doi:

DOI: 10.3724/SP.J.1005.2012.00134

Hereditas (Beijing) (遗传) 2012/34:2 PP.134-144

Advances on molecular mechanisms of plant-pathogen interactions


Abstract:
Plants have established a complicated immune defense system during co-evolution with pathogens. The innate immune system of plants can be generally divided into two levels. One, named PAMP-triggered immunity (PTI), is based on the recognition of pathogen-associated molecular patterns by pattern-recognition receptors, which confers resistance to most pathogenic microbes. The other begins in cytoplasm and mainly relies on recognition of microbial effectors by plant resistance proteins in direct or indirect ways, which then initiates potent defense responses. This process, termed ef-fector-triggered immunity (ETI), is necessary for defense against pathogens that can secret effectors to suppress the first level of immunity. Activation of these two layers of immunity in plant is based on distinguishing and recognition of “self” and “non-self” signals. Recognition of “non-self” signals can activate signal cascades, such as MAPK cascades, which will then induce defense gene expression and corresponding defense responses. In this review, we focused on underlying mo-lecular mechanisms of plant-pathogen interactions and the latest advances of the PTI and ETI signaling network.

Key words:plant,pathogen,innate immunity,resistance gene,signaling pathway

ReleaseDate:2014-07-21 16:04:58



[1] Jones JDG, Dangl JL. The plant immune system. Nature, 2006, 444(7117): 323-329.

[2] Boller T, He SY. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324(5928): 742-744.

[3] Takken FLW, Tameling WIL. To nibble at plant resistance proteins. Science, 2009, 324(5928): 744-746.

[4] Zipfel C. Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol, 2008, 20(1): 10-16.

[5] Naito K, Taquchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant-Microbe Interact, 2008, 21(9): 1165-1174.

[6] van de Veerdonk FL, Kullberg BJ, van der Meer JW, Gow NA, Netea MG. Host-microbe interactions: innate pattern recognition of fungal pathogens. Curr Opin Micro-biol, 2008, 11(4): 305-312.

[7] Postel S, Kemmerling B. Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol, 2009, 20(9): 1025-1031.

[8] Felix G, Duran JD, Volko S, Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J, 1999, 18(3): 265-276.

[9] Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell, 2006, 18(2): 465-476.

[10] Dunning FM, Sun WX, Jansen KL, Helft L, Bent AF. Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell, 2007, 19(10): 3297-3313.

[11] Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G, Shiu SH, Boller T. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol Biol, 2007, 64(5): 539-547.

[12] Hann DR, Rathjen JP. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana bentha-miana. Plant J, 2007, 49(4): 607-618.

[13] Takai R, Isogai A, Takayama S, Che FS. Analysis of flag-ellin perception mediated by flg22 receptor OsFLS2 in rice. Mol Plant-Microbe Interact, 2008, 21(12): 1635-1642.

[14] de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, Tsiamis G, Forsyth A, Robatzek S, Grant M, Boch J. Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant J, 2006, 47(3): 368-382.

[15] Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 2004, 428(6984): 764-767.

[16] Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell, 2004, 16(12): 3496-3507.

[17] Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 2006, 125(4): 749-760.

[18] Dallo SF, Kannan TR, Blaylock MW, Baseman JB. Elon-gation factor Tu and E1 β subunit of pyruvate dehydro-genase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol, 2002, 46(4): 1041-1051.

[19] Granato D, Bergonzelli GE, Pridmore RD, Marvin L, Rouvet M, Corthésy-Theulaz IE. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun, 2004, 72(4): 2160-2169.

[20] Lee Sw, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science, 2009, 326(5954): 850-853.

[21] Ron M, Avni A. The receptor for the fungal elicitor ethyl-ene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell, 2004, 16(6): 1604-1615.

[22] Wang GD, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu CM, Woods-Tör A, Zipfel C, de Wit PJGM, Jones JDG, Tör M, Thomma BPHJ. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol, 2008, 147(2): 503-517.

[23] Ramonell K, Berrocal-Lobo M, Koh S, Wan JR, Edwards H, Stacey G, Somerville S. Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol, 2005, 138(2): 1027-1036.

[24] Fliegmann J, Mithöfer A, Wanner G, Ebel J. An ancient enzyme domain hidden in the putative β-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J Biol Chem, 2004, 279(2): 1132-1140.

