1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 69, 2018
  5. Article

Annual Review of Plant Biology

Volume 69, 2018

Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling

Abstract

Receptor kinases (RKs) are of paramount importance in transmembrane signaling that governs plant reproduction, growth, development, and adaptation to diverse environmental conditions. Receptor-like cytoplasmic kinases (RLCKs), which lack extracellular ligand-binding domains, have emerged as a major class of signaling proteins that regulate plant cellular activities in response to biotic/abiotic stresses and endogenous extracellular signaling molecules. By associating with immune RKs, RLCKs regulate multiple downstream signaling nodes to orchestrate a complex array of defense responses against microbial pathogens. RLCKs also associate with RKs that perceive brassinosteroids and signaling peptides to coordinate growth, pollen tube guidance, embryonic and stomatal patterning, floral organ abscission, and abiotic stress responses. The activity and stability of RLCKs are dynamically regulated not only by RKs but also by other RLCK-associated proteins. Analyses of RLCK-associated components and substrates have suggested phosphorylation relays as a major mechanism underlying RK-mediated signaling.

Keyword(s): abiotic stresses, development, growth, MAP kinases, mitogen-activated protein kinases, plant immunity, reactive oxygen species, receptor-like cytoplasmic kinases, ROS
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040540
2018-04-29
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/arplant/69/1/annurev-arplant-042817-040540.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040540&mimeType=html&fmt=ahah

Literature Cited

  1. Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB. 1.  2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22:60–69 [Google Scholar]
  2. Abuqamar S, Chai MF, Luo H, Song F, Mengiste T. 2.  2008. Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 20:1964–83 [Google Scholar]
  3. Ade J, DeYoung BJ, Golstein C, Innes RW. 3.  2007. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. PNAS 104:2531–36 [Google Scholar]
  4. Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I. 4.  et al. 2013. Hydrogen peroxide-regulated genes in the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 198:179–89 [Google Scholar]
  5. Anthony RG, Khan S, Costa J, Pais MS, Bogre L. 5.  2006. The Arabidopsis protein kinase PTI1–2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J. Biol. Chem. 281:37536–46 [Google Scholar]
  6. Ao Y, Li Z, Feng D, Xiong F, Liu J. 6.  et al. 2014. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J 80:1072–84 [Google Scholar]
  7. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E. 7.  et al. 1997. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. J. Biol. Chem. 272:217–21 [Google Scholar]
  8. Baudin M, Hassan JA, Schreiber K, Lewis JD. 8.  2017. Analysis of the ZAR1 immune complex reveals determinants for immunity and molecular interactions. Plant Physiol 174:2038–53 [Google Scholar]
  9. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. 9.  2009. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–88Shows that the RLCK SSP functions upstream of YDA to regulate asymmetric division during embryo and stomata development. [Google Scholar]
  10. Bergmann DC, Lukowitz W, Somerville C. 10.  2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–97 [Google Scholar]
  11. Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U. 11.  2015. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. PNAS 112:12211–16Demonstrates that an RLCK acts downstream of RKs to control pollen tube and root hair growth. [Google Scholar]
  12. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U. 12.  2013. ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLOS Biol 11:e1001719 [Google Scholar]
  13. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M. 13.  et al. 2009. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–88 [Google Scholar]
  14. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L. 14.  et al. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–22 [Google Scholar]
  15. Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojarvi J. 15.  et al. 2015. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLOS Genet 11:e1005373 [Google Scholar]
  16. Breiden M, Simon R. 16.  2016. Q&A: How does peptide signaling direct plant development?. BMC Biol 14:58 [Google Scholar]
  17. Brutus A, Sicilia F, Macone A, Cervone F, Lorenzo GD. 17.  2010. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. PNAS 107:9452–57 [Google Scholar]
  18. Bücherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M. 18.  et al. 2017. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6:e25114 [Google Scholar]
  19. Burdiak P, Rusaczonek A, Witon D, Glow D, Karpinski S. 19.  2015. Cysteine-rich receptor-like kinase CRK5 as a regulator of growth, development, and ultraviolet radiation responses in Arabidopsis thaliana. J. Exp. Bot 66:3325–37 [Google Scholar]
  20. Burr CA, Leslie ME, Orlowski SK, Chen I, Wright CE. 20.  et al. 2011. CAST AWAY, a membrane-associated receptor-like kinase, inhibits organ abscission in Arabidopsis. Plant Physiol 156:1837–50 [Google Scholar]
  21. Busch W, Benfey PN. 21.  2010. Information processing without brains—the power of intercellular regulators in plants. Development 137:1215–26 [Google Scholar]
  22. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS. 22.  et al. 2003. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–307 [Google Scholar]
  23. Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H. 23.  et al. 2014. Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26:1838–47 [Google Scholar]
  24. Buttner D.24.  2016. Behind the lines—actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40:894–937 [Google Scholar]
  25. Cao A, Xing L, Wang X, Yang X, Wang W. 25.  et al. 2011. Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. PNAS 108:7727–32 [Google Scholar]
  26. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP. 26.  et al. 2014. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:03766 [Google Scholar]
  27. Carol RJ, Dolan L. 27.  2006. The role of reactive oxygen species in cell growth: lessons from root hairs. J. Exp. Bot. 57:1829–34 [Google Scholar]
  28. Chen T, Bi K, He Z, Gao Z, Zhao Y. 28.  et al. 2016. Arabidopsis mutant bik1 exhibits strong resistance to Plasmodiophora brassicae. Front. Physiol 7:402 [Google Scholar]
  29. Cheng W, Munkvold KR, Gao H, Mathieu J, Schwizer S. 29.  et al. 2011. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10:616–26 [Google Scholar]
  30. Cheung AY, Wu HM. 30.  2011. THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases?. Curr. Opin. Plant Biol. 14:632–41 [Google Scholar]
  31. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T. 31.  et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500 [Google Scholar]
  32. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL. 32.  et al. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. PNAS 105:15629–34 [Google Scholar]
  33. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J. 33.  et al. 2014. Identification of a plant receptor for extracellular ATP. Science 343:290–94 [Google Scholar]
  34. Chung EH, da Cunha L, Wu AJ, Gao Z, Cherkis K. 34.  et al. 2011. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9:125–36 [Google Scholar]
  35. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL. 35.  2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–94 [Google Scholar]
  36. Clouse SD, Langford M, McMorris TC. 36.  1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–78 [Google Scholar]
  37. Costa ML, Marshell E, Tesfaye M, Silverstein KAT, Mori M. 37.  et al. 2014. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344:168–72 [Google Scholar]
  38. Couto D, Niebergall R, Liang X, Bucherl CA, Sklenar J. 38.  et al. 2016. The Arabidopsis protein phosphatase PP2C38 negatively regulates the central immune kinase BIK1. PLOS Pathog 12:e1005811 [Google Scholar]
  39. Couto D, Zipfel C. 39.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  40. Daudi A, Cheng Z, O'Brien JA, Mammarella N, Khan S. 40.  et al. 2012. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–87 [Google Scholar]
