporum, C. liaoningense and C. musae were the first report on mango worldwide. Pathogenicity tests revealed that all 13 species caused symptoms on artificially wounded mango fruit and leaves (cv. Tainong). There was no obvious relationship between aggressiveness and the geographic origin of the isolates. These findings will help in mango disease management and future disease resistance breeding.
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http://dx.doi.org/10.1038/s41598-019-54809-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6906457PMC
December 2019