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Front Biol    2012, Vol. 7 Issue (2) : 155-166    https://doi.org/10.1007/s11515-011-1185-8
REVIEW
Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity
Xin YANG1, Fengyang DENG1,2, Katrina M. RAMONELL1()
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
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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     
Corresponding Author(s): RAMONELL Katrina M.,Email:kramonel@bama.ua.edu   
Issue Date: 01 April 2012
 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]. Front Biol, 2012, 7(2): 155-166.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-011-1185-8
https://academic.hep.com.cn/fib/EN/Y2012/V7/I2/155
Name of RLK/RLPOrganismType of RLK/RLPResistantSusceptibleReferences
BIK1ArabidopsisRLCKB. cinereaA. brassicicolaPst DC3000Veronese et al., 2006
BIR1ArabidopsisLRR RLKH. parasitica Noco2Gao et al., 2009
SOBIR1ArabidopsisLRR RLKPst DC3000Gao et al.,2009
OSBRR1RiceLRR RLKM. oryzaePeng et al., 2009
BSR1ArabidopsisRLCKC. higginsianum Pst DC3000Dubouzet et al., 2011
CERK1/LysM RLK1ArabidopsisLysM RLKG. cichoracearumA. brassicicolaWan et al., 2008; Miya et al., 2007;
OsCERK1RiceLysM RLKShimizu et al., 2010
CEBiPRiceLysM RLPM. oryzaeKaku et al., 2006Kishimoto et al., 2010
HvCEBiPBarleyLysM RLPM. oryzaeTanaka et al., 2010
LeEix1 and 2TobaccoLRR RLPRon and Avni, 2004
CBRLK1ArabidopsisS-locus RLKPst DC3000Kim et al., 2009
EFRArabidopsisLRR RLKA. tumefaciensZipfel et al., 2006
ERECTAArabidopsisLRR RLKP. cucumerinaP. irregulareLlorente et al., 2005Adie et al., 2007
FLS2ArabidopsisLRR RLKPst DC3000Gómez-Gómez and Boller 2000;Zipfel et al., 2004
FERArabidopsisG. orontii Pst DC3000Kessler et al., 2010Keinath et al., 2010
NbLRK1N. benthamianaLectin-like RLKKanzaki et al., 2008
AtPepR1 and 2ArabidopsisLRR RLKYamaguchi et al., 2006; Krol et al.,2010
NgRLK1N. glutinosaB-lectin, S-locus glycoproteinKim et al., 2010
TaRLK-R1,2,and 3WheatWheat stripe rustZhou et al., 2007
AtRLP30ArabidopsisLRR RLPP. syringae pv phaseolicola 1448AWang et al., 2008
RIPKArabidopsisRLCKPst DC3000Liu et al., 2011
NbSERK3/BAK1N. benthamianaLRR RLKPta 11528 PtoDC3000PtoDC3000 hrcCP. infestansHeese et al., 2007 Chaparro-Garcia et al., 2011
SNC2ArabidopsisLRR RLPPst DC3000Zhang et al., 2010b
SNC3ArabidopsisLRR RLPZhang et al., 2010b
TARK1TomatoLRR RLKXanthomonas campestris pathovar vesicatoria (Xcv)Kim et al., 2009
TPK1bTomatoRLCKB. cinerea Tobacco hornworm (Manteca seta)AbuQamar et al.,2008
Ve1TomatoLRR RLPV. dahliaeV. albo-atrumFradin et al., 2009
Vfa4AppleLRR RLPV. inaequalisMalnoy et al., 2008
Vfa1 and Vfa2AppleLRR RLPV. inaequalisMalnoy et al., 2008; Belfanti et al., 2004
WAK1ArabidopsisEGF-like RLKB. cinereaDecreux and Messiaen 2005; Decreux et al., 2006
OsWAK1RiceEGF-like RLKM. oryzaeLi et al., 2009b
XA21RiceLRR RLKXanthomonas oryzae pv. oryzaeLee et al., 2009
Xa3/Xa26RiceRLKXanthomonas oryzae pv. oryzaeSun et al., 2004
Xa21DRiceRLPXanthomonas oryzae pv. oryzaeWang et al., 1998
Tab.1  RLKs and RLPs involved in plant innate immunity
Fig.1  Models of activation of the FLS2, EFR and CERK1 RLKs. (A) In the absence of flg22, BIK1 associates with FLS2. Step 1: Upon flg22 treatment, FLS2 interacts with BAK1 and BKK1 directly. Simultaneously both FLS2 and BAK1 are phosphorylated. Step 2: BIK1 is then phosphorylated rapidly and may then activate downstream disease resistance genes, thereby positively regulating PAMP signaling. Step 3: Phosphorylated BIK1 can also transphosphorylate FLS2 and BAK1. The fully activated FLS2/BAK1 complex may further phosphorylate BIK1 at alternate sites. These transphosphorylation and phosphorylation events may lead to the activation of ion channels and the NADPH oxidase complex. Step 4: After phosphorylation, BIK1 dissociates from FLS2. After activating the flagellin signaling pathway, FLS2 is internalized into the cytoplasm within 20–40 min. It is then ubiquitinated and degraded. (B) Like FLS2, the EFR can also interact with both BAK1 and BIK1, in fact FLS2 and EFR share a common signaling pathway. (C) The chitin receptor CERK1 is also capable of interacting with BIK1 but not with BAK1. All three PAMP receptors activate MAPK cascades.
Fig.2  XA21 and CEBiP/OsCERK1 complex activation. (A) XA21 is localized to both the endoplasmic reticulum (ER) and the plasma membrane (PM). The interaction between Xa21 and BiP3 in the ER may function in its proper folding. Interactions between XA21 and its binding proteins such as XB3, XB10, XB15, XB24 and their phosphorylation may activate defense pathways. In this signaling pathway OsWRKY62 acts as a negative regulator of XA21 mediated defenses. (B) The chitin signaling pathway in rice requires two RLKs: CEBiP and OsCERK1. In unstimulated plant cells, CEBiP and OsCERK1 exist separately from one another and CEBiP forms homooligomers. Once activated by chitin, a receptor complex that includes both CEBiP and OsCERK1 forms immediately and may result in the activation of downstream signaling pathways leading to ROS production and activation of MAPK cascades.
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: 10.1105/tpc.108.059477 pmid:18599583
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: 10.1105/tpc.106.048041 pmid:17513501
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: 10.1038/415977a pmid:11875555
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: 10.1111/j.1365-313X.2010.04282.x pmid:20561260
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: 10.1073/pnas.0304808101 pmid:14715897
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: 10.1104/pp.109.149930 pmid:19933383
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: 10.1073/pnas.1000675107 pmid:20439716
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: 10.1371/journal.pone.0016608 pmid:21304602
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: 10.1093/mp/ssq038 pmid:20616165
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: 10.1016/j.tplants.2009.08.002 pmid:19748302
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: 10.1038/nature05999 pmid:17625569
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: 10.1093/pcp/pci026 pmid:15769808
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: 10.1016/j.phytochem.2006.03.009 pmid:16631829
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: 10.1093/mp/ssn019 pmid:19825551
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: 10.1111/j.1467-7652.2010.00568.x pmid:20955180
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: 10.1104/pp.121.2.391 pmid:10517830
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: 10.1104/pp.109.136762 pmid:19321708
18 Fritz-Laylin L K, Krishnamurthy N, T?r M, Sj?lander K V, Jones J D (2005). Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol , 138(2): 611–623
doi: 10.1104/pp.104.054452 pmid:15955925
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: 10.1038/cr.2008.300 pmid:18982020
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: 10.1016/j.chom.2009.05.019 pmid:19616764
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: 10.1016/j.cub.2009.01.054 pmid:19249211
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: 10.1046/j.1365-313X.2003.01877.x pmid:14617092
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:10911994
24 Govers F, Angenent G C (2010). Plant science. Fertility goddesses as Trojan horses. Science , 330(6006): 922–923
doi: 10.1126/science.1198347 pmid:21071655
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: 10.1073/pnas.0705306104 pmid:17626179
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: 10.1073/pnas.0603727103
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: 10.1074/jbc.M605319200 pmid:17023433
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: 10.1074/jbc.M109.027540 pmid:19951949
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: 10.1111/j.1365-313X.2010.04155.x pmid:20113440
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: 10.1007/s00299-007-0494-5 pmid:18087702
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: 10.1073/pnas.0508882103 pmid:16829581
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: 10.1007/s00425-008-0797-y pmid:18682978
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: 10.1074/jbc.M110.160531 pmid:20843791
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: 10.1126/science.1195211 pmid:21071669
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: 10.1016/j.bbrc.2009.02.050 pmid:19222996
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: 10.1007/s11033-009-9570-y pmid:19449126
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: 10.1111/j.1365-313X.2010.04328.x pmid:21070413
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: 10.1074/jbc.M109.097394 pmid:20200150
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: 10.1038/nbt.1613 pmid:20231819
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: 10.1105/tpc.111.087122 pmid:21862710
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: 10.1105/tpc.111.089656 pmid:21949153
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: 10.1126/science.1173438 pmid:19892983