[25] Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA, 2006, 103(29): 11086-11091.

[26] Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA, 2007, 104(49): 19613-19618.

[27] Wan JR, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 2008, 20(2): 471-481.

[28] Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol, 2009, 19(5): 423-429.

[29] Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol, 2001, 127(3): 803-816.

[30] Wang WF, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell, 2008, 15(2): 220-235.

[31] Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T. A flagel-lin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 2007, 448(7152): 497-500.

[32] Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA, 2007, 104(29): 12217-12222.

[33] Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell, 2006, 124(4): 783-801.

[34] Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, Mengiste T. The mem-brane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell, 2006, 18(1): 257-273.

[35] Zhang J, Li W, Xiang TT, Liu ZX, Laluk K, Ding XJ, Zou Y, Gao MH, Zhang XJ, Chen S, Mengiste T, Zhang YL, Zhou JM. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe, 2010, 7(4): 290-301.

[36] Lu DP, Wu SJ, Gao XQ, Zhang YL, Shan LB, He P. A re-ceptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immu-nity. Proc Natl Acad Sci USA, 2010, 107(1): 496-501.

[37] MAPK Group, Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang SQ, Hirt H, Wil-son C, Heberle-Bors E, Ellis BE, Morris PC, Innes RW, Ecker JR, Scheel D, Klessig DF, Machida Y, Mundy J, Ohashi Y, Walker JC. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci, 2002, 7(7): 301-308.

[38] Pitzschke A, Schikora A, Hirt H. MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol, 2009, 12(4): 421-426.

[39] Gao MH, Liu JM, Bi DL, Zhang ZB, Cheng F, Chen SF, Zhang YL. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res, 2008, 18(12): 1190-1198.

[40] Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, MacKinlay J, Loake GJ, Mundy J, Morris PC. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol, 2008, 148(1): 212-222.

[41] Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu SJ, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjørn Nielsen H, Hirt H, Somssich I, Mattsson O, Mundy J. The MAP kinase sub-strate MKS1 is a regulator of plant defense responses. EMBO J, 2005, 24(14): 2579-2589.

[42] Brodersen P, Petersen M, Bjørn Nielsen H, Zhu SJ, New-man MA, Shokat KM, Rietz S, Parker J, Mundy J. Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J, 2006, 47(4): 532-546.

[43] Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sand-bech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J, 2008, 27(16): 2214-2221.

[44] Ichimura K, Casais C, Peck SC, Shinozaki K, Shirasu K. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J Biol Chem, 2006, 281(48): 36969-36976.

[45] Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 2002, 415(6875): 977-983.

[46] Pitzschke A, Schikora A, Hirt H. MAPK cascade signal-ling networks in plant defence. Curr Opin Plant Biol, 2009, 12(4): 421-426.

[47] Ren DT, Liu YD, Yang KY, Han L, Mao GH, Glazebrook J, Zhang SQ. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA, 2008, 105(14): 5638-5643.

[48] Mao GH, Meng XZ, Liu YD, Zheng ZY, Chen ZX, Zhang SQ. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin bio-synthesis in Arabidopsis. Plant Cell, 2011, Epub ahead of print.

[49] Citovsky V, Kapelnikov A, Oliel S, Zakai N, Rojas MR, Gilbertson RL, Tzfira T, Loyter A. Protein interactions involved in nuclear import of the Agrobacterium VirE2 protein in vivo and in vitro. J Biol Chem, 2004, 279(28): 29528-29533.

[50] Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H. Tro-jan horse strategy in Agrobacterium transforma-tion: abusing MAPK defense signaling. Science, 2007, 318(5849): 453-456.

[51] Schulze-Lefert P, Panstruga R. Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu Rev Phytopathol, 2003, 41: 641- 667.

[52] Badel JL, Charkowski AO, Deng WL, Collmer A. A gene in the Pseudomonas syringae pv. tomato Hrp pathogenicity island conserved effector locus, hopPtoA1, contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. Mol Plant-Microbe Interact, 2002, 15(10): 1014-1024.

[53] Lindgren RB. The role of hrp genes during plant-bacterial interactions. Annu Rev Phytopathol, 1997, 35: 129-152.

[54] Hauck P, Thilmony R, He SY. A Pseudomonas syrin-gae type III effector suppresses cell wall-based ex-tracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA, 2003, 100(14): 8577-8582.

[55] He P, Shan LB, Lin NC, Martin GB, Kemmerling B, Nürnberger T, Sheen J. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidop-sis innate immunity. Cell, 2006, 125(3): 563-575.

[56] Xiang TT, Zong N, Zou Y, Wu Y, Zhang J, Xing WM, Li Y, Tang XY, Zhu LH, Chai JJ, Zhou JM. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol, 2008, 18(1): 74-80.

[57] Shan LB, He P, Li JM, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe, 2008, 4(1): 17-27.

[58] Gohre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol, 2008, 18(23): 1824-1832.

[59] Li XY, Lin HQ, Zhang WG, Zou Y, Zhang J, Tang XY, Zhou JM. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA, 2005, 102(36): 12990-12995.

[60] Kang L, Li JX, Zhao TH, Xiao FM, Tang XY, Thilmony R, He Sy, Zhou JM. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA, 2003, 100(6): 3519-3524.

[61] Zhang J, Shao F, Li Y, Cui HT, Chen LJ, Li HT, Zou Y, Long CZ, Lan LF, Chai JJ, Chen S, Tang XY, Zhou JM. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe, 2007, 1(3): 175-185.

[62] Panstruga R, Dodds PN. Terrific protein traffic: the mys-tery of effector protein delivery by filamentous plant pathogens. Science, 2009, 324(5928): 748-750.

[63] Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PRJ. A translocation signal for delivery of oomycete ef-fector proteins into host plant cells. Nature, 2007, 450(7166): 115-118.

[64] Dou DL, Kale SD, Wang X, Jiang RHY, Bruce NA, Arre-dondo FD, Zhang XM, Tyler BM. RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell, 2008, 20(7): 1930-1947.

[65] Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 2006, 18(1): 243-256.

[66] Manning VA, Ciuffetti LM. Localization of Ptr ToxA pro-duced by Pyrenophora triticirepentis reveals protein import into wheat mesophyll cells. Plant Cell, 2005, 17(11): 3203-3212.

[67] Lukasik E, Takken FL. STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol, 2009, 12(4): 427-436.

[68] Dangl JL, Jones JDG. Plant pathogens and integrated defence responses to infection. Nature, 2001, 411(6839): 826-833.

[69] Elmore JM, Lin ZJD, Coaker G. Plant NB-LRR signaling: upstreams and downstreams. Curr Opin Plant Biol, 2011, 14(4): 365-371.

[70] Collier SM, Moffett P. NB-LRRs work a "bait and switch" on pathogens. Trends Plant Sci, 2009, 14(10): 521-529.

[71] Axtell MJ, Staskawicz BJ. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2- directed elimination of RIN4. Cell, 2003, 112(3): 369-377.

[72] Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D. The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to pro-mote Pseudomonas syringae virulence. Proc Natl Acad Sci USA, 2010, 107(5): 2349-2354.

[73] Mackey D, Holt BF III, Wiig A, Dangl JL. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell, 2002, 108(6): 743-754.

[74] Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G. RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during patho-gen attack. PLoS Biol, 2009, 7(6): e1000139.

[75] Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science, 2003, 301(5637): 1230-1233.

[76] Abramovitch RB, Martin GB. AvrPtoB: a bacterial type III effector that both elicits and suppresses programmed cell death associated with plant immunity. FEMS Microbiol Lett, 2005, 245(1): 1-8.

[77] Mucyn TS, Clemente A, Andriotis VME, Balmuth AL, Oldroyd GED, Staskawicz BJ, Rathjen JP. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell, 2006, 18(10): 2792-2806.

[78] Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y. Physical interaction between RRS1-R, a protein conferring resis-tance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA, 2003, 100(13): 8024-8029.

[79] Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, Ayliffe MA, Kobe B, Ellis JG. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA, 2006, 103(23): 8888-8893.

[80] Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ. The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol Plant-Microbe Inter-act, 2010, 23(1): 49-57.

[81] Jia YL, McAdams SA, Bryan GT, Hershey HP Valent B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J, 2000, 19(15): 4004-4014.

[82] Krasileva KV, Dahlbeck D, Staskawicz BJ. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell, 2010, 22(7): 2444-2458.

[83] Caplan J, Padmanabhan M, Dinesh-Kumar SP. Plant NB-LRR immune receptors: from recognition to tran-scriptional reprogramming. Cell Host Microbe, 2008, 3(3): 126-135.