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Acta Agron Sin ›› 2011, Vol. 37 ›› Issue (06): 935-942.doi: 10.3724/SP.J.1006.2011.00935

• REVIEW •     Next Articles

Recent Findings in Plant Innate Immunity and Possible Impacts on Crop Disease-resistance Breeding

ZHAO Kai-Jun1,2,*,LI Yan-Qiang1,3,WANG Chun-Lian1,2,GAO Ying1,2   

  1. 1 Key Laboratory of Crop Genetics and Breeding, Ministry of Agriculture / Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; 2 National Key Facility for Crop Gene Resources and Genetic Improvement, Beijing 100081, China; ?3 Graduate School of the Chinese Academy of Agricultural Sciences, Beijing 100081, China
  • Received:2010-12-06 Revised:2011-03-06 Online:2011-06-12 Published:2011-04-12

Abstract: Plants have been successfully living in such an environment in which there are myriads of potential microbial pathogens, indicating that plants possess an efficient immunity system. Recent studies have revealed that the plant immunity system consists of two layers of defense. The first layer, based on the sensitive perception of pathogen-associated molecular patterns (PAMPs) through pattern recognition receptors (PRRs) at the plant cell surface, is named as PAMP-triggered immunity (PTI). The second is called effector-triggered immunity (ETI), in which plants use additional receptors (such as R-gene products) to perceive pathogen virulence effectors that have evolved to suppress PTI. The conventional gene-for-gene resistance in plants belongs actually to ETI. For millions of years, natural selection has been driving pathogens to avoid ETI either by diversifying the recognized effectors or by acquiring additional effectors that suppress ETI. On the other hand, natural selection favors plant new R-genes that can recognize the newly acquired effectors in pathogen, resulting in new ETI to be triggered again. The latest studies have revealed the simple cipher that governs DNA recognition by TAL (transcription activator-like) effectors from plant pathogenic Xanthomonas. TAL effectors can specifically bind the target DNA of host plant with a novel protein-DNA binding pattern in which two amino acids recognize one nucleotide. Using this recognition code, TAL effectors can bind the promoter of target genes and induce the host diseases or resistance responses. Recent findings about plant innate immunity are reviewed in this paper and their possible applications in plant breeding for disease resistance are discussed.

Key words: Plant innate immunity, TAL-effectors, Plant-pathogen interaction, Recognition code, Plant breeding for disease resistance

