REVIEW

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

  • Xin YANG 1 ,
  • Fengyang DENG 1,2 ,
  • Katrina M. RAMONELL , 1
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  • 1. Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA
  • 2. College of Life Sciences, Northwest A&F University, Yangling, Shaanxi, 712100, China

Received date: 13 Sep 2011

Accepted date: 01 Nov 2011

Published date: 01 Apr 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

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[J]. Frontiers in Biology, 2012 , 7(2) : 155 -166 . DOI: 10.1007/s11515-011-1185-8

Acknowledgments

We thank the members of the Ramonell laboratory for helpful discussions and review of the manuscript. This work was supported by the University of Alabama and by a grant from the US Department of Agriculture (Grant no. 2007-01652 to K. M. R.).
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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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