Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity
Xin YANG, Fengyang DENG, Katrina M. RAMONELL
Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity
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.
receptor-like kinases (RLKs) / receptor-like proteins (RLPs) / biotrophic fungi / necrotrophic fungi / bacterial pathogens
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
Pubmed
|
[24] |
Govers F, Angenent G C (2010). Plant science. Fertility goddesses as Trojan horses. Science, 330(6006): 922–923
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[45] |
Li J, Chory J (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell, 90(5): 929–938
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[57] |
Postel S, Kemmerling B (2009). Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol, 20(9): 1025–1031
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
Pubmed
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
Pubmed
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |