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Receptor-mediated signalling in plants: molecular patterns and programmes

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Tör, Mahmut, Lotze, Michael T. and Holton, Nicholas. (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. Journal of Experimental Botany . ISSN 0022-0957

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Official URL: http://dx.doi.org/10.1093/jxb/erp233

Abstract

A highly evolved surveillance system in plants is able to detect a broad range of signals originating from pathogens, damaged tissues, or altered developmental processes, initiating sophisticated molecular mechanisms that result in defence, wound healing, and development. Microbe-associated molecular pattern molecules (MAMPs), damage-associated molecular pattern molecules (DAMPs), virulence factors, secreted proteins, and processed peptides can be recognized directly or indirectly by this surveillance system. Nucleotide binding-leucine rich repeat proteins (NB-LRR) are intracellular receptors and have been targeted by breeders for decades to elicit resistance to crop pathogens in the field. Receptor-like kinases (RLKs) or receptor like proteins (RLPs) are membrane bound signalling molecules with an extracellular receptor domain. They provide an early warning system for the presence of potential pathogens and activate protective immune signalling in plants. In addition, they act as a signal amplifier in the case of tissue damage, establishing symbiotic relationships and effecting developmental processes. The identification of several important ligands for the RLK-type receptors provided an opportunity to understand how plants differentiate, how they distinguish beneficial and detrimental stimuli, and how they co-ordinate the role of various types of receptors under varying environmental conditions. The diverse roles of extra-and intracellular plant receptors are examined here and the recent findings on how they promote defence and development is reviewed.