  41. Dodds PN, Rathjen JP. 41.  2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  42. Dong J, Xiao F, Fan F, Gu L, Cang H. 42.  et al. 2009. Crystal structure of the complex between Pseudomonas effector AvrPtoB and the tomato Pto kinase reveals both a shared and a unique interface compared with AvrPto-Pto. Plant Cell 21:1846–59 [Google Scholar]
  43. Dorjgotov D, Jurca ME, Fodor-Dunai C, Szucs A, Otvos K. 43.  et al. 2009. Plant Rho-type (Rop) GTPase-dependent activation of receptor-like cytoplasmic kinases in vitro. FEBS Lett 583:1175–82 [Google Scholar]
  44. Dou D, Zhou JM. 44.  2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–95 [Google Scholar]
  45. Du C, Li X, Chen J, Chen W, Li B. 45.  et al. 2016. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. PNAS 113:E8326–34 [Google Scholar]
  46. Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L. 46.  et al. 2014. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun 5:3129 [Google Scholar]
  47. Duan Q, Kita D, Li C, Cheung AY, Wu HM. 47.  2010. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. PNAS 107:17821–26 [Google Scholar]
  48. Dubiella U, Seybold H, Durian G, Komander E, Lassig R. 48.  et al. 2013. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. PNAS 110:8744–49 [Google Scholar]
  49. Dubouzet JG, Maeda S, Sugano S, Ohtake M, Hayashi N. 49.  et al. 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. 9:466–85 [Google Scholar]
  50. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J. 50.  et al. 2007. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–60 [Google Scholar]
  51. Felix G, Duran JD, Volko S, Boller T. 51.  1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–76 [Google Scholar]
  52. Feng F, Yang F, Rong W, Wu X, Zhang J. 52.  et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–18 [Google Scholar]
  53. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Mylona H. 53.  et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–46 [Google Scholar]
  54. Forzani C, Carreri A, de la Fuente van Bentem S, Lecourieux D, Lecourieux F, Hirt H. 54.  2011. The Arabidopsis protein kinase Pto-interacting 1–4 is a common target of the oxidative signal-inducible 1 and mitogen-activated protein kinases. FEBS J 278:1126–36 [Google Scholar]
  55. Frederick RD, Thilmony RL, Sessa G, Martin GB. 55.  1998. Recognition specificity for the bacterial avirulence protein AvrPto is determined by Thr-204 in the activation loop of the tomato Pto kinase. Mol. Cell 2:241–45 [Google Scholar]
  56. Fritz-Laylin LK, Krishnamurthy N, Tor M, Sjolander KV, Jones JD. 56.  2005. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol 138:611–23 [Google Scholar]
  57. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S. 57.  et al. 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535–39 [Google Scholar]
  58. Gao M, Wang X, Wang D, Xu F, Ding X. 58.  et al. 2009. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6:34–44 [Google Scholar]
  59. Ge Z, Bergonci T, Zhao Y, Zou Y, Du S. 59.  et al. 2017. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358:1596–600 [Google Scholar]
  60. Giri J, Vij S, Dansana PK, Tyagi AK. 60.  2011. Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol 191:721–32 [Google Scholar]
  61. Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T. 61.  et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824–32 [Google Scholar]
  62. Gómez-Gómez L, Boller T. 62.  2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 51003–11
  63. Groner WD, Christy ME, Kreiner CM, Liljegren SJ. 63.  2016. Allele-specific interactions between CAST AWAY and NEVERSHED control abscission in Arabidopsis flowers. Front. Plant Sci. 7:1588 [Google Scholar]
  64. Grutter C, Sreeramulu S, Sessa G, Rauh D. 64.  2013. Structural characterization of the RLCK family member BSK8: a pseudokinase with an unprecedented architecture. J. Mol. Biol. 425:4455–67 [Google Scholar]
  65. Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR. 65.  1998. Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. PNAS 95:382–87 [Google Scholar]
  66. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y. 66.  2009. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. PNAS 106:7648–53 [Google Scholar]
  67. Guo L, Guo C, Li M, Wang W, Luo C. 67.  et al. 2014. Suppression of expression of the putative receptor-like kinase gene NRRB enhances resistance to bacterial leaf streak in rice. Mol. Biol. Rep. 41:2177–87 [Google Scholar]