[1]Bill B. A Short History of Nearly Everything. New York: Broadway Books, 2003. pp 188-202
[2]Butterfield N J. “Probable proterozoic fungi”. Paleobiology, 2005, 31: 165-182
[3]Takken F L W, Tameling W I L. To nibble at plant resistance proteins. Science, 2009, 324: 744-745
[4]Boller T, He S Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324: 742-744
[5]Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U. Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 2009, 326: 1509-1512
[6]Moscou M J, Bogdanove A J. A simple cipher governs DNA recognition by TAL effectors. Science, 2009, 326: 1501
[7]Jones J D G, Dangl J L. The plant immune system. Nature, 2006, 444: 323-329
[8]Dangl J L, Jones J D G. Plant pathogens and integrated defense responses to infection. Nature, 2001, 411: 826-833
[9]Ausubel F M. Are innate immune signaling pathways in plants and animals conserved? Nat Immunol, 2005, 6: 973-979
[10]Chisholm S T, Coaker G, Day B, Staskawicz B J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 2006, 124: 803-814
[11]Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol, 2009, 60: 379-406
[12]Navarro L, Jay F, Nomura K, He S Y, Voinnet O. Suppression of the MicroRNA pathway by bacterial effector proteins. Science, 2008, 321: 964-967
[13]Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, Torres M, Mansfield J W, Robatzek S. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol, 2008, 23: 1824-1832
[14]Zipfel C, Robatzek S, Navarro L, Oakeley E J, Jones J D, Felix G, Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 2004, 428: 764-767
[15]Gómez-Gómez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell, 2000, 5: 1003-1011
[16]Sun W, Dunning F M, Pfund C, Weingarten R, Bent A F. Within-species flagellin polymorphism in Xanthomonas campestris pv. campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell, 2006, 18: 764-779
[17]Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G, Shiu S H, 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: 539-547
[18]Takai R, Isogai A, Seiji S, Che F S. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol Plant-Microbe Interact, 2008, 12: 1635-1642
[19]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: 3496-3507
[20]Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones J D G. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium- mediated transformation. Cell, 2006, 125: 749-760
[21]Lee S W, Han S W, Sririyanum M, Park C J, Seo Y S, Ronald P C. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science, 2009, 326: 850-853
[22]Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA, 2006, 103: 11086-11091
[23]Shimizu T, Nakano T, Akamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N. Two LysM receptor molecules, EBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J, 2010, 64: 204-214
[24]Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA, 2007, 104: 19613-19618
[25]Chen L, Hamada S, Fujiwara M, Zhu T, Thao N P, Wong H L, Krishna P, Ueda T, Kaku H, Shibuya N, Kawasaki T, Shimamoto K. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host & Microbe, 2010, 7: 185-196
[26]Felix G, Boller T. Molecular sensing of bacteria in plants-the highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem, 2003, 278: 6201-6218
[27]Watt S A, Tellstrom V, Patschkowski T, Niehaus K. Identification of the bacterial superoxide dismutase (SodM) as plant-inducible elicitor of an oxidative burst reaction in tobacco cell suspension cultures. J Biotechnol, 2006, 126: 78-86
[28]Kim J G, Jeon E, Oh J, Moon J S, Hwang I. Mutational analysis of Xanthomonas harpin HpaG identifies a key functional region that elicits the hypersensitive response in nonhost plants. J Bacteriol, 2004, 186: 6239-6247
[29]Brunner F, Rosahl S, Lee J, Rudd J J, Geiler C, Kauppinen S. Pep-13, a plant defense-inducing pathogenassociated pattern from Phytophthora transglutaminases. EMBO J, 2002, 21: 6681-6688
[30]Boller T. Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol, 1995, 46: 189-214
[31]Granado J, Felix G, Boller T. Perception of fungal sterols in plants (subnanomolar concentrations of ergosterol elicit extracellular alkalinization in tomato cells. Plant Physiol, 1995, 107: 485-490
[32]Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, Flagiello A, Pucci P, Lanzetta R, Parrilli M, Molinaro A, Newman M A, Cooper R M. Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem & Biol, 2008, 15: 438-448
[33]Silipo A, Sturiale L, Garozzo D, Erbs G, Jensen T T, Lanzetta R, Dow J M, Parrilli M, Newman M A, Molinaro A. The acylation and phosphorylation pattern of lipid from Xanthomonas campestris strongly influence its ability to trigger the innate immune response in Arabidopsis. Chem Biol Chem, 2008, 9: 896-904
[34]Dulla G, Lindow S E. Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface. Proc Natl Acad Sci USA, 2008, 105: 3082-3087
[35]Johnson L. Iron and siderophores in fungal-host interactions. Mycol Res, 2008, 112: 170-183
[36]Abramovitch R B, Anderson J C, Martin G B. Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol, 2006, 7: 601-611
[37]Ellis J G, Dodds P N, Lawrence G J. Flax rust resistance gene specificity is based on direct resistance avirulence protein interactions. Annu Rev Phytopathol, 2007, 45: 289-306