Item Type:	Journal Article
Subjects:	S Agriculture > SB Plant culture
Divisions:	Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Protein kinases, Immune response, Plant proteins, Plant immunology, Electrophysiology of plants
Journal or Publication Title:	Journal of Experimental Botany
Publisher:	Oxford University Press
ISSN:	0022-0957
Date:	23 July 2009
Identification Number:	10.1093/jxb/erp233
Status:	Peer Reviewed
Access rights to Published version:	Restricted or Subscription Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), National Institutes of Health (U.S.) (NIH)
Grant number:	BB/C509490/1 (BBSRC), BB/E02484X/1 (BBSRC), 1 PO1 CA 101944-04 (NIH)
References:	Albrecht C, Russinova E, Kemmerling B, Kwaaitaal M, de Vries, SC. 2008. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-dependent and -independent signaling pathways. Plant Physiol. 148: 611-9. Asselbergh B, De Vleesschauwer D, Höfte M. 2008. Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol Plant Microbe Interact. 21: 709-719. Becraft PW, Stinard PS, McCarty DR. 1996. CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273: 1406-1409. Beliën T, Van Campenhout S, Robben J, Volckaert G. 2006. Microbial endoxylanases: effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems? Mol Plant Microbe Interact 19: 1072-81. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105: 15629-15634. Clark SE, Williams RW, Meyerowitz EM. 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575-585. De Wit PJGM. 2007. How plants recognize pathogens and defend themselves. Cell Mol Life Sci. 64: 2726-2732. DeYoung BJ, Innes RW. 2006. Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol. 7: 1243-1249. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F. 2003. The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci U S A 100: 10124-8. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci U S A 103: 8888-8893. Eastabrook G, Hu Y, von Dadelszen P. 2008. The role of decidual natural killer cells in normal placentation and in the pathogenesis of preeclampsia. J Obstet Gynaecol Can. 30: 467-476. Ellendorff U, Zhang Z, and Thomma BPHJ. 2008. Gene silencing to investigate the roles of receptor-like proteins in Arabidopsis. Plant Signaling and Behaviour 3: 893-896. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB. 2002. A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966. Eyüboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer KF, Schneitz K. 2007. Molecular characterisation of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol. 7: 16. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911-1914. Friesen TL, Faris JD, Solomon PS, Oliver RP. 2008. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol. 10: 1421-8. Fritz-Laylin LK, Krishnamurthy N, Tör M, Sjölander KV, Jones JDG. 2005. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis reveals four major super-clades of resistance proteins and new candidate developmental genes. Plant Physiol. 138: 611-623. Gabriëls SH, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM, van den Berg GC, Rainey DY, Martin GB, Takken FL, de Wit PJ, Joosten MH. 2007. An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins. Plant J. 50: 14-28. Gaudriault S, Malandrin L, Paulin JP, Barny MA. 1997. DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol. 26:1057-1069. Gendron JM, Wang ZY. 2007. Multiple mechanisms modulate brassinosteroid signaling. Curr. Opin. Plant Biol. 10: 436-441. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J. 2007. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17: 1109-1115. He Z, Wang ZY, Li J, Zhu Q, Lamb C, Ronald P, Chory J. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288: 2360-2363. He ZH, Fujiki M, Kohorn BD. 1996. A cell wall-associated, receptor-like protein kinase. J Biol Chem 271: 19789-19793. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104: 12217-12222. Hervé C, Dabos P, Galaud JP, Rougé P, Lescure B. 1996. Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domain. J Mol Biol. 258: 778-788. Holton N, Caño-Delgado A, Harrison K, Montoya T, Chory J, Bishop GJ. 2007. Tomato BRASSINOSTEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling. Plant Cell 19: 1709-1717. Ingle RA, Carstens M, Denby KJ. 2006. PAMP recognition and the plant-pathogen arms race. Bioessays 28: 880-889. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J; 19: 4004-4014. Jeong S, Trotochaud AE, Clark SE. 1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11: 1925-1933. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444: 323-329. Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Ann Rev Phytopathol. 44: 41-60. Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S. 2006. The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18: 626-638. Karlova R, Boeren S, van Dongen W, Kwaaitaal M, Aker J, Vervoort J, de Vries S. 2008. Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 12: 24 Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A 98: 6511-6515. Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Müssig C, Thomma BP, Albrecht C, de Vries SC, Hirt H, Nürnberger T. 2007. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr. Biol. 17: 1116-1122. Kruijt M, Kip DJ, Joosten MH, Brandwagt BF, de Wit PJ. 2005. The Cf-4 and Cf-9 resistance genes against Cladosporium fulvum are conserved in wild tomato species. Mol Plant Microbe Interact 18: 1011-1021. Lee SW, Jeong KS, Han SW, Lee SE, Phee BK, Hahn TR, Ronald P. 2008. The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 190: 2183-2197. Li J, Chory J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938. Li Y, Yang S, Yang H, Hua J. 2007. The TIR-NB-LRR gene SNC1 is regulated at the transcript level by multiple factors. Mol Plant Microbe Interact. 20: 1449-1456. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, Devera ME, Liang X, Tör M, Billiar T. 2007. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev. 220: 60–81. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640. Marathe R, Dinesh-Kumar SP. 2003. Plant defense: one post, multiple guards? Mol Cell 11: 284-286. Matsubayashi Y, Sakagami Y. 1996. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci U S A 93: 7623-7627. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. 2002. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296: 1470-1472. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. Meng X, Bonasera JM, Kim JF, Nissinen RM, Beer SV. 2006. Apple proteins that interact with DspA/E, a pathogenicity effector of Erwinia amylovora, the fire blight pathogen. Mol. Plant Microbe Interact. 19: 53-61. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. 2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-34. Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S. 2008. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49 :1752-1757. Mudgett MB, Staskawicz BJ. 1998. Protein signaling via type III secretion pathways in phytopathogenic bacteria. Curr. Opin. Microbiol. 1: 109-114. Muller R, Bleckmann A, Simon R. 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20: 934-46. Morillo SA, Tax FE. 2006. Functional analysis of receptor-like kinases in monocots and dicots. Curr. Opin. Plant Biol. 9: 460-469. Nadeau JA, Sack FD. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296: 1697-700. Nagamune K, Hicks LM, Fux B, Brossier F, Chini EN, Sibley LD. 2008. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451: 207-210. Naito K, Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2008. Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact. 21: 1165-1174. Nam KH, Li J. 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110: 203-212. Narusaka Y, Kawakami N, Kaku H, Shibuya N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104: 19613-19618. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M. 2002. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420: 426-429. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K. 2005. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17: 1105-1119. Park CJ, Peng Y, Chen X, Dardick C, Ruan D, Bart R, Canlas PE, Ronald PC. 2008. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol. 6: e231 Pearce G, Strydom D, Johnson S, Ryan CA. 1991. A Polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895-897. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585-592. Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S. 2005. Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol. 138: 1027-1036. Robatzek S, Chinchilla D, Boller T. 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20: 537-542. Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16: 3216-3229. Ryan CA, Huffaker A, Yamaguchi Y. 2007. New insights into innate immunity in Arabidopsis. Cell Microbiol. 9: 1902-1908. Sanabria N, Goring D, Nürnberger T, Dubery I. 2008. Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity. New Phytol. 178: 503-514. Schaller A, Ryan CA. 1994. Identification of a 50-kDa systemin-binding protein in tomato plasma membranes having Kex2p-like properties. Proc Natl Acad Sci U S A 91: 11802-11806. Scheer JM, Ryan CA Jr. 2002. The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci U S A 99: 9585-9590. Seong SY, Matzinger P. 2004. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol. 6: 469-478. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RA. 2008. Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20: 1169-1183. Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4: 17-27. Shen QH, Schulze-Lefert P. 2007. Rumble in the nuclear jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J. 26: 4293-4301. Shiba H, Takayama S, Iwano M, Shimosato H, Funato M, Nakagawa T. 2001. A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125: 2095-2103. Shiu SH, Bleecker AB. 2003a. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132: 530-543 Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. 2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16: 1220-34. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. 2005. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309: 290-293. Sinapidou E, Williams K, Nott L, Bahkt S, Tör M, Crute I, Bittner-Eddy P, Beynon J. 2004. Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 38: 898-909. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB. 1991. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A 88: 8816-8820. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA. 2008. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20: 1805-1817 Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF. 2006. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18: 764-779. Sweat TA, Lorang JM, Bakker EG, Wolpert TJ. 2008. Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis. Mol Plant Microbe Interact. 21: 7-19. Swiderski MR, Innes RW. 2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26: 101-112. Tellström V, Usadel B, Thimm O, Stitt M, Küster H, Niehaus K. 2007. T
URI:	http://wrap.warwick.ac.uk/id/eprint/1270