  68. Gust AA, Pruitt R, Nurnberger T. 68.  2017. Sensing danger: key to activating plant immunity. Trends Plant Sci 22:779–91 [Google Scholar]
  69. Guy E, Lautier M, Chabannes M, Roux B, Lauber E. 69.  et al. 2013. xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLOS ONE 8:e73469 [Google Scholar]
  70. Han Z, Sun Y, Chai J. 70.  2014. Structural insight into the activation of plant receptor kinases. Curr. Opin. Plant Biol. 20:55–63 [Google Scholar]
  71. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 71.  2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:1720–25 [Google Scholar]
  72. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S. 72.  et al. 2009. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–31 [Google Scholar]
  73. Haruta M, Sabat M, Stecker K, Minkoff BB, Sussman MR. 73.  2014. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–11 [Google Scholar]
  74. He Z, Wang ZY, Li J, Zhu Q, Lamb C. 74.  et al. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360–63 [Google Scholar]
  75. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K. 75.  et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22 [Google Scholar]
  76. Henty-Ridilla JL, Li J, Day B, Staiger CJ. 76.  2014. ACTIN DEPOLYMERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell 26:340–52 [Google Scholar]
  77. Herrmann MM, Pinto S, Kluth J, Wienand U, Lorbiecke R. 77.  2006. The PTI1-like kinase ZmPti1a from maize (Zea mays L.) co-localizes with callose at the plasma membrane of pollen and facilitates a competitive advantage to the male gametophyte. BMC Plant Biol 6:22 [Google Scholar]
  78. Hohmann U, Lau K, Hothorn M. 78.  2017. The structural basis of ligand perception and signal activation by receptor kinases. Annu. Rev. Plant Biol. 68:109–37 [Google Scholar]
  79. Hua D, Wang C, He J, Liao H, Duan Y. 79.  et al. 2012. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:2546–61 [Google Scholar]
  80. Huesmann C, Reiner T, Hoefle C, Preuss J, Jurca ME. 80.  et al. 2012. Barley ROP binding kinase1 is involved in microtubule organization and in basal penetration resistance to the barley powdery mildew fungus. Plant Physiol 159:311–20 [Google Scholar]
  81. Hunt L, Gray JE. 81.  2009. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19:864–69 [Google Scholar]
  82. Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL. 82.  et al. 2011. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev 25:232–37 [Google Scholar]
  83. Jinn TL, Stone JM, Walker JC. 83.  2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–17 [Google Scholar]
  84. Jones JDG, Dangl JL. 84.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  85. Jones JDG, Vance RE, Dangl JL. 85.  2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395 [Google Scholar]
  86. Kadota Y, Shirasu K, Zipfel C. 86.  2015. Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56:1472–80 [Google Scholar]
  87. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S. 87.  et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55Shows that BIK1 directly phosphorylates RBOHD, which is required for ROS production and immunity (see also 113). [Google Scholar]
  88. Kakita M, Murase K, Iwano M, Matsumoto T, Watanabe M. 88.  et al. 2007. Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 19:3961–73 [Google Scholar]
  89. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. 89.  et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103:11086–91 [Google Scholar]
  90. Kanda Y, Yokotani N, Maeda S, Nishizawa Y, Kamakura T, Mori M. 90.  2017. The receptor-like cytoplasmic kinase BSR1 mediates chitin-induced defense signaling in rice cells. Biosci. Biotechnol. Biochem. 81:1497–502 [Google Scholar]
  91. Kawai T, Akira S. 91.  2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11:373–84 [Google Scholar]
  92. Kim DS, Hwang BK. 92.  2011. The pepper receptor-like cytoplasmic protein kinase CaPIK1 is involved in plant signaling of defense and cell-death responses. Plant J 66:642–55 [Google Scholar]
  93. Kim DS, Kim NH, Hwang BK. 93.  2015. GLYCINE-RICH RNA-BINDING PROTEIN1 interacts with RECEPTOR-LIKE CYTOPLASMIC PROTEIN KINASE1 and suppresses cell death and defense responses in pepper (Capsicum annuum). New Phytol 205:786–800 [Google Scholar]
