Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity

Abstract

Plants have evolved multiple layers of defense against various pathogens in the environment. Receptor-like kinases/proteins (RLKs/RLPs) are on the front lines of the battle between plants and pathogens since they are present at the plasma membrane and perceive signature molecules from either the invading pathogen or damaged plant tissue. With a few notable exceptions, most RLKs/RLPs are positive regulators of plant innate immunity. In this review, we summarize recently discovered RLKs/RLPs that are involved in plant defense responses against various classes of pathogens. We also describe what is currently known about the mechanisms of RLK-mediated initiation of signaling via protein-protein interactions and phosphorylation.

Keywords

receptor-like kinases (RLKs) / receptor-like proteins (RLPs) / biotrophic fungi / necrotrophic fungi / bacterial pathogens

References

[1] AbuQamar S, Chai M F, Luo H, Song F, Mengiste T (2008). Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell, 20(7): 1964–1983

[2] Adie B A, Pérez-Pérez J, Pérez-Pérez M M, Godoy M, Sánchez-Serrano J J, Schmelz E A, Solano R (2007). ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell, 19(5): 1665–1681

[3] Asai T, Tena G, Plotnikova J, Willmann M R, Chiu W L, Gomez-Gomez L, Boller T, Ausubel F M, Sheen J (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415(6875): 977–983

[4] Bar M, Sharfman M, Ron M, Avni A (2010). BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J, 63(5): 791–800

[5] Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J, Vinatzer B A, Gianfranceschi L, Gessler C, Sansavini S (2004). The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA, 101(3): 886–890

[6] Bleckmann A, Weidtkamp-Peters S, Seidel C A, Simon R (2010). Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol, 152(1): 166–176

[7] 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(20): 9452–9457

[8] Chaparro-Garcia A, Wilkinson R C, Gimenez-Ibanez S, Findlay K, Coffey M D, Zipfel C, Rathjen J P, Kamoun S, Schornack S (2011). The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen phytophthora infestans in Nicotiana benthamiana. PLoS ONE, 6(1): e16608

[9] Chen F, Gao M J, Miao Y S, Yuan Y X, Wang M Y, Li Q, Mao B Z, Jiang L W, He Z H (2010). Plasma membrane localization and potential endocytosis of constitutively expressed XA21 proteins in transgenic rice. Mol Plant, 3(5): 917–926

[10] Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009). One for all: the receptor-associated kinase BAK1. Trends Plant Sci, 14(10): 535–541

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

[12] Decreux A, Messiaen J (2005). Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol, 46(2): 268–278

[13] Decreux A, Thomas A, Spies B, Brasseur R, Van Cutsem P, Messiaen J (2006). In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry, 67(11): 1068–1079

[14] Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel F M, Dewdney J (2008). Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant, 1(3): 423–445

[15] Dubouzet J G, Maeda S, Sugano S, Ohtake M, Hayashi N, Ichikawa T, Kondou Y, Kuroda H, Horii Y, Matsui M, Oda K, Hirochika H, Takatsuji H, Mori M (2011). Screening for resistance against Pseudomonas syringae in rice-FOX Arabidopsis lines identified a putative receptor-like cytoplasmic kinase gene that confers resistance to major bacterial and fungal pathogens in Arabidopsis and rice. Plant Biotechnol J, 9(4): 466–485

[16] Enkerli J, Felix G, Boller T (1999). The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol, 121(2): 391–398

[17] Fradin E F, Zhang Z, Juarez Ayala J C, Castroverde C D, Nazar R N, Robb J, Liu C M, Thomma B P (2009). Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol, 150(1): 320–332

[18] Fritz-Laylin L K, Krishnamurthy N, Tör M, Sjölander K V, Jones J D (2005). Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol, 138(2): 611–623

[19] Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008). MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res, 18(12): 1190–1198

[20] Gao M, Wang X, Wang D, Xu F, Ding X, Zhang Z, Bi D, Cheng Y T, Chen S, Li X, Zhang Y (2009). Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe, 6(1): 34–44

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

[22] Godiard L, Sauviac L, Torii K U, Grenon O, Mangin B, Grimsley N H, Marco Y (2003). ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J, 36(3): 353–365

[23] Gómez-Gómez L, Boller T (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell, 5(6): 1003–1011

[24] Govers F, Angenent G C (2010). Plant science. Fertility goddesses as Trojan horses. Science, 330(6006): 922–923

[25] Heese A, Hann D R, Gimenez-Ibanez S, Jones A M, He K, Li J, Schroeder J I, Peck S C, Rathjen J P (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA, 104(29): 12217–12222

[26] Huffaker A, Pearce G, & Ryan, C. A. (2006). An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA, 103(26): 10098–10103

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

[28] Iizasa E, Mitsutomi M, Nagano Y (2010). Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem, 285(5): 2996–3004

[29] Jeworutzki E, Roelfsema M R, Anschütz U, Krol E, Elzenga J T, Felix G, Boller T, Hedrich R, Becker D (2010). Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels. Plant J, 62(3): 367–378

[30] Jurca M E, Bottka S, Fehér A (2008). Characterization of a family of Arabidopsis receptor-like cytoplasmic kinases (RLCK class VI). Plant Cell Rep, 27(4): 739–748

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

[32] Kanzaki H, Saitoh H, Takahashi Y, Berberich T, Ito A, Kamoun S, Terauchi R (2008). NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta, 228(6): 977–987

[33] Keinath N F, Kierszniowska S, Lorek J, Bourdais G, Kessler S A, Shimosato-Asano H, Grossniklaus U, Schulze W X, Robatzek S, Panstruga R (2010). PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem, 285(50): 39140–39149

[34] Kessler S A, Shimosato-Asano H, Keinath N F, Wuest S E, Ingram G, Panstruga R, Grossniklaus U (2010). Conserved molecular components for pollen tube reception and fungal invasion. Science, 330(6006): 968–971

[35] Kim H S, Jung M S, Lee S M, Kim K E, Byun H, Choi M S, Park H C, Cho M J, Chung W S (2009). An S-locus receptor-like kinase plays a role as a negative regulator in plant defense responses. Biochem Biophys Res Commun, 381(3): 424–428

[36] Kim Y T, Oh J, Kim K H, Uhm J Y, Lee B M (2010). Isolation and characterization of NgRLK1, a receptor-like kinase of Nicotiana glutinosa that interacts with the elicitin of Phytophthora capsici. Mol Biol Rep, 37(2): 717–727

[37] Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y (2010). Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J, 64(2): 343–354

[38] Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel S, Arents M, Jeworutzki E, Al-Rasheid K A, Becker D, Hedrich R (2010). Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem, 285(18): 13471–13479

[39] Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse H P, Smoker M, Rallapalli G, Thomma B P, Staskawicz B, Jones J D, Zipfel C (2010). Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol, 28(4): 365–369

[40] 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(8): 2831–2849

[41] Lee H Y, Bowen C H, Popescu G V, Kang H G, Kato N, Ma S, Dinesh-Kumar S, Snyder M, Popescu S C (2011). Arabidopsis RTNLB1 and RTNLB2 reticulon-like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell, 23(9): 3374–3391

[42] Lee S W, Han S W, Sririyanum M, Park C J, Seo Y S, Ronald P C (2009). A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science, 326(5954): 850–853

[43] Li D, Wang L, Wang M, Xu Y Y, Luo W, Liu Y J, Xu Z H, Li J, Chong K (2009a). Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnol J, 7(8): 791–806

[44] Li H, Zhou S Y, Zhao W S, Su S C, Peng Y L (2009b). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol, 69(3): 337–346

[45] Li J, Chory J (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell, 90(5): 929–938

[46] Liu J, Elmore J M, Lin Z J, Coaker G (2011). A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe, 9(2): 137–146

[47] Liu P, Wei W, Ouyang S, Zhang J S, Chen S Y, Zhang W K (2009). Analysis of expressed receptor-like kinases (RLKs) in soybean. J Genet Genomics, 36(10): 611–619

[48] Llorente F, Alonso-Blanco C, Sánchez-Rodriguez C, Jorda L, Molina A (2005). ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J, 43(2): 165–180

[49] 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(1): 496–501

[50] Malnoy M, Xu M, Borejsza-Wysocka E, Korban S S, Aldwinckle H S (2008). Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol Plant Microbe Interact, 21(4): 448–458

[51] Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, 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 USA, 104(49): 19613–19618

[52] Nühse T S, Bottrill A R, Jones A M, Peck S C (2007). Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J, 51(5): 931–940

[53] Park C J, Peng Y, Chen X, Dardick C, Ruan D, Bart R, Canlas P E, Ronald P C (2008). Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol, 6(9): e231

[54] Peng H, Zhang Q, Li Y, Lei C, Zhai Y, Sun X, Sun D, Sun Y, Lu T (2009). A putative leucine-rich repeat receptor kinase, OsBRR1, is involved in rice blast resistance. Planta, 230(2): 377–385

[55] Peng Y, Bartley L E, Chen X, Dardick C, Chern M, Ruan R, Canlas P E, Ronald P C (2008). OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant, 1(3): 446–458

[56] Petutschnig E K, Jones A M, Serazetdinova L, Lipka U, Lipka V (2010). The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem, 285(37): 28902–28911

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

[58] Qi Y, Tsuda K, Glazebrook J, Katagiri F (2011). Physical association of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) immune receptors in Arabidopsis. Mol Plant Pathol, 12(7): 702–708

