全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用：99美元
投递稿件

查看量下载量

相关文章

更多...

Novel Disease Susceptibility Factors for Fungal Necrotrophic Pathogens in Arabidopsis

DOI: 10.1371/journal.ppat.1004800

Full-Text   Cite this paper   Add to My Lib

Abstract:

Host cells use an intricate signaling system to respond to invasions by pathogenic microorganisms. Although several signaling components of disease resistance against necrotrophic fungal pathogens have been identified, our understanding for how molecular components and host processes contribute to plant disease susceptibility is rather sparse. Here, we identified four transcription factors (TFs) from Arabidopsis that limit pathogen spread. Arabidopsis mutants defective in any of these TFs displayed increased disease susceptibility to Botrytis cinerea and Plectosphaerella cucumerina, and a general activation of non-immune host processes that contribute to plant disease susceptibility. Transcriptome analyses revealed that the mutants share a common transcriptional signature of 77 up-regulated genes. We characterized several of the up-regulated genes that encode peptides with a secretion signal, which we named PROVIR (for provirulence) factors. Forward and reverse genetic analyses revealed that many of the PROVIRs are important for disease susceptibility of the host to fungal necrotrophs. The TFs and PROVIRs identified in our work thus represent novel genetic determinants for plant disease susceptibility to necrotrophic fungal pathogens.

 References

[1]  Glazebrook J (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–27. pmid:16078883 doi: 10.1146/annurev.phyto.43.040204.135923
[2]  Mengiste T. (2012). Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267–94. doi: 10.1146/annurev-phyto-081211-172955. pmid:22726121
[3]  Van Kan JA (2006). Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253 pmid:16616579 doi: 10.1016/j.tplants.2006.03.005
[4]  Boller T, Felix G (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. doi: 10.1146/annurev.arplant.57.032905.105346. pmid:19400727
[5]  Jones JDG, Dangl JF (2006). The plant immune system. Nature 444: 323–329. pmid:17108957 doi: 10.1038/nature05286
[6]  Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD et al. (2012). The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13: 414–430. doi: 10.1111/j.1364-3703.2011.00783.x. pmid:22471698
[7]  Poinssot B, Vandelle E, Bentéjac M, Adrian M, Levis C, Brygoo Y et al. (2003). The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe Interact 16: 553–564. pmid:12795381 doi: 10.1094/mpmi.2003.16.6.553
[8]  Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007). Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144: 367–379. pmid:17384165 doi: 10.1104/pp.107.095596
[9]  Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107: 9452–9457. doi: 10.1073/pnas.1000675107. pmid:20439716
[10]  Galletti R, Ferrari S, De Lorenzo G. (2011). Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiol 157: 804–814. doi: 10.1104/pp.111.174003. pmid:21803860
[11]  Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. (2010). A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl. Acad. Sci. USA 107: 496–501. doi: 10.1073/pnas.0909705107. pmid:20018686
[12]  Laluk K, Luo H, Chai M, Dhawan R, Lai Z, Mengiste T. (2011). Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 23: 2831–2849. doi: 10.1105/tpc.111.087122. pmid:21862710
[13]  Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X et al. (2010). Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 22:290–301. doi: 10.1016/j.chom.2010.03.007
[14]  Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA et al. (1998). Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbialpathogens. Proc Natl Acad Sci USA, 95, 15107–15111. pmid:9844023 doi: 10.1073/pnas.95.25.15107
[15]  Berrocal-Lobo M1, Molina A, Solano R. (2002). Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23–32. pmid:12060224 doi: 10.1046/j.1365-313x.2002.01191.x
[16]  Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA et al. (2007). ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19: 1665–1681. pmid:17513501 doi: 10.1105/tpc.106.048041
[17]  García-Andrade J, Ramírez V, Flors V, Vera P (2011). Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. Plant J 67: 783–794. doi: 10.1111/j.1365-313X.2011.04633.x. pmid:21564353
[18]  Glawischnig E. (2007). Camalexin. Phytochemistry 68: 401–406. pmid:17217970 doi: 10.1016/j.phytochem.2006.12.005
[19]  Bednarek P, Pi？lewska-Bednarek M, Svato？ A, Schneider B, Doubsky J, Mansurova M et al. (2009). A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101–106. doi: 10.1126/science.1163732. pmid:19095900
[20]  Sánchez-Vallet A, Ramos B, Bednarek P, López G, Pi？lewska-Bednarek M, Schulze-Lefert P et al. (2010). Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J. 63: 115–127. doi: 10.1111/j.1365-313X.2010.04224.x. pmid:20408997
[21]  Hernández-Blanco C, Feng DX, Hu J, Sánchez-Vallet A, Deslandes L, Llorente F, et al. (2007). Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19: 890–903. pmid:17351116 doi: 10.1105/tpc.106.048058
[22]  Cantu D, Vicente AR, Greve LC, Dewey FM, Bennett AB, Labavitch JM et al. (2008). The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea. Proc Natl Acad Sci USA 105: 859–864 doi: 10.1073/pnas.0709813105. pmid:18199833
[23]  Ramírez V, Agorio A, Coego A, García-Andrade J, Hernández MJ, Balaguer B et al. (2011). MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiol 115: 1920–1935. doi: 10.1104/pp.110.171843
[24]  Ellis C, Karafyllidis I, Wastemack C and Turner JG (2002). The Arabidopsis mutant cev1 links cell wall signalling to jasmonate and ethylene responses. Plant Cell 14: 1557–1566. pmid:12119374 doi: 10.1105/tpc.002022
[25]  Moore JW, Loake GJ, Spoel SH (2011). Transcription dynamics in plant immunity. Plant Cell 23: 2809–2820. doi: 10.1105/tpc.111.087346. pmid:21841124
[26]  Qamar SA, Chen Z, Mengiste T (2006). Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48:592–605. pmid:17059405 doi: 10.1111/j.1365-313x.2006.02901.x
[27]  Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011). Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis. Plant Cell 23:1639–1653 doi: 10.1105/tpc.111.084996. pmid:21498677
[28]  Mengiste T1, Chen X, Salmeron J, Dietrich R (2003). The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–65. pmid:14555693 doi: 10.1105/tpc.014167
[29]  Nurmberg PL, Knox KA, Yun BW, Morris PC, Shafiei R, Hudson A et al. (2007). The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. Proc Natl Acad Sci U S A. 104:18795–800. pmid:18003921 doi: 10.1073/pnas.0705586104
[30]  Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009). Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95–101. doi: 10.1126/science.1164627. pmid:19095898
[31]  Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB et al. 2007). MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell. 19: 2225–45. pmid:17616737 doi: 10.1105/tpc.106.048017
[32]  Coego A, Ramirez V, Gil MJ, Flors V, Mauch-Mani B, Vera P (2005). An Arabidopsis homeodomain transcription factor, OVEREXPRESSOR OF CATIONIC PEROXIDASE 3, mediates resistance to infection by necrotrophic pathogens. Plant Cell 17: 2123–2137. pmid:15923348 doi: 10.1105/tpc.105.032375
[33]  García-Andrade J, Ramírez V, López A, Vera P (2013). Mediated plastid RNA editing in plant immunity. PLoS Pathogens 9(10): e1003713. doi: 10.1371/journal.ppat.1003713. pmid:24204264
[34]  Ramírez V, García-Andrade J, Vera P (2011). Enhanced disease resistance to Botrytis cinerea in myb46 Arabidopsis plants is associated to an early downregulation of CesA genes. Plant Signaling & Behavior. 6, 1–3. doi: 10.4161/psb.6.6.15354
