Abstract
Fusarium graminearum is a prominent fungal pathogen that causes economically important losses by infesting a wide variety of cereal crops. F. graminearum produces both asexual and sexual spores which disseminate and inoculate hosts. Therefore, to better understand the disease cycle and to develop strategies to improve disease management, it is important to further clarify molecular mechanisms of F. graminearum conidiogenesis. In this study, we functionally characterized the FgMed1, a gene encoding an ortholog of a conserved MedA transcription factor known to be a key conidiogenesis regulator in Aspergillus nidulans. The gene deletion mutants ΔFgMed1 produced significantly less conidia, and these were generated from abnormal conidiophores devoid of phialides. Additionally, we observed defective sexual development along with reduced virulence and deoxynivalenol (DON) production in ΔFgMed1. The GFP-tagged FgMed1 protein localized to the nuclei of conidiophores and phialides during early conidiogenesis. Significantly, RNA-Seq analyses showed that a number of the conidiation- and toxin-related genes are differentially expressed in the ΔFgMed1 mutant in early conidiogenesis. These data strongly suggest that FgMed1 involved in regulation of genes associated with early conidiogenesis, DON production, and virulence in F. graminearum.
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References
Al Abdallah Q, Choe SI, Campoli P, Baptista S, Gravelat FN, Lee MJ, Sheppard DC (2012) A conserved C-terminal domain of the Aspergillus fumigatus developmental regulator MedA is required for nuclear localization, adhesion and virulence. PLoS One 7(11):e49959. https://doi.org/10.1371/journal.pone.0049959
Arnaise S, Zickler D, Poisier C, Debuchy R (2001) pah1: a homeobox gene involved in hyphal morphology and microconidiogenesis in the filamentous ascomycete Podospora anserina. Mol Microbiol 39(1):54–64
Arratia-Quijada J, Sanchez O, Scazzocchio C, Aguirre J (2012) FlbD, a Myb transcription factor of Aspergillus nidulans, is uniquely involved in both asexual and sexual differentiation. Eukaryot Cell 11(9):1132–1142. https://doi.org/10.1128/EC.00101-12
Bluhm BH, Zhao X, Flaherty JE, Xu JR, Dunkle LD (2007) RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol Plant-Microbe Interact 20(6):627–636. https://doi.org/10.1094/MPMI-20-6-0627
Cappellini RA, Peterson JL (1965) Macroconidium formation in submerged cultures by a non-sporulating strain of Gibberella zeae. Mycologia 57(6):962–966
Catlett NL, Yoder OC, Turgeon BG (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2(6):1151–1161
Chacko N, Gold S (2012) Deletion of the Ustilago maydis ortholog of the Aspergillus sporulation regulator medA affects mating and virulence through pheromone response. Fungal Genet Biol 49(6):426–432. https://doi.org/10.1016/j.fgb.2012.04.002
Chung DW, Greenwald C, Upadhyay S, Ding S, Wilkinson HH, Ebbole DJ, Shaw BD (2011) acon-3, the Neurospora crassa ortholog of the developmental modifier, medA, complements the conidiation defect of the Aspergillus nidulans mutant. Fungal Genet Biol 48(4):370–376. https://doi.org/10.1016/j.fgb.2010.12.008
Clutterbuck AJ (1969) A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63(2):317–327
Desjardins AE (2003) Gibberella from A (venaceae) to Z (eae). Annu Rev Phytopathol 41:177–198. https://doi.org/10.1146/annurev.phyto.41.011703.115501
Dutton JR, Johns S, Miller BL (1997) StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J 16(18):5710–5721. https://doi.org/10.1093/emboj/16.18.5710
Fan G, Zhang K, Huang H, Zhang H, Zhao A, Chen L, Chen R, Li G, Wang Z, Lu GD (2017) Multiprotein-bridging factor 1 regulates vegetative growth, osmotic stress, and virulence in Magnaporthe oryzae. Curr Genet 63(2):293–309. https://doi.org/10.1007/s00294-016-0636-9
Gaffoor I, Brown DW, Plattner R, Proctor RH, Qi W, Trail F (2005) Functional analysis of the polyketide synthase genes in the filamentous fungus Gibberella zeae (anamorph Fusarium graminearum). Eukaryot Cell 4(11):1926–1933. https://doi.org/10.1128/EC.4.11.1926-1933.2005
Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, Macdonald KD, al-Bader N, Filler SG, Sheppard DC (2010) Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol 12(4):473–488. https://doi.org/10.1111/j.1462-5822.2009.01408.x
Ho CY, Smith M, Houston ME, Adamson JG, Hodges RS (2002) A possible mechanism for partitioning between homo- and heterodimerization of the yeast homeodomain proteins MATa1 and MATα2. J Pept Res 59(1):34–43
Jiang J, Liu X, Yin Y, Ma Z (2011) Involvement of a velvet protein FgVeA in the regulation of asexual development, lipid and secondary metabolisms and virulence in Fusarium graminearum. PLoS One 6(11):e28291. https://doi.org/10.1371/journal.pone.0028291
Jonkers W, Dong Y, Broz K, Kistler HC (2012) The Wor1-like protein Fgp1 regulates pathogenicity, toxin synthesis and reproduction in the phytopathogenic fungus Fusarium graminearum. PLoS Pathog 8(5):e1002724. https://doi.org/10.1371/journal.ppat.1002724
Khang CH, Park SY, Lee YH, Kang S (2005) A dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet Biol 42(6):483–492
Kim JE, Han KH, Jin J, Kim H, Kim JC, Yun SH, Lee YW (2005) Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl Environ Microbiol 71(4):1701–1708. https://doi.org/10.1128/AEM.71.4.1701-1708.2005
Kim JE, Jin J, Kim H, Kim JC, Yun SH, Lee YW. (2006) GIP2, a putative transcription factor that regulates the aurofusarin biosynthetic gene cluster in Gibberella zeae. Appl Environ Microbiol 72 (2):1645-1652
Kim S, Park SY, Kim KS, Rho HS, Chi MH, Choi J, Park J, Kong S, Park J, Goh J, Lee YH (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5(12):e1000757. https://doi.org/10.1371/journal.pgen.1000757
Kim HK, Cho EJ, Lee S, Lee YS, Yun SH (2012) Functional analyses of individual mating-type transcripts at MAT loci in Fusarium graminearum and Fusarium asiaticum. FEMS Microbiol Lett 337(2):89–96. https://doi.org/10.1111/1574-6968.12012
Kim Y, Kim H, Son H, Choi GJ, Kim JC, Lee YW (2014) MYT3, a Myb-like transcription factor, affects fungal development and pathogenicity of Fusarium graminearum. PLoS One 9(4):e94359. https://doi.org/10.1371/journal.pone.0094359
Kim HK, Jo SM, Kim GY, Kim DW, Kim YK, Yun SH (2015) A large-scale functional analysis of putative target genes of mating-type loci provides insight into the regulation of sexual development of the cereal pathogen Fusarium graminearum. PLoS Genet 11(9):e1005486. https://doi.org/10.1371/journal.pgen.1005486
Lau GW, Hamer JE (1998) Acropetal: a genetic locus required for conidiophore architecture and pathogenicity in the rice blast fungus. Fungal Genet Biol 24(1-2):228–239. https://doi.org/10.1006/fgbi.1998.1053
Lin Y, Son H, Lee J, Min K, Choi GJ, Kim JC, Lee YW (2011) A putative transcription factor MYT1 is required for female fertility in the ascomycete Gibberella zeae. PLoS One 6(10):e25586. https://doi.org/10.1371/journal.pone.0025586
Lin Y, Son H, Min K, Lee J, Choi GJ, Kim JC, Lee YW (2012) A putative transcription factor MYT2 regulates perithecium size in the ascomycete Gibberella zeae. PLoS One 7(5):e37859. https://doi.org/10.1371/journal.pone.0037859
Liu N, Fan F, Qiu D, Jiang L (2013) The transcription cofactor FgSwi6 plays a role in growth and development, carbendazim sensitivity, cellulose utilization, lithium tolerance, deoxynivalenol production and virulence in the filamentous fungus Fusarium graminearum. Fungal Genet Biol 58-59:42–52. https://doi.org/10.1016/j.fgb.2013.08.010
Lysoe E, Klemsdal SS, Bone KR, Frandsen RJ, Johansen T, Thrane U, Giese H (2006) The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Appl Environ Microbiol 72(6):3924–3932. https://doi.org/10.1128/AEM.00963-05
Lysoe E, Pasquali M, Breakspear A, Kistler HC (2011) The transcription factor FgStuAp influences spore development, pathogenicity, and secondary metabolism in Fusarium graminearum. Mol Plant-Microbe Interact 24(1):54–67. https://doi.org/10.1094/MPMI-03-10-0075
Martinelli SD (1979) Phenotypes of double conidiation mutants of Aspergillus nidulans. J Gen Microbiol 114(2):277–287. https://doi.org/10.1099/00221287-114-2-277
Matar KAO, Chen X, Chen D, Anjago WM, Norvienyeku J, Lin Y, Chen M, Wang Z, Ebbole DJ, Lu GD (2017) WD40-repeat protein MoCreC is essential for carbon repression and is involved in conidiation, growth and pathogenicity of Magnaporthe oryzae. Curr Genet 63(4):685–696. https://doi.org/10.1007/s00294-016-0668-1
Mateos L, Jimenez A, Revuelta JL, Santos MA (2006) Purine biosynthesis, riboflavin production, and trophic-phase span are controlled by a Myb-related transcription factor in the fungus Ashbya gossypii. Appl Environ Microbiol 72(7):5052–5060. https://doi.org/10.1128/AEM.00424-06
McMullen M, Jones R, Gallenberg D (1997) Scab of wheat and barley: a re-emerging disease of devastating impact. Plant Dis 18(12):1340–1348
Min K, Son H, Lim JY, Choi GJ, Kim JC, Harris SD, Lee YW (2014) Transcription factor RFX1 is crucial for maintenance of genome integrity in Fusarium graminearum. Eukaryot Cell 13(3):427–436. https://doi.org/10.1128/EC.00293-13
Nishimura M, Hayashi N, Jwa NS, Lau GW, Hamer JE, Hasebe A (2000) Insertion of the LINE retrotransposon MGL causes a conidiophore pattern mutation in Magnaporthe grisea. Mol Plant-Microbe Interact 13(8):892–894. https://doi.org/10.1094/MPMI.2000.13.8.892
Odenbach D, Breth B, Thines E, Weber RW, Anke H, Foster AJ (2007) The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Mol Microbiol 64(2):293–307. https://doi.org/10.1111/j.1365-2958.2007.05643.x
Ohara T, Inoue I, Namiki F, Kunoh H, Tsuge T (2004) REN1 is required for development of microconidia and macroconidia, but not of chlamydospores, in the plant pathogenic fungus Fusarium oxysporum. Genetics 166(1):113–124
Park HS, Yu JH (2012) Genetic control of asexual sporulation in filamentous fungi. Curr Opin Microbiol 15(6):669–677. https://doi.org/10.1016/j.mib.2012.09.006
Park AR, Cho AR, Seo JA, Min K, Son H, Lee J, Choi GJ, Kim JC, Lee YW (2012) Functional analyses of regulators of G protein signaling in Gibberella zeae. Fungal Genet Biol 49(7):511–520. https://doi.org/10.1016/j.fgb.2012.05.006
Pasquali M, Kistler C (2006) Gibberella zeae ascospore production and collection for microarray experiments. J Vis Exp 30(1):115. https://doi.org/10.3791/115
Pestka JJ, Smolinski AT (2005) Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health B Crit Rev 8(1):39–69. https://doi.org/10.1080/10937400590889458
Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant-Microbe Interact 8(4):593–601
Ruiz-Roldan C, Pareja-Jaime Y, Gonzalez-Reyes JA, Roncero MI (2015) The transcription factor Con7-1 is a master regulator of morphogenesis and virulence in Fusarium oxysporum. Mol Plant-Microbe Interact 28(1):55–68. https://doi.org/10.1094/MPMI-07-14-0205-R
Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, Lin Y, Cao P, Hong SY, Kim EK, Lee SH, Cho A, Lee S, Kim MG, Kim Y, Kim JE, Kim JC, Choi GJ, Yun SH, Lim JY, Kim M, Lee YH, Choi YD, Lee YW (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7(10):e1002310. https://doi.org/10.1371/journal.ppat.1002310
Son H, Kim MG, Min K, Seo YS, Lim JY, Choi GJ, Kim JC, Chae SK, Lee YW (2013) AbaA regulates conidiogenesis in the ascomycete fungus Fusarium graminearum. PLoS One 8(9):e72915. https://doi.org/10.1371/journal.pone.0072915
Son H, Kim MG, Chae SK, Lee YW (2014a) FgFlbD regulates hyphal differentiation required for sexual and asexual reproduction in the ascomycete fungus Fusarium graminearum. J Microbiol 52(11):930–939. https://doi.org/10.1007/s12275-014-4384-6
Son H, Kim MG, Min K, Lim JY, Choi GJ, Kim JC, Chae SK, Lee YW (2014b) WetA is required for conidiogenesis and conidium maturation in the ascomycete fungus Fusarium graminearum. Eukaryot Cell 13(1):87–98. https://doi.org/10.1128/EC.00220-13
Wang G, Wang C, Hou R, Zhou X, Li G, Zhang S, Xu JR (2012) The AMT1 arginine methyltransferase gene is important for plant infection and normal hyphal growth in Fusarium graminearum. PLoS One 7(5):e38324. https://doi.org/10.1371/journal.pone.0038324
Yang C, Liu H, Li G, Liu M, Yun Y, Wang C, Ma Z, Xu JR (2015) The MADS-box transcription factor FgMcm1 regulates cell identity and fungal development in Fusarium graminearum. Environ Microbiol 17(8):2762–2776. https://doi.org/10.1111/1462-2920.12747
Ye J, Zhang Y, Cui H, Liu J, Wu Y, Cheng Y, Xu H, Huang X, Li S, Zhou A, Zhang X, Bolund L, Chen Q, Wang J, Yang H, Fang L, Shi C (2018) WEGO 2.0: a web tool for analyzing and plotting GO annotations, 2018 update. Nucleic Acids Res 46(W1):W71–W75. https://doi.org/10.1093/nar/gky400
Zhang YZ, Wei ZZ, Liu CH, Chen Q, Xu BJ, Guo ZR, Cao YL, Wang Y, Han YN, Chen C, Feng X, Qiao YY, Zong LJ, Zheng T, Deng M, Jiang QT, Li W, Zheng YL, Wei YM, Qi PF (2017) Linoleic acid isomerase gene FgLAI12 affects sensitivity to salicylic acid, mycelial growth and virulence of Fusarium graminearum. Sci Rep 7:46129. https://doi.org/10.1038/srep46129
Zheng D, Zhang S, Zhou X, Wang C, Xiang P, Zheng Q, Xu JR (2012a) The FgHOG1 pathway regulates hyphal growth, stress responses, and plant infection in Fusarium graminearum. PLoS One 7(11):e49495. https://doi.org/10.1371/journal.pone.0049495
Zheng W, Zhao X, Xie Q, Huang Q, Zhang C, Zhai H, Xu L, Lu G, Shim WB, Wang Z (2012b) A conserved homeobox transcription factor Htf1 is required for phialide development and conidiogenesis in Fusarium species. PLoS One 7(9):e45432. https://doi.org/10.1371/journal.pone.0045432
Zheng H, Zheng W, Wu C, Yang J, Xi Y, Xie Q, Zhao X, Deng X, Lu G, Li G, Ebbole D, Zhou J, Wang Z (2015) Rab GTPases are essential for membrane trafficking-dependent growth and pathogenicity in Fusarium graminearum. Environ Microbiol 17(11):4580–4599. https://doi.org/10.1111/1462-2920.12982
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This research is supported by the International scientific and technological cooperation and exchange project of Fujian Agriculture and Forestry University (KXGH17007) to Guo-dong Lu.
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Fan, G., Zhang, K., Zhang, J. et al. The transcription factor FgMed1 is involved in early conidiogenesis and DON biosynthesis in the plant pathogenic fungus Fusarium graminearum. Appl Microbiol Biotechnol 103, 5851–5865 (2019). https://doi.org/10.1007/s00253-019-09872-2
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DOI: https://doi.org/10.1007/s00253-019-09872-2