[59] Ricci P, Bonnet P, Huet J C, Sallantin M, Beauvais-Cante F, Bruneteau M, Billard V, Michel G, Pernollet J C (1989). Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur J Biochem, 183(3): 555–563

[60] Robatzek S, Chinchilla D, Boller T (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev, 20(5): 537–542

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

[62] Ron M, Kantety R, Martin G B, Avidan N, Eshed Y, Zamir D, Avni A (2000). High-resolution linkage analysis and physical characterization of the EIX-responding locus in tomato. Theor Appl Genet, 100(2): 184–189

[63] Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky F G, Tör M, de Vries S, Zipfel C (2011). The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to Hemibiotrophic and Biotrophic pathogens. Plant Cell, 23(6): 2440–2455

[64] Rowland O, Ludwig A A, Merrick C J, Baillieul F, Tracy F E, Durrant W E, Fritz-Laylin L, Nekrasov V, Sjölander K, Yoshioka H, Jones J D (2005). Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell, 17(1): 295–310

[65] Sánchez-Rodríguez C, Estévez J M, Llorente F, Hernández-Blanco C, Jordá L, Pagán I, Berrocal M, Marco Y, Somerville S, Molina A (2009). The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol Plant Microbe Interact, 22(8): 953–963

[66] Schulze B, Mentzel T, Jehle A K, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010). Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem, 285(13): 9444–9451

[67] Senes A, Engel D E, DeGrado W F (2004). Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol, 14(4): 465–479

[68] Shan L, He P, Li J, Heese A, Peck S C, Nürnberger T, Martin G B, 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(1): 17–27

[69] Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010). Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J, 64(2): 204–214

[70] Shiu S H, Bleecker A B (2001). Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA, 98(19): 10763–10768

[71] Shiu S H, Karlowski W M, Pan R, Tzeng Y H, Mayer K F, Li W H (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell, 16(5): 1220–1234

[72] Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004). Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J, 37(4): 517–527

[73] Tanaka S, Ichikawa A, Yamada K, Tsuji G, Nishiuchi T, Mori M, Koga H, Nishizawa Y, O’Connell R, Kubo Y (2010). HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol, 10(1): 288

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

[75] Vij S, Giri J, Dansana P K, Kapoor S, Tyagi A K (2008). The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant, 1(5): 732–750

[76] Wan J, Zhang X C, Neece D, Ramonell K M, Clough S, Kim S Y, Stacey M G, Stacey G (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 20(2): 471–481

[77] Wang G, Ellendorff U, Kemp B, Mansfield J W, Forsyth A, Mitchell K, Bastas K, Liu C M, Woods-Tör A, Zipfel C, de Wit P J, Jones J D, Tör M, Thomma B P (2008). A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol, 147(2): 503–517

[78] Wang G L, Ruan D L, Song W Y, Sideris S, Chen L, Pi L Y, Zhang S, Zhang Z, Fauquet C, Gaut B S, Whalen M C, Ronald P C (1998). Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell, 10(5): 765–779

[79] Wang G L, Song W Y, Ruan D L, Sideris S, Ronald P C (1996). The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Mol Plant Microbe Interact, 9(9): 850–855

[80] Wang Y S, Pi L Y, Chen X, Chakrabarty P K, Jiang J, De Leon A L, Liu G Z, Li L, Benny U, Oard J, Ronald P C, Song W Y (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell, 18(12): 3635–3646

[81] Xu M, Korban S S (2002). A cluster of four receptor-like genes resides in the Vf locus that confers resistance to apple scab disease. Genetics, 162(4): 1995–2006

[82] Xu W H, Wang Y S, Liu G Z, Chen X, Tinjuangjun P, Pi L Y, Song W Y (2006). The autophosphorylated Ser686, Thr688, and Ser689 residues in the intracellular juxtamembrane domain of XA21 are implicated in stability control of rice receptor-like kinase. Plant J, 45(5): 740–751

[83] Yamaguchi Y, Huffaker A, Bryan A C, Tax F E, Ryan C A (2010). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell, 22(2): 508–522

[84] Yamaguchi Y, Pearce G, Ryan C A (2006). The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA, 103(26): 10104–10109

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

[86] Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X, Zhang Y (2010b). Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell, 22(9): 3153–3163

[87] Zhou H, Li S, Deng Z, Wang X, Chen T, Zhang J, Chen S, Ling H, Zhang A, Wang D, Zhang X (2007). Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J, 52(3): 420–434

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

[89] Zipfel C, Robatzek S, Navarro L, Oakeley E J, Jones J D, Felix G, Boller T (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428(6984): 764–767

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag Berlin Heidelberg