[35]  Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–92. pmid:17890373 doi: 10.1105/tpc.107.053678
[36]  Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M et al. (2009). Coexpression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ 32: 1633–1651. doi: 10.1111/j.1365-3040.2009.02040.x. pmid:19712066
[37]  Mutwil M, Klie S, Tohge T, Giorgi FM, Wilkins O, Campbell MM et al. (2011). PlaNet: Combined Sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23: 895–910. doi: 10.1105/tpc.111.083667. pmid:21441431
[38]  Lu P, Chai M, Yang J, Ning G, Wang G, Ma H (2014). The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol 164:1893–1904. doi: 10.1104/pp.113.233387. pmid:24567187
[39]  Bassa C, Etemadi M, Combier J-P, Bouzayen M, Audran-Delalande C (2013). Sl-IAA27 gene expression is induced during arbuscular mycorrhizal symbiosis in tomato and in Medicago truncatula. Plant Signaling & Behavior 8:10, e25637 doi: 10.4161/psb.25637
[40]  Cai S, Lashbrook CC (2008). Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol 146:1305–21. doi: 10.1104/pp.107.110908. pmid:18192438
[41]  Weigel RR, Pfitzner UM and Gatz C (2005). Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell, 17, 1279–1291. pmid:15749762 doi: 10.1105/tpc.104.027441
[42]  Matsubayashi Y, Sakagami Y (2006). Peptide hormones in plants. Annu Rev Plant Biol 57: 649–74. pmid:16669777 doi: 10.1146/annurev.arplant.56.032604.144204
[43]  Matsubayashi Y, Sakagami Y (1996). Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. USA 93:7623–27 pmid:8755525 doi: 10.1073/pnas.93.15.7623
[44]  Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007). Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:18333–38 pmid:17989228 doi: 10.1073/pnas.0706403104
[45]  Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H et al. (2004). Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38:699–713. pmid:15125775 doi: 10.1111/j.1365-313x.2004.02078.x
[46]  Wen J, Lease KA, Walker JC (2004). DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J 37:668–677. pmid:14871303 doi: 10.1111/j.1365-313x.2003.01994.x
[47]  Pearce G, Moura DS, Stratmann J, Ryan CA (2001) RALF, a 5 kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 8:12843–7. doi: 10.1073/pnas.201416998
[48]  Scheer JM, Pearce G, Ryan CA (2005) LeRALF, a plant peptide that regulates root growth and development, specifically binds to 25 and 120 kDa cell surface membrane proteins of Lycopersicon peruvianum. Planta 221:667–74. pmid:15909150 doi: 10.1007/s00425-004-1442-z
[49]  Ellis M, Egelund J, Schultz CJ, Bacic A (2010). Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153: 403–419 doi: 10.1104/pp.110.156000. pmid:20388666
[50]  Mangeon A, Magrani Junqueira R, Sachetto-Martins G (2010). Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5: 99–104. pmid:20009520 doi: 10.4161/psb.5.2.10336
[51]  Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G et al. (2001). Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine-rich protein, AtGRP-3. J Biol Chem 276: 26688–26693. pmid:11335717 doi: 10.1074/jbc.m101283200
[52]  Fukuda H, Higashiyama T (2011). Diverse functions of plant peptides: entering a new phase. Plant Cell Physiol 52: 1–4. doi: 10.1093/pcp/pcq193. pmid:21248365
[53]  Wheeler JI, Irving HR (2010). Evolutionary advantages of secreted peptide signalling molecules in plants. Funct Plant Biol 37: 382–394. doi: 10.1071/fp09242
[54]  Geilfus C-M and Mühling KH (2011). Real-time imaging of leaf apoplastic pH dynamics in response to NaCl stress. Frontiers in Plant Science 2:13. doi: 10.3389/fpls.2011.0001. pmid:22639578
[55]  Popper ZA (2011). Extraction and Detection of Arabinogalactan Proteins in The Plant Cell Wall—Methods and Protocols, edited by John M. Walker. Humana Press, New York, pp.245–254.
[56]  Kinoshita T, Fujita M, Maeda Y (2008). Biosynthesis, remodelling and functions of mammalian GPI-anchored proteins: recent progress. J Biochem 144: 287–294. doi: 10.1093/jb/mvn090
[57]  Johnson KL, Jones BJ, Schultz CJ (2003). The Fasciclin-Like Arabinogalactan Proteins of Arabidopsis. A Multigene Family of Putative Cell Adhesion Molecules. Plant Physiol 133: 1911–1925. pmid:14645732 doi: 10.1104/pp.103.031237
[58]  Ceserani T, Trofka A, Gandotra N, Nelson T. (2009). VH1/BRL2 receptor-like kinase interacts with vascular-specific adaptor proteins VIT and VIK to influence leaf venation. Plant J. 57:1000–1014. doi: 10.1111/j.1365-313X.2008.03742.x. pmid:19000166
[59]  Bendtsen JD, Nielsen H, von Heijne G, Brunak S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–95. pmid:15223320 doi: 10.1016/j.jmb.2004.05.028
[60]  Lapin D. and Van den Ackerveken G. (2013). Susceptibility to plant disease: more than a failure of host immunity. Trends Plant Sci 18: 546–554 doi: 10.1016/j.tplants.2013.05.005. pmid:23790254
[61]  Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. (2009). Plant peptides in signalling: looking for new partners. Trends Plant Sci 14: 255–263. doi: 10.1016/j.tplants.2009.02.002. pmid:19362511
[62]  Jarsch IK, Konrad SSA, Stratil TF, Urbanus SL, Szymanski W, Braun P et al. (2014). Plasma Membranes Are Subcompartmentalized into a Plethora of Coexisting and Diverse Microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26: 1698–1711 pmid:24714763 doi: 10.1105/tpc.114.124446
[63]  López A, Ramírez V, García-Andrade J, Vera P (2011) The RNA silencing enzyme RNA Polymerase V is required for plant immunity. PLoS Genet 7(12): e1002434. doi: 10.1371/journal.pgen.1002434. pmid:22242006
[64]  Ramírez V, López A, Mauch-Mani B, Gil MJ, Vera P (2013). An Extracellular Subtilase Switch for Immune Priming in Arabidopsis. PLoS Pathog 9(6):e1003445. doi: 10.1371/journal.ppat.1003445. pmid:23818851
[65]  Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83–92. pmid:15327980 doi: 10.1016/j.febslet.2004.07.055
[66]  Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825–7. pmid:16982708 doi: 10.1093/bioinformatics/btl476
[67]  Lisanti MP, Caras IW, Rodriguez-Boulan E J (1991). Fusion proteins containing a minimal GPI-attachment signal are apically expressed in transfected MDCK cells. Cell Sci 99: 637–40.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133