大丽轮枝菌致病及微菌核形成相关基因研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2017-1025

摘要/Abstract

摘要： 大丽轮枝菌（Verticillium dahliae）致病力强且宿主范围广,能以微菌核的形式在土壤中存活多年,当遇到合适的宿主就萌发,因此极难防控,对农业生产造成巨大危害。目前已经发现多种影响大丽轮枝菌致病力的基因,最为重要的发现为大丽轮枝菌能够形成侵入钉入侵植物,许多效应因子也是由侵入钉颈环处分泌出大丽轮枝菌并最终调控植物的免疫防御。同时,研究也表明黑色素对于形成成熟的微菌核非常关键,并且许多与微菌核形成相关的基因也与大丽轮枝菌致病相关。但目前的研究尚未完全阐明大丽轮枝菌如何导致植物萎蔫坏死以及微菌核形成的分子机理。综述了近年来有关大丽轮枝菌致病及微菌核相关基因的研究进展,以期为大丽轮枝菌致病及微菌核形成机理的进一步研究奠定理论基础。

关键词: 大丽轮枝菌, 致病基因, 微菌核, 分子机理

Abstract: Verticillium dahliae causes serious damages to agricultural production because of its strong pathogenicity and wide host area,as well as it may live many years as microsclerotia in soil,and germinate as long as there is a appropriate host,thus it is particularly difficult to control it. Currently,the many genes affecting the pathogenicity of V. dahliae have been discovered,and the most critical result is that penetration pegs are generated to infect plant,and some effectors were secreted to be V. dahliae at the hyphal neck of penetration pegs,which regulates plant immunity. Furthermore,the studies have suggested that melanin was vital for the formation of mature microsclerotia,and some genes involved in microsclerotia formation also were related to V. dahliae pathogenicity. However,current researches did not completely elucidate the molecular mechanisms of V. dahliae causing plant wilting and necrosis and microsclerotia formation. This review summarizes research advances on V. dahliae genes involved in pathogenicity and microsclerotia formation,aiming at establishing the theoretical basis for further research on the mechanisms of V. dahliae pathogenicity and microsclerotia formation.

Key words: Verticillium dahliae, pathogenetic gene, microsclerotia, molecular mechanism

谢成建. 大丽轮枝菌致病及微菌核形成相关基因研究进展[J]. 生物技术通报, 2018, 34(4): 51-59.

XIE Cheng-jian. Research Advances on Verticillium dahliae Genes Resulting in Pathogenicity and Microsclerotia Formation[J]. Biotechnology Bulletin, 2018, 34(4): 51-59.

