Effectors and Their Involvement in Pathogenicity of Wheat Stripe Rust Fungus

doi:10.13560/j.cnki.biotech.bull.1985.2017-0472

Abstract

Abstract: The complex molecules called effectors are secreted during the process of competition and evolution between pathogens and host plants,and they escape or subvert hosts defense responses,as well as interfere with various physiological processes of the host,subsequently,which is beneficial to increase the pathogen’s capacity of fitness,propagation and long-distance migration. Over two thousands of candidate effectors were predicted in Puccinia striiformis f. sp. tritici（Pst）based on the genome or transcriptome sequences,however,few have been analyzed for their effector function because of lacking an efficient and reliable system for stable transformation. In this paper,we summarized the current knowledge of effectors for its classification and structure characterization,and explained the molecular basis of interaction between Pst and host,along with technological methods suitable for function analysis in Pst. Also we considered the relationship between the targeted subcellular compartments of hosts and pathogenesis. These progresses may help comprehensively understand the biology of the effectors,and may be beneficial to offer further insights into the pathogenesis in Pst and to contribute new strategies for durably controlling this disease.

Key words: wheat stripe rust, effectors, pathogenesis

LIU Xiu-feng, YUAN Wen-ya, SUN Zhen-yu, LIANG Dan, SHI Xiao-wei. Effectors and Their Involvement in Pathogenicity of Wheat Stripe Rust Fungus[J]. Biotechnology Bulletin, 2018, 34(2): 112-120.