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: 10.1111/j.1467-7652.2009.00444.x pmid:19754838
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: 10.1007/s11103-008-9430-5 pmid:19039666
45 Li J, Chory J (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell , 90(5): 929–938
doi: 10.1016/S0092-8674(00)80357-8 pmid:9298904
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: 10.1016/j.chom.2011.01.010 pmid:21320696
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: 10.1016/S1673-8527(08)60153-8 pmid:19840759
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: 10.1111/j.1365-313X.2005.02440.x pmid:15998304
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: 10.1073/pnas.0909705107 pmid:20018686
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: 10.1094/MPMI-21-4-0448 pmid:18321190
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: 10.1073/pnas.0705147104 pmid:18042724
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: 10.1111/j.1365-313X.2007.03192.x pmid:17651370
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: 10.1371/journal.pbio.0060231 pmid:18817453
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: 10.1007/s00425-009-0951-1 pmid:19468748
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: 10.1093/mp/ssn024 pmid:19825552
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: 10.1074/jbc.M110.116657 pmid:20610395
57 Postel S, Kemmerling B (2009). Plant systems for recognition of pathogen-associated molecular patterns. Semin Cell Dev Biol , 20(9): 1025–1031
doi: 10.1016/j.semcdb.2009.06.002 pmid:19540353
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: 10.1111/j.1364-3703.2010.00704.x pmid:21726371
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: 10.1111/j.1432-1033.1989.tb21084.x pmid:2776750
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: 10.1101/gad.366506 pmid:16510871
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: 10.1105/tpc.022475 pmid:15155877
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: 10.1007/s001220050025
63 Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky F G, T?r 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: 10.1105/tpc.111.084301 pmid:21693696
64 Rowland O, Ludwig A A, Merrick C J, Baillieul F, Tracy F E, Durrant W E, Fritz-Laylin L, Nekrasov V, Sj?lander 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: 10.1105/tpc.104.026013 pmid:15598806
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: 10.1094/MPMI-22-8-0953 pmid:19589071
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: 10.1074/jbc.M109.096842 pmid:20103591
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: 10.1016/j.sbi.2004.07.007 pmid:15313242
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: 10.1016/j.chom.2008.05.017 pmid:18621007
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: 10.1111/j.1365-313X.2010.04324.x pmid:21070404
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: 10.1073/pnas.181141598 pmid:11526204
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: 10.1105/tpc.020834 pmid:15105442
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: 10.1046/j.1365-313X.2003.01976.x pmid:14756760
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: 10.1186/1471-2229-10-288 pmid:21190588
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: 10.1105/tpc.105.035576 pmid:16339855
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: 10.1093/mp/ssn047 pmid:19825577
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: 10.1105/tpc.107.056754 pmid:18263776
77 Wang G, Ellendorff U, Kemp B, Mansfield J W, Forsyth A, Mitchell K, Bastas K, Liu C M, Woods-T?r A, Zipfel C, de Wit P J, Jones J D, T?r 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: 10.1104/pp.108.119487 pmid:18434605
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:9596635
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: 10.1094/MPMI-9-0850 pmid:8969533
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: 10.1105/tpc.106.046730 pmid:17172358
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:12524365
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: 10.1111/j.1365-313X.2005.02638.x pmid:16460508
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: 10.1105/tpc.109.068874 pmid:20179141
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: 10.1073/pnas.0603729103 pmid:16785433
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: 10.1016/j.chom.2010.03.007 pmid:20413097
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: 10.1105/tpc.110.074120 pmid:20841424
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: 10.1111/j.1365-313X.2007.03246.x pmid:17764502
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: 10.1016/j.cell.2006.03.037 pmid:16713565
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: 10.1038/nature02485 pmid:15085136
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