参考文献

[1] Maruthachalam K, Klosterman SJ, Kang S, et al.Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNA insertional mutagenesis[J]. Mol Biotechnol, 2011, 49(3):209-221.
[2] Fradin EF and Thomma BP. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum[J]. Mol Plant Pathol, 2006, 7(2):71-86.
[3] Amyotte SG, Tan X, Pennerman K, et al.Transposable elements in phytopathogenic Verticillium spp. :insights into genome evolution and inter- and intra-specific diversification[J]. BMC Genomics, 2012, 13:314.
[4] Rauyaree P, Ospina-Giraldo MD, Kang S, et al.Mutations in VMK1, a mitogen-activated protein kinase gene, affect microsclerotia formation and pathogenicity in Verticillium dahliae[J]. Curr Genet, 2005, 48(2):109-116.
[5] Xie C, Wang C, Wang X, et al.Proteomics-based analysis reveals that Verticillium dahliae toxin induces cell death by modifying the synthesis of host proteins[J]. Journal of General Plant Pathology, 2013, 79(5):335-345.
[6] Klosterman SJ, Subbarao KV, Kang S, et al.Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens[J]. PLoS Pathog, 2011, 7(7):e1002137.
[7] Liu SY, Chen JY, Wang JL, et al.Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae[J]. Gene, 2013, 529(2):307-316.
[8] Chen JY, Xiao HL, Gui YJ, et al.Characterization of the Verticillium dahliae exoproteome involves in pathogenicity from cotton-containing medium[J]. Front Microbiol, 2016, 7:1709.
[9] Tzima AK, Paplomatas EJ, Rauyaree P, et al.VdSNF1, the sucrose nonfermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell-wall degradation[J]. Mol Plant Microbe Interact, 2011, 24(1):129-142.
[10] Eboigbe L, Tzima AK, Paplomatas EJ, et al.The role of the beta-1, 6-endoglucanase gene vegB in physiology and virulence of Verticillium dahliae[J]. Phytopathologia Mediterranea, 2014, 53(1):94-107.
[11] Chen S, Su L, Chen J, et al.Cutinase:characteristics, preparation, and application[J]. Biotechnol Adv, 2013, 31(8):1754-67.
[12] Gui Y, Zhang W, Zhang D, et al.A Verticillium dahliae extracellular cutinase modulates plant immune responses[J]. Mol Plant Microbe Interact, 208, 31(2):260-273.
[13] Stergiopoulos I and de Wit P. Fungal effector proteins[J]. Annu Rev Phytopathol, 2009, 47:233-263.
[14] de Jonge R, Bolton MD, Kombrink A, et al. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen[J]. Genome Res, 2013, 23(8):1271-1282.
[15] de Jonge R, van Esse HP, Maruthachalam K, et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing[J]. Proc Natl Acad Sci USA, 2012, 109(13):5110-5115.
[16] Zhang Z, van Esse HP, van Damme M, et al. Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis[J]. Molecular Plant Pathology, 2013, 14(7):719-727.
[17] Castroverde CDM, Nazar RN, Robb J.Verticillium Ave1 effector induces tomato defense gene expression independent of Ve1 protein[J]. Plant Signaling & Behavior, 2016, 11(11):e1245254.
[18] Kombrink A, Rovenich H, Shi-Kunne X, et al.Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts[J]. Molecular Plant Pathology, 2017, 18(4):596-608.
[19] Zhang Y, Gao YH, Liang YB, et al.The Verticillium dahliae SnodProt1-Like Protein VdCP1 Contributes to Virulence and Triggers the Plant Immune System[J]. Frontiers in Plant Science, 2017, 8:1880.
[20] Liu W, Zeng H, Liu Z, et al.Mutational analysis of the Verticillium dahliae protein elicitor PevD1 identifies distinctive regions responsible for hypersensitive response and systemic acquired resistance in tobacco[J]. Microbiol Res, 2014, 169(5-6):476-482.
[21] Liu M, Khan NU, Wang N, et al.The protein elicitor PevD1 enhances resistance to pathogens and promotes growth in Arabidopsis[J]. Int J Biol Sci, 2016, 12(8):931-943.
[22] Zhou R, Zhu T, Han L, et al.The asparagine-rich protein NRP interacts with the Verticillium effector PevD1 and regulates the subcellular localization of cryptochrome 2[J]. J Exp Bot, 2017, 68(13):3427-3440.
[23] Liu T, Song T, Zhang X, et al.Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis[J]. Nat Commun, 2014, 5:4686.
[24] Zhang L, Ni H, Du X, et al.The Verticillium-specific protein VdSCP7 localizes to the plant nucleus and modulates immunity to fungal infections[J]. New Phytol, 2017, 215(1):368-381.
[25] Wang JY, Cai Y, Gou JY, et al.VdNEP, an elicitor from Verticillium dahliae, induces cotton plant wilting[J]. Appl Environ Microbiol, 2004, 70(8):4989-4995.
[26] Yao Z, Rashid KY, Adam LR, et al.Verticillium dahliae’s VdNEP acts both as a plant defence elicitor and a pathogenicity factor in the interaction with Helianthus annuus[J]. Canadian Journal of Plant Pathology, 2011, 33(3):375-388.
[27] Santhanam P, Esse PV, Albert I, et al.Evidence for functional diversification within a fungal NEP1-like protein family[J]. Mol Plant Microbe Interact, 2013, 26(3):278-286.
[28] Zhou BJ, Jia PS, Gao F, et al.Molecular characterization and functional analysis of a necrosis- and ethylene-inducing, protein-encoding gene family from Verticillium dahliae[J]. Molecular Plant-Microbe Interactions, 2012, 25(7):964-975.
[29] Zhao YL, Zhou TT, Guo HS.Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+ signaling is required for plant infection by Verticillium dahliae[J]. PLoS Pathog, 2016, 12(7):e1005793.
[30] Zhou TT, Zhao YL, Guo HS.Secretory proteins are delivered to the septin-organized penetration interface during root infection by Verticillium dahliae[J]. PLoS Pathog, 2017, 13(3):e1006275.
[31] Tzima A, Paplomatas EJ, Rauyaree P, et al.Roles of the catalytic subunit of cAMP-dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae[J]. Fungal Genet Biol, 2010, 47(5):406-415.
[32] Tzima AK, Paplomatas EJ, Tsitsigiannis DI, et al.The G protein beta subunit controls virulence and multiple growth- and development-related traits in Verticillium dahliae[J]. Fungal Genet Biol, 2012, 49(4):271-283.
[33] Wang FX, Ma YP, Yang CL, et al.Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae[J]. Proteomics, 2011, 11(22):4296-4309.
[34] Pantelides IS, Tjamos SE, Paplomatas EJ.Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae[J]. Molecular Plant Pathology, 2010, 11(2):191-202.
[35] Deng S, Wang CY, Zhang X, et al.VdNUC-2, the Key Regulator of phosphate responsive signaling pathway, is required for Verticillium dahliae infection[J]. PLoS One, 2015, 10(12):e0145190.
[36] Santhanam P, Boshoven JC, Salas O, et al.Rhamnose synthase activity is required for pathogenicity of the vascular wilt fungus Verticillium dahliae[J]. Mol Plant Pathol, 2017, 18(3):347-362.
[37] Hoppenau CE, Tran V-T, Kusch H, et al.Verticillium dahliae VdTHI4, involved in thiazole biosynthesis, stress response and DNA repair functions, is required for vascular disease induction in tomato[J]. Environ Exp Bot, 2014, 108:14-22.
[38] Qi X, Su X, Guo H, et al.VdThit, a thiamine transport protein, is required for pathogenicity of the vascular pathogen Verticillium dahliae[J]. Mol Plant Microbe Interact, 2016, 29(7):545-559.
[39] Timpner C, Braus-Stromeyer S, Tran V, et al.The Cpc1 regulator of the cross-pathway control of amino acid biosynthesis is required for pathogenicity of the vascular pathogen Verticillium longisporum[J]. Mol Plant Microbe Interact, 2013, 26(11):1312-1324.
[40] Van Twest SM, Grant SJ, Cucullo J, et al.Characterization of ATG8 autophagy gene homologs in Verticillium dahliae and Verticillium albo-atrum[J]. Phytopathology, 2011, 101(6):S251.
[41] El Hadrami A, Islam MR, Adam LR, et al.A cupin domain-containing protein with a quercetinase activity(VdQase)regulates Verticillium dahliae’s pathogenicity and contributes to counteracting host defenses[J]. Front Plant Sci, 2015, 6:440.
[42] Islam MR, Eihardami A, Adam LR, et al.A cupin domain containing protein(VdQase)is required for optimum virulence in Verticillium dahliae[J]. Canadian Journal of Plant Pathology, 2014, 36(2):267-268.
[43] Tian H, Zhou L, Guo W, et al.Small GTPase Rac1 and its interaction partner Cla4 regulate polarized growth and pathogenicity in Verticillium dahliae[J]. Fungal Genet Biol, 2015, 74:21-31.
[44] Qi X, Zhou S, Shang X, et al.VdSho1 Regulates Growth, Oxidant Adaptation and Virulence in Verticillium dahliae[J]. Journal of Phytopathology, 2016, 164(11-12):1064-1074.
[45] Santhanam P and Thomma BP. Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes[J]. Mol Plant Microbe Interact, 2013, 26(2):249-256.
[46] Fang Y, Xiong D, Tian L, et al.Functional characterization of two bZIP transcription factors in Verticillium dahliae[J]. Gene, 2017, 626:386-394.
[47] Lopez-Escudero FJ, Roca JM, Valverde-Corredor A, et al.Correlation between virulence and morphological characteristics of microsclerotia of Verticillium dahliae isolates infecting olive[J]. Journal of Phytopathology, 2012, 160(7-8):431-433.
[48] Wheeler MH, Tolmsoff WJ, Meola S.Ultrastructure of melanin formation in Verticillium-Dahliae with(+)-scytalone as a biosynthetic intermediate[J]. Canadian Journal of Microbiology, 1976, 22(5):702-711.
[49] Griffiths DA.The fine structure of developing microsclerotia of Verticillium dahliae Kleb[J]. Archiv für Mikrobiologie, 1970, 74(3):207-212.
[50] Brown MF, Wyllie TD.Ultrastructure of microsclerotia of Vertici-llium alboatrum[J]. Phytopathology, 1970, 60:538-542.
[51] Neumann MJ, Dobinson KF.Sequence tag analysis of gene expre-ssion during pathogenic growth and microsclerotia development in the vascular wilt pathogen Verticillium dahliae[J]. Fungal Genet Biol, 2003, 38(1):54-62.
[52] Fan R, Klosterman SJ, Wang C, et al.Vayg1 is required for microsclerotium formation and melanin production in Verticillium dahliae[J]. Fungal Genet Biol, 2017, 98:1-11.
[53] Xiong DG, Wang YL, Ma J, et al.Deep mRNA sequencing reveals stage-specific transcriptome alterations during microsclerotia development in the smoke tree vascular wilt pathogen, Verticillium dahliae[J]. BMC Genomics, 2014, 15:324.
[54] Zhang T, Zhang BS, Hua CL, et al.VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae[J]. Science China-Life Sciences, 2017, 60(8):868-879.
[55] Luo X, Mao H, Wei Y, et al.The fungal-specific transcription factor Vdpf influences conidia production, melanized microsclerotia formation and pathogenicity in Verticillium dahliae[J]. Molecular Plant Pathology, 2016, 17(9):1364-1381.
[56] Bell A, Puhalla J, Tolmsoff W, et al.Use of mutants to establish(+)-scytalone as an intermediate in melanin biosynthesis by Verticillium dahliae[J]. Canadian Journal of Microbiology, 1976, 22(6):787-799.
[57] Duressa D, Anchieta A, Chen D, et al.RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae[J]. BMC Genomics, 2013, 14:607.
[58] Xiong DG, Wang YL, Tian LY, et al.MADS-Box Transcription Factor VdMcm1 Regulates Conidiation, Microsclerotia Formation, Pathogenicity, and Secondary Metabolism of Verticillium dahliae[J]. Frontiers in Microbiology, 2016, 7:1192.
[59] Sarmiento-Villamil JL, García-Pedrajas NE, Baeza-Montañez L, et al.The APSES transcription factor Vst1 is a key regulator of development in microsclerotium and resting mycelium producing Verticillium species[J]. Molecular Plant Pathology, 2016, 19(1):59-76.
[60] Xiong D, Wang Y, Tang C, et al.VdCrz1 is involved in microsclerotia formation and required for full virulence in Verticillium dahliae[J]. Fungal Genet Biol, 2015, 82:201-212.
[61] Tran VT, Braus-Stromeyer SA, Kusch H, et al.Verticillium transcription activator of adhesion Vta2 suppresses microsclerotia formation and is required for systemic infection of plant roots[J]. New Phytol, 2014, 202(2):565-581.
[62] Papapostolou I, Georgiou CD.Hydrogen peroxide is involved in the sclerotial differentiation of filamentous phytopathogenic fungi[J]. Appl Microbiol, 2010, 109(6):1929-1936.
[63] Liu J, Yin Y, Song Z, et al.NADH:flavin oxidoreductase/NADH oxidase and ROS regulate microsclerotium development in Nomuraea rileyi[J]. World J Microbiol Biotechnol, 2014, 30(7):1927-1935.
[64] Song Z, Yin Y, Jiang S, et al.Comparative transcriptome analysis of microsclerotia development in Nomuraea rileyi[J]. BMC Genomics, 2013, 14(1):411.
[65] Xiao X, Xie J, Cheng J, et al.Novel secretory protein Ss-Caf1 of the plant-pathogenic fungus Sclerotinia sclerotiorum is required for host penetration and normal sclerotial development[J]. Mol Plant Microbe Interact, 2014, 27(1):40-55.
[66] Yu Y, Jiang D, Xie J, et al.Ss-Sl2, a novel cell wall protein with PAN modules, is essential for sclerotial development and cellular integrity of Sclerotinia sclerotiorum[J]. PLoS One, 2012, 7(4):e34962.
[67] O’Rourke SM, Herskowitz I. Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis[J]. Molecular Biology of the Cell, 2004, 15(2):532-542.
[68] Boisnard S, Ruprich-Robert G, Florent M, et al.Role of Sho1p adaptor in the pseudohyphal development, drugs sensitivity, osmotolerance and oxidant stress adaptation in the opportunistic yeast Candida lusitaniae[J]. Yeast, 2008, 25(11):849-859.
[69] Song Z, Shen L, Yin Y, et al.Role of two Nomuraea rileyi transmembrane sensors Sho1p and Sln1p in adaptation to stress due to changing culture conditions during microsclerotia development[J]. World J Microbiol Biotechnol, 2015, 31(3):477-485.
[70] Brewster JL, Devaloir T, Dwyer ND, et al.An osmosensing signal transduction pathway in yeast[J]. Science, 1993, 259(5102):1760-1763.
[71] Tian L, Xu J, Zhou L, et al.VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae[J]. Gene, 2014, 550(2):238-244.
[72] Wang YL, Tian LY, Xiong DG, et al.The mitogen-activated protein kinase gene, VdHog1, regulates osmotic stress response, microsclerotia formation and virulence in Verticillium dahliae[J]. Fungal Genet Biol, 2016, 88:13-23.
[73] Tian LY, Wang YL, Yu J, et al.The mitogen-activated protein kinase kinase VdPbs2 of Verticillium dahliae regulates microsclerotia formation, stress response, and plant infection[J]. Frontiers in Microbiology, 2016, 7:1532.
[74] Chen C, Harel A, Gorovoits R, et al.MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing[J]. Mol Plant Microbe Interact, 2004, 17(4):404-413.
[75] Bashi ZD, Gyawali S, Bekkaoui D, et al.The Sclerotinia sclerotiorum Slt2 mitogen-activated protein kinase ortholog, SMK3, is required for infection initiation but not lesion expansion[J]. Can J Microbiol, 2016, 62(10):836-850.
[76] Song ZY, Zhong Q, Yin YP, et al.The high osmotic response and cell wall integrity pathways cooperate to regulate morphology, microsclerotia development, and virulence in Metarhizium rileyi[J]. Scientific Reports, 2016, 6:38765.
[77] He XJ, Li XL and Li YZ. Disruption of Cerevisin via Agrobacterium tumefaciens-mediated transformation affects microsclerotia formation and virulence of Verticillium dahliae[J]. Plant Pathology, 2015, 64(5):1157-1167.
[78] Xie C, Li Q, Yang X.Characterization of VdASP F2 secretory factor from Verticillium dahliae by a fast and easy gene knockout system[J]. Mol Plant Microbe Interact, 2017, 30(6):444-454.
[79] Tang C, Xiong D, Fang Y, et al.The two-component response regulator VdSkn7 plays key roles in microsclerotial development, stress resistance and virulence of Verticillium dahliae[J]. Fungal Genet Biol, 2017, 108:26-35.
[80] Gao F, Zhou BJ, Li GY, et al.A glutamic acid-rich protein identified in Verticillium dahliae from an insertional mutagenesis affects microsclerotial formation and pathogenicity[J]. PLoS One, 2010, 5(12):e15319.
[81] Klimes A, Dobinson KF.A hydrophobin gene, VDH1, is involved in microsclerotial development and spore viability in the plant pathogen Verticillium dahliae[J]. Fungal Genet Biol, 2006, 43
(4):283-294.
[82] Klimes A, Amyotte SG, Grant S, et al.Microsclerotia development in Verticillium dahliae:Regulation and differential expression of the hydrophobin gene VDH1[J]. Fungal Genet Biol, 2008, 45(12):1525-1532.
[83] Wang L, Wu SM, Zhu Y, et al.Functional characterization of a novel jasmonate ZIM-domain interactor(NINJA)from upland cotton(Gossypium hirsutum)[J]. Plant Physiol Biochem, 2017, 112:152-160.
[84] Li ZF, Liu YJ, Feng ZL, et al.VdCYC8, encoding CYC8 glucose repression mediator protein, is required for microsclerotia formation and full virulence in Verticillium dahliae[J]. PLoS One, 2015, 10(12):e0144020.
[85] Zhang YL, Mao JC, Huang JF, et al.A uracil-DNA glycosylase functions in spore development and pathogenicity of Verticillium dahliae[J]. Physiological and Molecular Plant Pathology, 2015, 92:148-153.
[86] Zhang YL, Li ZF, Feng ZL, et al.Functional analysis of the pathogenicity-related gene VdPR1 in the vascular wilt fungus Verticillium dahliae[J]. PLoS One, 2016, 11(11):e0166000.
[87] Zhang YL, Li ZF, Feng ZL, et al.Isolation and functional analysis of the pathogenicity-related gene VdPR3 from Verticillium dahliae on cotton[J]. Curr Genet, 2015, 61(4):555-566.
[88] Yuan L, Su Y, Zhou S, et al.A RACK1-like protein regulates hyphal morphogenesis, root entry and in vivo virulence in Verticillium dahliae[J]. Fungal Genet Biol, 2017, 99:52-61.
[89] Sperschneider J, Gardiner DM, Dodds PN, et al.EffectorP:predicting fungal effector proteins from secretomes using machine learning[J]. New Phytol, 2016, 210(2):743-761.