  94. Kim DS, Kim NH, Hwang BK. 94.  2015. The Capsicum annuum class IV chitinase ChitIV interacts with receptor-like cytoplasmic protein kinase PIK1 to accelerate PIK1-triggered cell death and defence responses. J. Exp. Bot. 66:1987–99 [Google Scholar]
  95. Kim TW, Guan S, Burlingame AL, Wang ZY. 95.  2011. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol. Cell 43:561–71 [Google Scholar]
  96. Kim TW, Guan S, Sun Y, Deng Z, Tang W. 96.  et al. 2009. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol. 11:1254–60 [Google Scholar]
  97. Kim TW, Wang ZY. 97.  2010. Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61:681–704 [Google Scholar]
  98. Kim YJ, Lin NC, Martin GB. 98.  2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–98 [Google Scholar]
  99. Kong Q, Sun T, Qu N, Ma J, Li M. 99.  et al. 2016. Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis. Plant Physiol 171:1344–54 [Google Scholar]
  100. Krol E, Mentzel T, Chinchilla D, Boller T, Felix G. 100.  et al. 2010. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285:13471–79 [Google Scholar]
  101. Laluk K, Luo H, Chai M, Dhawan R, Lai Z, Mengiste T. 101.  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 23:2831–49 [Google Scholar]
  102. Lecourieux D, Ranjeva R, Pugin A. 102.  2006. Calcium in plant defence-signalling pathways. New Phytol 171:249–69 [Google Scholar]
  103. Lee D, Bourdais G, Yu G, Robatzek S, Coaker G. 103.  2015. Phosphorylation of the plant immune regulator RPM1-INTERACTING PROTEIN4 enhances plant plasma membrane H+-ATPase activity and inhibits flagellin-triggered immune responses in Arabidopsis. Plant Cell 27:2042–56 [Google Scholar]
  104. Lee IC, Hong SW, Whang SS, Lim PO, Nam HG. 104.  et al. 2011. Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol 52:651–62 [Google Scholar]
  105. Lehti-Shiu MD, Zou C, Hanada K, Shiu SH. 105.  2009. Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26 [Google Scholar]
  106. Lemmon MA, Freed DM, Schlessinger J, Kiyatkin A. 106.  2016. The dark side of cell signaling: positive roles for negative regulators. Cell 164:1172–84 [Google Scholar]
  107. Lemmon MA, Schlessinger J. 107.  2010. Cell signaling by receptor tyrosine kinases. Cell 141:1117–34 [Google Scholar]
  108. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ. 108.  2010. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137:467–76 [Google Scholar]
  109. Lewis JD, Lee AH, Hassan JA, Wan J, Hurley B. 109.  et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:18722–27 [Google Scholar]
  110. Li J, Chory J. 110.  1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–38 [Google Scholar]
  111. Li J, Nam KH. 111.  2002. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 295:1299–301 [Google Scholar]
  112. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. 112.  2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–22 [Google Scholar]
  113. Li L, Li M, Yu L, Zhou Z, Liang X. 113.  et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38Shows that BIK1 directly phosphorylates RBOHD, which is required for RBOHD activation and immunity (see also 87). [Google Scholar]
  114. Li L, Yu Y, Zhou Z, Zhou JM. 114.  2016. Plant pattern-recognition receptors controlling innate immunity. Sci. China Life Sci. 59:878–88 [Google Scholar]
  115. Li Z, Ao Y, Feng D, Liu J, Wang J. 115.  et al. 2017. OsRLCK57, OsRLCK107 and OsRLCK118 positively regulate chitin- and PGN-induced immunity in rice. Rice 10:6 [Google Scholar]
  116. Liang X, Ding P, Lian K, Wang J, Ma M. 116.  et al. 2016. Arabidopsis heterotrimeric G proteins regulate immunity by directly coupling to the FLS2 receptor. eLife 5:e13568 [Google Scholar]
  117. Liao H, Zhu MM, Cui HH, Du XY, Tang Y. 117.  et al. 2016. MARIS plays important roles in Arabidopsis pollen tube and root hair growth. J. Integr. Plant Biol. 58:927–40 [Google Scholar]
  118. Liebrand TW, van den Burg HA, Joosten MH. 118.  2014. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19:123–32 [Google Scholar]
  119. Liljegren SJ, Leslie ME, Darnielle L, Lewis MW, Taylor SM. 119.  et al. 2009. Regulation of membrane trafficking and organ separation by the NEVERSHED ARF-GAP protein. Development 136:1909–18 [Google Scholar]
  120. Lin W, Li B, Lu D, Chen S, Zhu N. 120.  et al. 2014. Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. PNAS 111:3632–37 [Google Scholar]
  121. Lin W, Lu D, Gao X, Jiang S, Ma X. 121.  et al. 2013. Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1. PNAS 110:12114–19 [Google Scholar]
  122. Lin W, Ma X, Shan L, He P. 122.  2013. Big roles of small kinases: the complex functions of receptor-like cytoplasmic kinases in plant immunity and development. J. Integr. Plant Biol. 55:1188–97 [Google Scholar]
  123. Lin ZJ, Liebrand TW, Yadeta KA, Coaker G. 123.  2015. PBL13 is a serine/threonine protein kinase that negatively regulates Arabidopsis immune responses. Plant Physiol 169:2950–62 [Google Scholar]
  124. Lindner H, Muller LM, Boisson-Dernier A, Grossniklaus U. 124.  2012. CrRLK1L receptor-like kinases: not just another brick in the wall. Curr. Opin. Plant Biol. 15:659–69 [Google Scholar]
  125. Liu J, Ding P, Sun T, Nitta Y, Dong O. 125.  et al. 2013. Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol 161:2146–58 [Google Scholar]
  126. Liu J, Elmore JM, Lin ZJ, Coaker G. 126.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46 [Google Scholar]
  127. Liu J, Zhong S, Guo X, Hao L, Wei X. 127.  et al. 2013. Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr. Biol 23:993–98 [Google Scholar]
  128. Liu T, Liu Z, Song C, Hu Y, Han Z. 128.  et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–64 [Google Scholar]
  129. Liu Z, Jia Y, Ding Y, Shi Y, Li Z. 129.  et al. 2017. Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol. Cell 66:117–28.e5 [Google Scholar]
  130. Liu Z, Wu Y, Yang F, Zhang Y, Chen S. 130.  et al. 2013. BIK1 interacts with PEPRs to mediate ethylene-induced immunity. PNAS 110:6205–10 [Google Scholar]
  131. Lu D, Lin W, Gao X, Wu S, Cheng C. 131.  et al. 2011. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–42 [Google Scholar]
  132. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. 132.  2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. PNAS 107:496–501Identifies BIK1 as an RLCK required for immunity mediated by FLS2 (see also 247). [Google Scholar]
  133. Lukowitz W, Roeder A, Parmenter D, Somerville C. 133.  2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 9:109–19 [Google Scholar]
  134. Mao D, Yu F, Li J, Van de Poel B, Tan D. 134.  et al. 2015. FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant Cell Environ 38:2566–74 [Google Scholar]
  135. Marshall A, Aalen RB, Audenaert D, Beeckman T, Broadley MR. 135.  et al. 2012. Tackling drought stress: receptor-like kinases present new approaches. Plant Cell 24:2262–78 [Google Scholar]
  136. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW. 136.  et al. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–36 [Google Scholar]
  137. Maruta N, Trusov Y, Brenya E, Parekh U, Botella JR. 137.  2015. Membrane-localized extra-large G proteins and Gβγ of the heterotrimeric G proteins form functional complexes engaged in plant immunity in Arabidopsis. Plant Physiol 167:1004–16 [Google Scholar]
  138. Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A. 138.  et al. 2017. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358:1600–3 [Google Scholar]
  139. Meng X, Zhang S. 139.  2013. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51:245–66 [Google Scholar]
  140. Meng X, Zhou J, Tang J, Li B, de Oliveira MV. 140.  et al. 2016. Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–38 [Google Scholar]
  141. Mithoe SC, Ludwig C, Pel MJ, Cucinotta M, Casartelli A. 141.  et al. 2016. Attenuation of pattern recognition receptor signaling is mediated by a MAP kinase kinase kinase. EMBO Rep 17:441–54 [Google Scholar]
  142. Mittler R.142.  2017. ROS are good. Trends Plant Sci 22:11–19 [Google Scholar]
  143. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. 143.  et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. PNAS 104:19613–18 [Google Scholar]
  144. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T. 144.  et al. 2009. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19:1327–31 [Google Scholar]
  145. Molendijk AJ, Ruperti B, Singh MK, