Mycoparasitism illuminated by genome and transcriptome sequencing of , an important biocontrol fungus of the plant pathogen Open Access

Abstract

is a mycoparasite of the notorious plant pathogen . To further understand the parasitism of , we assembled and analysed its genome and performed transcriptome analyses. The genome of strain ZS-1 was assembled into 350 scaffolds and had a size of 39.8 Mb. A total of 11 437 predicted genes and proteins were annotated, and 30.8 % of the hits matched proteins encoded by another member of the Pleosporales, , a worldwide soilborne fungus with biocontrol ability. The transcriptome of strain ZS-1 during the early interaction with at 0, 4 and 12 h was analysed. The detected expressed genes were involved in responses to host defenses, including cell-wall-degrading enzymes, transporters, secretory proteins and secondary metabolite productions. Seventeen differentially expressed genes (DEGs) of fungal cell-wall-degrading enzymes (FCWDs) were up-regulated during parasitism, with only one down-regulated. Most of the monocarboxylate transporter genes of the major facilitator superfamily and all the detected ABC transporters, especially the heavy metal transporters, were significantly up-regulated. Approximately 8 % of the 11 437 proteins in were predicted to be secretory proteins with catalytic activity. In the molecular function category, hydrolase activity, peptidase activity and serine hydrolase activity were enriched. Most genes involved in serine hydrolase activity were significantly up-regulated. This genomic analysis and genome-wide expression study demonstrates that the mycoparasitism process of is complex and a broad range of proteins are deployed by to successfully invade its host. Our study provides insights into the mechanisms of the mycoparasitism between and and identifies potential secondary metabolites from for application as a biocontrol agent.

Funding
This study was supported by the:
  • the earmarked fund for China Agriculture Research System (Award CARS-13)
    • Principle Award Recipient: Daohong Jiang
  • National Natural Science Foundation of China (Award 31572048)
  • the National Key R&D Program of China (Award 2017YFD0200400)
    • Principle Award Recipient: Yanping Fu
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2020-03-06
2024-03-28
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References

  1. Sandys-Winsch C, Whipps JM, Gerlagh M, Kruse M. World distribution of the sclerotial mycoparasite Coniothyrium minitans . Mycol Res 1993; 97:1175–1178 [View Article]
    [Google Scholar]
  2. Li G, Wang D, Zhang S, Dan H. Characterization of the sclerotial parasite Coniothyrium minitans I: biological characteristics and the natural distribution in Hubei Province. J Huazhong Agr Univ 1995; 14:125–130
    [Google Scholar]
  3. Verkley GJM, da Silva M, Wicklow DT, Crous PW. Paraconiothyrium, a new genus to accommodate the mycoparasite Coniothyrium minitans, anamorphs of Paraphaeosphaeria, and four new species. Stud Mycol 2004; 50:323–335
    [Google Scholar]
  4. Campbell WA. A new species of Coniothyrium parasitic on sclerotia. Mycologia 1947; 39:190–195 [View Article]
    [Google Scholar]
  5. Whipps JM, Gerlagh M. Biology of Coniothyrium minitans and its potential for use in disease biocontrol. Mycol Res 1992; 96:897–907 [View Article]
    [Google Scholar]
  6. Yang R, Han YC, Li GQ, Jiang DH, Huang HC. Suppression of Sclerotinia sclerotiorum by antifungal substances produced by the mycoparasite Coniothyrium minitans . Eur J Plant Pathol 2007; 119:411–420 [View Article]
    [Google Scholar]
  7. JC Tu. Mycoparasitism by Coniothyrium minitans on Sclerotinia sclerotiorum and its effect on sclerotial germination. J Phytopathol 1984; 109:261–268 [View Article]
    [Google Scholar]
  8. Huang HC, Hoes JA. Penetration and infection of Sclerotinia sclerotiorum by Coniothyrium minitans . Can J Bot 1976; 54:406–410 [View Article]
    [Google Scholar]
  9. Turner GJ, Tribe HT. On Coniothyrium minitans and its parasitism of sclerotinia species. Transactions Brit Mycol Soc 1976; 66:97–105 [View Article]
    [Google Scholar]
  10. McQuilken MP, Gemmell J, Whipps JM. Some nutritional factors affecting production of biomass and antifungal metabolites of Coniothyrium minitans . Biocontrol Sci Techn 2002; 12:443–454 [View Article]
    [Google Scholar]
  11. Budge SP, Whipps JM. Potential for integrated control of Sclerotinia sclerotiorum in glasshouse Lettuce using Coniothyrium minitans and reduced fungicide application. Phytopathology 2001; 91:221–227 [View Article]
    [Google Scholar]
  12. Elsheshtawi M, Elkhaky MT, Sayed SR, Bahkali AH, Mohammed AA et al. Integrated control of white rot disease on beans caused by Sclerotinia sclerotiorum using Contans and reduced fungicides application. Saudi J Biol Sci 2017; 24:405–409 [View Article]
    [Google Scholar]
  13. Gerlagh M, Goossen-van de Geijn HM, Fokkema NJ, Vereijken PFG. Long-Term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum infected crops. Phytopathology 1999; 89:141–147 [View Article]
    [Google Scholar]
  14. Kamal MM, Savocchia S, Lindbeck KD, Ash GJ. Biology and biocontrol of Sclerotinia sclerotiorum (Lib.) de Bary in oilseed Brassicas. Australasian Plant Pathol 2016; 45:1–14 [View Article]
    [Google Scholar]
  15. Benigni M, Bompeix G. Chemical and biological control of Sclerotinia sclerotiorum in witloof chicory culture. Pest Manag Sci 2010; 66:1332–1336 [View Article]
    [Google Scholar]
  16. Chitrampalam P, Figuli PJ, Matheron ME, Subbarao KV, Pryor BM. Biocontrol of lettuce drop caused by Sclerotinia sclerotiorum and S. minor in desert agroecosystems. Plant Disease 2008; 92:1625–1634 [View Article]
    [Google Scholar]
  17. Partridge DE, Sutton TB, Jordan DL, Curtis VL, Bailey JE. Management of sclerotinia blight of peanut with the biological control agent Coniothyrium minitans . Plant Disease 2006; 90:957–963 [View Article]
    [Google Scholar]
  18. GQ L, Huang HC, Acharya SN, Erickson RS. Effectiveness of Coniothyrium minitans and Trichoderma atroviride in suppression of sclerotinia blossom blight of alfalfa. Plant Pathol 2005; 54:204–211
    [Google Scholar]
  19. McLaren DL, Huang HC, Kozub GC, Rimmer SR. Biological control of sclerotinia wilt of sunflower with Talaromyces flavus and Coniothyrium minitans . Plant Dis. 1994; 78:231–235 [View Article]
    [Google Scholar]
  20. Jones D, Johnson RPC. Ultrastructure of frozen, fractured and etched pycnidiospores of Coniothyrium minitans . Transactions Brit Mycol Soc 1970; 55:83–IN9 [View Article]
    [Google Scholar]
  21. Huang HC, Kokko EG. Ultrastructure of hyperparasitism of Coniothyrium minitans on sclerotia of Sclerotinia sclerotiorum . Can. J. Bot. 1987; 65:2483–2489 [View Article]
    [Google Scholar]
  22. Huang HC, Kokko EG. Penetration of hyphae of Sclerotinia sclerotiorum by Coniothyrium minitans without the formation of Appressoria. J Phytopathol 1988; 123:133–139 [View Article]
    [Google Scholar]
  23. Jones D, Gordon AH, Bacon JSD. Co-operative action by endo- and exo-β-(1→3)-glucanases from parasitic fungi in the degradation of cell-wall glucans of Sclerotinia sclerotiorum (Lib.) de Bary. Biochem J 1974; 140:47–55 [View Article]
    [Google Scholar]
  24. Phillips AJL, Price K. Structural aspects of the parasitism of sclerotia of Sclerotinia sclerotiorum (Lib) de Bary by Coniothyrium minitans Campb. J Phytopathol 1983; 107:193–203 [View Article]
    [Google Scholar]
  25. Hu Y, Li G, Yang L. Characterization of factors affecting enzymatic activity of chitinase produced by mycoparasite Coniothyrium minitans . Chin J Appl Environ Biol 2009; 2010:226–229
    [Google Scholar]
  26. Giczey G, Kerenyi Z, Fulop L, Hornok L. Expression of cmg1, an Exo- -1,3-glucanase gene from Coniothyrium minitans, increases during sclerotial parasitism. Appl Environ Microbiol 2001; 67:865–871 [View Article]
    [Google Scholar]
  27. Ren L, Li G, Han YC, Jiang DH, Huang H-C. Degradation of oxalic acid by Coniothyrium minitans and its effects on production and activity of β-1,3-glucanase of this mycoparasite. Biol Control 2007; 43:1–11 [View Article]
    [Google Scholar]
  28. Zeng F, Gong X, Hamid MI, Fu Y, Jiatao X et al. A fungal cell wall integrity-associated MAP kinase cascade in Coniothyrium minitans is required for conidiation and mycoparasitism. Fungal Genet Biol 2012; 49:347–357 [View Article]
    [Google Scholar]
  29. Wei W, Zhu W, Cheng J, Xie J, Jiang D et al. Nox complex signal and MAPK cascade pathway are cross-linked and essential for pathogenicity and conidiation of mycoparasite Coniothyrium minitans . Sci Rep 2016; 6:24325 [View Article]
    [Google Scholar]
  30. Zeng L-M, Zhang J, Han Y-C, Yang L, Wu M-de et al. Degradation of oxalic acid by the mycoparasite Coniothyrium minitans plays an important role in interacting with Sclerotinia sclerotiorum . Environ Microbiol 2014; 16:2591–2610 [View Article]
    [Google Scholar]
  31. Luo C, Zhao H, Yang X, Qiang C, Cheng J et al. Functional analysis of the melanin-associated gene CmMR1 in Coniothyrium minitans . Front Microbiol 2018; 9:2658 [View Article]
    [Google Scholar]
  32. Lou Y, Han Y, Yang L, Wu M, Zhang J et al. CmpacC regulates mycoparasitism, oxalate degradation and antifungal activity in the mycoparasitic fungus C oniothyrium minitans . Environ Microbiol 2015; 17:4711–4729 [View Article]
    [Google Scholar]
  33. Han Y-C, Li G-Q, Yang L, Jiang D-H. Molecular cloning, characterization and expression analysis of a pacC homolog in the mycoparasite Coniothyrium minitans . World J Microb Biot 2011; 27:381–391 [View Article]
    [Google Scholar]
  34. Wei W, Zhu W, Cheng J, Xie J, Li B et al. CmPEX6, a gene involved in peroxisome biogenesis, Is essential for parasitism and conidiation by the sclerotial parasite Coniothyrium minitans . Appl Environ Microbiol 2013; 79:3658–3666 [View Article]
    [Google Scholar]
  35. Hamid MI, Zeng F, Cheng J, Jiang D, Fu Y. Disruption of heat shock factor 1 reduces the formation of conidia and thermotolerance in the mycoparasitic fungus Coniothyrium minitans . Fungal Genet Biol 2013; 53:42–49 [View Article]
    [Google Scholar]
  36. He Z, Hu X, Fu Y, Jiang D. Metabolic profile of Coniothyrium minitans co-cultured with Sclerotinia sclerotiorum . J Huazhong Agr Univ 2017; 36:35–41
    [Google Scholar]
  37. McQuilken MP, Gemmell J, Hill RA, Whipps JM. Production of macrosphelide A by the mycoparasite Coniothyrium minitans . FEMS Microbiol Lett 2003; 219:27–31 [View Article]
    [Google Scholar]
  38. Jiang D, Li G, Yi X, Fu Y, Wang D. Studies on the properties of antibacterial substance produced by Coniothyrium minitans . Acta Phytopathol Sin 1998; 28:29–32
    [Google Scholar]
  39. Wang H, Hu X, Jiang D. Separation of the metabolic product of Coniothyrium minitans against Xanthomonas oryzae pv. oryzae. J Huazhong Agr Univ 2009; 28:148–150
    [Google Scholar]
  40. Yang L, Miao HJ, Li GQ, Yin LM, Huang H-C. Survival of the mycoparasite Coniothyrium minitans on flower petals of oilseed rape under field conditions in central China. Biological Control 2007; 40:179–186 [View Article]
    [Google Scholar]
  41. Luo R, Liu B, Xie Y, Li Z, Huang W et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012; 1: [View Article]
    [Google Scholar]
  42. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article]
    [Google Scholar]
  43. Boetzer M, Pirovano W. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics 2014; 15:211 [View Article]
    [Google Scholar]
  44. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015; 12:357–360 [View Article]
    [Google Scholar]
  45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
    [Google Scholar]
  46. Trapnell C, Roberts A, Goff L, Pertea G, Kim D et al. Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7:562–578 [View Article]
    [Google Scholar]
  47. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 2013; 8:1494–1512 [View Article]
    [Google Scholar]
  48. Haas BJ, Zeng Q, Pearson MD, Cuomo CA, Wortman JR. Approaches to fungal genome annotation. Mycology 2011; 2:118–141 [View Article]
    [Google Scholar]
  49. Besemer J, Borodovsky M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 2005; 33:W451–W454 [View Article]
    [Google Scholar]
  50. Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M. BRAKER1: unsupervised RNA-Seq-Based genome annotation with GeneMark-ET and AUGUSTUS: table 1. Bioinformatics 2016; 32:767–769 [View Article]
    [Google Scholar]
  51. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013; 14:R36 [View Article]
    [Google Scholar]
  52. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol 2008; 9:R7 [View Article]
    [Google Scholar]
  53. Lee E, Helt GA, Reese JT, Munoz-Torres MC, Childers CP et al. Web Apollo: a web-based genomic annotation editing platform. Genome Biol 2013; 14:R93 [View Article]
    [Google Scholar]
  54. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005; 21:3674–3676 [View Article]
    [Google Scholar]
  55. The UniProt Consortium UniProt: the universal protein knowledgebase. Nucleic Acids Res 2017; 45:D158–D169 [View Article]
    [Google Scholar]
  56. Galperin MY, Makarova KS, Wolf YI, Koonin EV. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 2015; 43:D261–D269 [View Article]
    [Google Scholar]
  57. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 2017; 45:D200–D203 [View Article]
    [Google Scholar]
  58. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 2016; 44:D279–D285 [View Article]
    [Google Scholar]
  59. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007; 35:W182–W185 [View Article]
    [Google Scholar]
  60. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 2008; 5:621628 [View Article]
    [Google Scholar]
  61. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res 1997; 7:986–995 [View Article]
    [Google Scholar]
  62. Fischer S, Brunk BP, Chen F, Gao X, Harb OS et al. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr Protoc Bioinformatics 2011; Chapter 6:6.12.11–6.12.16 [View Article]
    [Google Scholar]
  63. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article]
    [Google Scholar]
  64. Lyu X, Shen C, Fu Y, Xie J, Jiang D et al. Comparative genomic and transcriptional analyses of the carbohydrate-active enzymes and secretomes of phytopathogenic fungi reveal their significant roles during infection and development. Sci Rep 2015; 5:15565 [View Article]
    [Google Scholar]
  65. Zhao Z, Liu H, Wang C, Xu J-R. Correction: comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2014; 15:6 [View Article]
    [Google Scholar]
  66. Saier MH, Reddy VS, Tsu BV, Ahmed MS, Li C et al. The transporter classification database (tcdB): recent advances. Nucleic Acids Res 2016; 44:D372–D379 [View Article]
    [Google Scholar]
  67. Saier MH, Tran CV, Barabote RD. Tcdb: the transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res 2006; 34:D181–D186 [View Article]
    [Google Scholar]
  68. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using diamond. Nat Methods 2015; 12:59–60 [View Article]
    [Google Scholar]
  69. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580 [View Article]
    [Google Scholar]
  70. Blin K, Medema MH, Kottmann R, Lee SY, Weber T. The antiSMASH database, a comprehensive database of microbial secondary metabolite biosynthetic gene clusters. Nucleic Acids Res 2017; 45:D555–D559 [View Article]
    [Google Scholar]
  71. Nielsen H. Predicting secretory proteins with SignalP. In Kihara D. editor Methods in Molecular Biology 1611 New York, NY: Humana Press; 2017 pp 59–73 [View Article]
    [Google Scholar]
  72. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011; 8:785786 [View Article]
    [Google Scholar]
  73. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2007; 2:953–971 [View Article]
    [Google Scholar]
  74. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000; 300:1005–1016 [View Article]
    [Google Scholar]
  75. Horton P, Park K-J, Obayashi T, Fujita N, Harada H et al. Wolf PSORT: protein localization predictor. Nucleic Acids Res 2007; 35:W585–W587 [View Article]
    [Google Scholar]
  76. Yu Y, Jiang D, Xie J, Cheng J, Li G et al. Ss-Sl2, a novel cell wall protein with PAN modules, is essential for sclerotial development and cellular integrity of Sclerotinia sclerotiorum . PLoS One 2012; 7:e34962 [View Article]
    [Google Scholar]
  77. Zeiner CA, Purvine SO, Zink EM, Paša-Tolić L, Chaput DL et al. Comparative analysis of secretome profiles of Manganese(II)-oxidizing ascomycete fungi. PLoS One 2016; 11:e0157844 [View Article]
    [Google Scholar]
  78. Turhan G. Further hyperparasites of Rhizoctonia solarni Kühn as promising candidates for biological control. J Plant Dis Protect 1990; 97:208–215
    [Google Scholar]
  79. Knapp DG, Németh JB, Barry K, Hainaut M, Henrissat B et al. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Sci Rep 2018; 8:6321 [View Article]
    [Google Scholar]
  80. Lopez D, Ribeiro S, Label P, Fumanal B, Venisse J-S et al. Genome-wide analysis of Corynespora cassiicola leaf fall disease putative effectors. Front Microbiol 2018; 9:276 [View Article]
    [Google Scholar]
  81. Zhang H, Hyde KD, Mckenzie EHC, Bahkali AH, Zhou D. Sequence data reveals phylogenetic affinities of Acrocalymma aquatica sp. nov., Aquasubmersa mircensis gen. et sp. nov. and Clohesyomyces aquaticus (Freshwater Coelomycetes). Cryptogamie Mycol 2012; 33:333–346 [View Article]
    [Google Scholar]
  82. Perlin MH, Andrews J, Toh SS. Essential letters in the fungal alphabet: ABC and MFS transporters and their roles in survival and pathogenicity. Adv Genet 2014; 85:201–253 [View Article]
    [Google Scholar]
  83. Donzelli BGG, Harman GE. Interaction of ammonium, glucose, and chitin regulates the expression of cell wall-degrading enzymes in Trichoderma atroviride strain P1. Appl Environ Microbiol 2001; 67:5643–5647 [View Article]
    [Google Scholar]
  84. Gruber S, Seidl-Seiboth V. Self versus non-self: fungal cell wall degradation in Trichoderma . Microbiology 2012; 158:26–34 [View Article]
    [Google Scholar]
  85. NAR G, Latge J-P, Munro CA. The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr 2017; 5:FUNK-0035-2016
    [Google Scholar]
  86. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma . Genome Biol 2011; 12:R40 [View Article]
    [Google Scholar]
  87. Seidl V, Huemer B, Seiboth B, Kubicek CP. A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. Febs J 2005; 272:5923–5939 [View Article]
    [Google Scholar]
  88. Carsolio C, Benhamou N, Haran S, Cortés C, Gutiérrez A et al. Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl Environ Microbiol 1999; 65:929–935 [View Article]
    [Google Scholar]
  89. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 2008; 26:553–560 [View Article]
    [Google Scholar]
  90. Yang X, Cui H, Cheng J, Xie J, Jiang D et al. A HOPS protein, CmVps39, is required for vacuolar morphology, autophagy, growth, conidiogenesis and mycoparasitic functions of Coniothyrium minitans . Environ Microbiol 2016; 18:3785–3797 [View Article]
    [Google Scholar]
  91. Keller NP. Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol 2019; 17:167–180 [View Article]
    [Google Scholar]
  92. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ et al. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 2008; 72:80–86 [View Article]
    [Google Scholar]
  93. Mukherjee PK, Horwitz BA, Kenerley CM. Secondary metabolism in Trichoderma – a genomic perspective. Microbiology 2012; 158:35–45 [View Article]
    [Google Scholar]
  94. Tomprefa N, McQuilken MP, Hill RA, Whipps JM. Antimicrobial activity of Coniothyrium minitans and its macrolide antibiotic macrosphelide A. J Appl Microbiol 2009; 106:2048–2056 [View Article]
    [Google Scholar]
  95. Xiang Y. Cloning and Functional Analysis of Melanins Associated Gene CmPKS1 in Coniothyrium minitans Master Diss: Huazhong Agricultural University; 2011
    [Google Scholar]
  96. Scharf DH, Brakhage AA, Mukherjee PK. Gliotoxin - bane or boon?. Environ Microbiol 2016; 18:1096–1109 [View Article]
    [Google Scholar]
  97. Tsunawaki S, Yoshida LS, Nishida S, Kobayashi T, Shimoyama T. Fungal metabolite gliotoxin inhibits assembly of the human respiratory burst NADPH oxidase. Infect Immun 2004; 72:33733382 [View Article]
    [Google Scholar]
  98. Spikes S, Xu R, Nguyen CK, Chamilos G, Kontoyiannis DP et al. Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J Infect Dis 2008; 197:479–486 [View Article]
    [Google Scholar]
  99. Vargas WA, Mukherjee PK, Laughlin D, Wiest A, Moran-Diez ME et al. Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens . Microbiology 2014; 160:2319–2330 [View Article]
    [Google Scholar]
  100. Atanasova L, Crom SL, Gruber S, Coulpier F, Seidl-Seiboth V et al. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 2013; 14:121 [View Article]
    [Google Scholar]
  101. Woo SL, Scala F, Ruocco M, Lorito M. The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 2006; 96:181–185 [View Article]
    [Google Scholar]
  102. Ruocco M, Lanzuise S, Vinale F, Marra R, Turrà D et al. Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol Plant Microbe Interact 2009; 22:291–301 [View Article]
    [Google Scholar]
  103. Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G et al. Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea . Genome Biol Evol 2015; 7:465–480 [View Article]
    [Google Scholar]
  104. Dubey MK, Jensen DF, Karlsson M. An ATP-binding cassette pleiotropic drug transporter protein is required for xenobiotic tolerance and antagonism in the fungal biocontrol agent Clonostachys rosea . Mol Plant Microbe Interact 2014; 27:725–732 [View Article]
    [Google Scholar]
  105. Oide S, Krasnoff SB, Gibson DM, Turgeon BG. Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae . Eukaryot Cell 2007; 6:1339–1353 [View Article]
    [Google Scholar]
  106. Wallner A, Blatzer M, Schrettl M, Sarg B, Lindner H et al. Ferricrocin, a siderophore involved in intra- and transcellular iron distribution in Aspergillus fumigatus . Appl Environ Microbiol 2009; 75:4194–4196 [View Article]
    [Google Scholar]
  107. Mukherjee PK, Hurley JF, Taylor JT, Puckhaber L, Lehner S et al. Ferricrocin, the intracellular siderophore of Trichoderma virens, is involved in growth, conidiation, gliotoxin biosynthesis and induction of systemic resistance in maize. Biochem Biophys Res Commun 2018; 505:606–611 [View Article]
    [Google Scholar]
  108. Sun X, Zhao Y, Jia J, Xie J, Cheng J et al. Uninterrupted expression of CmSIT1 in a sclerotial parasite Coniothyrium minitans leads to reduced growth and enhanced antifungal ability. Front Microbiol 2017; 8:2208 [View Article]
    [Google Scholar]
  109. Pazzagli L, Seidl-Seiboth V, Barsottini M, Vargas WA, Scala A et al. Cerato-platanins: elicitors and effectors. Plant Sci 2014; 228:79–87 [View Article]
    [Google Scholar]
  110. Gomes EV, Costa MdoN, de Paula RG, de Azevedo RR, da Silva FL et al. The cerato-platanin protein Epl-1 from Trichoderma harzianum is involved in mycoparasitism, plant resistance induction and self cell wall protection. Sci Rep 2015; 5:17998 [View Article]
    [Google Scholar]
  111. Crutcher FK, Moran-Diez ME, Ding S, Liu J, Horwitz BA et al. A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens . Fungal Biol 2015; 119:476–486 [View Article]
    [Google Scholar]
  112. Guzmán-Guzmán P, Alemán-Duarte MI, Delaye L, Herrera-Estrella A, Olmedo-Monfil V. Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genet 2017; 18:16 [View Article]
    [Google Scholar]
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