References

[1] Jones JD, Dang JL.The plant immune system[J]. Nature, 2006, 444:323-329.
[2] Sonah H, Deshmukh RK, Bélanger RR.Computational prediction of effector proteins in fungi:opportunities and challenges[J]. Front Plant Sci, 2016, 7:126-132.
[3] Guttman DS, McHardy AC, Schulze-Lefert P. Microbial genome- enabled insights into plant-micro organism interactions[J]. Nat Rev, 2014, 15:797-813.
[4] Selin C, Kievit TR, Belmonte MF, et al.Elucidating the role of effectors in plant-fungal interactions:progress and challenges[J]. Front Microbiol, 2016, 7:600-610.
[5] Win J, Chaparro-Garcia A, Belhaj K, et al.Effector biology of plant associated organisms:concepts and perspectives[J]. Cold Spring Harb Symp Quant Biol, 2012, 77:235-247.
[6] 李振岐, 曾士迈. 中国小麦锈病[M]. 北京:中国农业出版社, 2002.
[7] 康振生, 王晓杰, 赵杰, 等. 小麦条锈菌致病性及其变异研究进展[J]. 中国农业科学, 2015, 17:3439-3453.
[8] Thach T, Ali S, de Vallavieille-Pope C, et al. Worldwide population structure of the wheat rust fungus Puccinia striiformis in the past[J]. Fungal Genet Biol, 2016, 87:1-8.
[9] Schwessinger B.Fundamental wheat stripe rust research in the 21^st century[J]. New Phytol, 2017, 213:1625-1631.
[10] Derevnina L, Richard WM.Wheat rusts never sleep but neither do sequencers:will pathogenomics transform the way plant diseases are managed?[J]. Genome Biol, 2015, 16:44.
[11] Hesham AYG, Bart PHJT, Michael FS.The age of effectors:genome-based discovery and applications[J]. Phytopathology, 2016, 106:1206-1212.
[12] Cantu D, Govindarajulu M, Kozik A, et al.Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust[J]. PLoS One, 2011, 6:e24230.
[13] Cantu D, Segovia V, MacLean D. Genome analyses of the wheat yellow(stripe)rust pathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors[J]. BMC Genomics, 2013, 14:270.
[14] Zheng W, Huang L, Huang J, et al.High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus[J]. Nat Commun, 2013, 4:2673.
[15] Duplessis S, Cuomo CA, Lin YC, et al.Obligate biotrophy features unraveled by the genomic analysis of rust fungi[J]. Proc Natl Acad Sci USA, 2011, 108:9166-9171.
[16] Christina AC, Guus B, Hala BK, et al.Comparative analysis highlights variable genome content of wheat rusts and divergence of the mating loci[J]. G3(Bethesda), 2017, 7:361-376.
[17] Sun F, Kale SD, Azurmendi HF, et al.Structural basis for interactions of the Phytophthora sojae RxLR effector Avh5 with phosphatidylinositol 3-phosphate and for host cell entry[J]. Mol Plant Microbe Interact, 2013, 26:330-344.
[18] Ye W, Wang Y, Wang Y.Bioinformatics analysis reveals abundant short alpha-helices as a common structural feature of oomycete RxLR effector proteins[J]. PLoS One, 2015, 10:e0135240.
[19] Sonah H, Deshmukh RK, Bélanger RR.Computational prediction of effector proteins in fungi:opportunities and challenges[J]. Front Plant Sci, 2016, 7:126-132.
[20] Tanaka S, Djamei A, Presti LL, et al.Experimental approaches to investigate effector translocation into host cells in the Ustilago maydis/maize patho system[J]. Eur J Cell Biol, 2015, 94:349-358.
[21] Petre B, Joly DL, Duplessis S.Effector proteins of rust fungi[J]. Front Plant Sci, 2014, 5:416.
[22] De Wit PJ, Testa AC, Oliver RP.Fungal plant pathogenesis mediated by effectors[J]. Microbiol Spectrum, 2016, 4(6):18-26.
[23] Hogenhout SA, van der Hoorn RA, Terauchi R, et al. Emerging concepts in effector biology of plant-associated organisms[J]. Mol Plant Microbe Interact, 2009, 22:115-122.
[24] Kamoun S.A catalogue of the effector secretome of plant pathogenic oomycetes[J]. Annu Rev Phytopathol, 2006, 44:41-60.
[25] Spanu PD, Abbott JC, Amselem J, et al.Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism[J]. Science, 2010, 330:1543-1546.
[26] Saunders DG, Win J, Cano LM, et al.Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi[J]. PLoS One, 2012, 7:e29847.
[27] Nemri A, Saunders DG, Anderson C, et al.The genome sequence and effector complement of the flax rust pathogen Melamp soralini[J]. Front Plant Sci, 2014, 5:98.
[28] Petre B, Kamoun S.How do filamentous pathogens deliver effector proteins into Plant Cells?[J]. PLoS Biol, 2014, 12:e1001801.
[29] Gout L, Fudal I, Kuhn ML, et al.Lost in the middle of nowhere:the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans[J]. Mol Microbiol, 2006, 60:67-80.
[30] Prateek C, Bulbul, David LJ, et al.Effector biology during biotrophic invasion of Plant Cells[J]. Virulence, 2014, 5:703-709.
[31] Giraldo MC, Valent B.Filamentous plant pathogen effectors in action[J]. Nat Rev Microbiol, 2013, 11:800-814.
[32] Caillaud MC, Piquerez SJ, Fabro G, et al.Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility[J]. Plant J, 2012, 69:252-265.
[33] Godfrey D, Böhlenius H, Pedersen C, et al.Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif[J]. BMC Genomics, 2010, 11:317-322.
[34] Oliveira-Garcia E, Valent B.How eukaryotic filamentous pathogens evade plant recognition[J]. Curr Opin Microbiol, 2015, 26:92-101
[35] Mueller AN, Ziemann S, Treitschke S, et al.Compatibility in the Ustilago maydis maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2[J]. PLoS Pathog, 2013, 9:e1003177.
[36] Garnica DP, Nemri A, Upadhyaya NM, et al.The ins and outs of rust haustoria[J]. PLoS Pathog, 2014, 10:e1004329.
[37] Redkar A, Hoser R, Schilling L, et al.A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors[J]. Plant Cell, 2015, 27:1332-1351.
[38] Hemetsberger C, Mueller AN, Matei A, et al.The fungal core effector Pep1 is conserved across smuts of dicots and monocots[J]. New Phytol, 2015, 206:1116-1126.
[39] Doehlemann G, van der Linde K, Assmann D, et al. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of Plant Cells[J]. PLoS Pathog, 2009, 5:e1000290.
[40] Djamei A, Schipper K, Rabe F, et al.Metabolic priming by a secreted fungal effector[J]. Nature, 2011, 478:395-398.
[41] Gueddari NE, Rauchhaus U, Moerschbacher BM, et al.Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi[J]. New Phytol, 2002, 156:103-112.
[42] Ellis JG, Dodds PN, Lawrence GJ.Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions[J]. Annu Rev Phytopathol, 2007, 45:289-306.
[43] Kemen E, Kemen AC, Rafiqi M, et al.Identification of a protein from rust fungi transferred from haustoria into infected Plant Cells[J]. Mol Plant Microbe Interact, 2005, 18:1130-1139.
[44] Upadhyaya NM, Mago R, Staskawicz BJ, et al.A bacterial type III secretion assay for delivery of fungal effector proteins into wheat[J]. Mol Plant Microbe Interact, 2014, 27:255-264.
[45] Ramachandran S, Yin C, Kud J, et al.Effectors from wheat rust fungi suppress multiple plant defense responses[J]. Phytopathology, 2017, 107:75-83.
[46] Petre B, Saunders DGO, Sklenar J, et al.Heterologous expression Screens in Nicotiana benthamiana identify a candidate effector of the wheat yellow rust pathogen that associates with processing bodies[J]. PLoS One, 2016, 11:e0149035.
[47] Liu CH, Pedersen C, Schultz-Larsen T, et al.The stripe rust fungal effector PEC6 suppresses pattern-triggered immunity in a host species-independent manner and interacts with adenosine kinases[J]. New Phytol, 2016, DOI:10. 1111/nph. 14034.
[48] Yin C, Chen X, Wang X, et al.Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici[J]. BMC Genomics, 2009, 10:626-633.
[49] Cheng YL, Wu K, Yao JN, et al.PSTha5a23, a candidate effector from the obligate biotrophic pathogen Puccinia striiformis f. sp. tritici, is involved in plant defense suppression and rust pathogenicity[J]. Environ Microbiol, 2017, 19:1717-1729.
[50] Wang XD, Yang BJ, Li K, et al.A conserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis-related genes in response to pathogens[J]. Mol Plant Microbe Interact, 2016, 29:977-989.
[51] Wirthmueller L, Maqbool A, Banfield MJ.On the front line:structural insights into plant-pathogen interactions[J]. Nat Rev Microbiol, 2013, 11:761-776.
[52] Qutob D, Tedman-Jones J, Dong S, et al.Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a[J]. PLoS One, 2009, 4:e5066.
[53] Ali S, Laurie JD, Linning R, et al.An immunity-triggering effector from the Barley smut fungus Ustilago hordei resides in an Ustilaginaceae-specific cluster bearing signs of transposable element-assisted evolution[J]. PLoS Pathog, 2014, 10:e1004223.
[54] Rep M, van der Does HC, Meijer M, et al. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato[J]. Mol Microbiol, 2004, 53:1373-1383.
[55] Na R, Gijzen M.Escaping host immunity:new tricks for plant pathogens[J]. PLoS Pathog, 2016, 12:e1005631.
[56] Shan WX, Cao M, Dan LU, et al.The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b[J]. Mol Plant Microbe Interact, 2004, 17:394-403.