[38]Kamoun S. Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol, 2007, 10: 358-365
[39]Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou J M. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol, 2008, 18: 74-80
[40]Shan L, He P, Li J, Heese A, Peck S C, Nürnberger T, Martin G B, 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: 17-27
[41]Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 2007, 448: 497-500
[42]Heese A, Hann D R, Gimenez-Ibanez S, Jones A M E, He K, Li J, Schroeder J I, Peck S C, Rathjen J P. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA, 2002, 104: 12217-12222
[43]Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou J M. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host & Microbe, 2007, 1: 175-185
[44]Block A, Li G Y, Fu Z Q, Alfano J R. Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol, 2008, 11: 396-403
[45]Wang Y, Li J, Hou S, Wang X, Li Y, Ren D, Chen S, Tang X, Zhou J. A Pseudomonas syringae ADP-Ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell, 2010, 22: 2033-2044
[46]Melotto M, Underwood W, Koczan J, Nomura K, He S Y. Plant stomata function in innate immunity against bacterial invasion. Cell, 2006, 126: 969-980
[47]Groll M, Schellenberg B, Bachmann A S, Archer C R, Huber R, Powell T K, Lindow S, Kaiser M, Dudler R. A plant pathogen virulence factor inhibits the eukaryotic proteasome by a novel mechanism. Nature, 2008, 452: 755-758
[48]Aslam S N, Newman M A, Erbs G, Morrissey K L, Chinchilla D, Boller T, Jensen T T, De Castro C, Ierano T, Molinaro A, Jackson R W, Knight M R, Cooper R M. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol, 2008, 18: 1078-1183
[49]Meyers B C, Kozik A, Griego A, Kuang H H, Michelmore R W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell, 2003, 15: 809-834
[50]Caplan J, Padmanabhan M, Dinesh-Kumar S P. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host & Microbe, 2008, 3: 126-135
[51]Lotze M T, Zeh H J, Rubartelli A, Sparvero L J, Amoscato A A, Washburn N R, Devera M E, Liang X, Tör M, Billiar T. The grateful dead: damage associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunologcal Rev, 2007, 220: 60-81
[52]Kay S, Bonas U. How Xanthomonas type III effectors manipulate the host plant. Curr Opin Microbiol, 2009, 12: 37-43
[53]White F F, Yang B. Host and pathogen factors controlling the Rice-Xanthomonas oryzae interaction. Plant Physiol, 2009, 150: 1677-1686
[54]Kay S, Hahn S, Marois E, Hause G, Bonas U. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science, 2007, 318: 648-651
[55]Römer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science, 2007, 318: 645-648
[56]Sugio A, Yang B, Zhu T, White F F. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAγ1 and OsTFX1 during bacterial blight of rice. Proc Natl Acad Sci USA, 2007, 104: 10720-10725
[57]Yang B, Sugio A, White F F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Nat Acad Sci USA, 2006, 103: 10503-10508
[58]Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang G L, White F F, Yin Z. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature, 2005, 435: 1122-1125
[59]Schornack S, Meyer A, Römer P, Jordan T, Lahaye T. Gene-for-gene-mediated recognition of nuclear-targeted AvrBs3-like bacterial effector proteins. J Plant Physiol, 2006, 163: 256-272
[60]Van den Ackerveken G, Marois E, Bonas U. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell, 1996, 87: 1307-1316
[61]Conrads-Strauch J H K, Bonas U. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature, 1992, 356: 172-174
[62]Yang B, Sugio A, White F F. Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact, 2005, 18: 142-149
[63]Bonas U, Stall R E, Staskawicz B. Genetic and Structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet, 1989, 218: 127-136
[64]Li T, Huang S, Jiang W Z, Wright D, Spalding M H, Weeks D P, Yang B. TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucl Acids Res, 2011, 39: 359-372
[65]Christian M, Cermak T, Doyle E L, Schmidt C, Zhang F, Hummel A, Bogdanove A J, Voytas D F. TAL effector nucleases create targeted DNA double-strand breaks. Genetics, 2010, 186: 757-761
[66]Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse H P, Smoker M, Rallapalli G, Thomma B, Staskawicz B, Jones J, Zipfel C. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol, 2010, 28: 365-369
[67]Römer P, Recht S, Lahaye T. A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci USA, 2009, 106: 20526-20531
[68]Zou L-F(邹丽芳), Chen G-Y(陈功友), Wu X-M(武晓敏), Wang J-S(王金生). Cloning and analysis of diverse members of avrBs3/PthA Family of Xanthomonas oryzae pv. oryzicola. Sci Agric Sin (中国农业科学), 2005, 38(5): 929-935 (in Chinese with English abstract)
[69]Zhao B, Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S. A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA, 2005, 102: 15383-15388
[70]Tian D, Yin Z. Constitutive heterologous expression of avrXa27 in rice containing the R gene Xa27 confers enhanced resistance to compatible Xanthomonas oryzae strains. Mol Plant Pathol, 2009, 10: 29-39
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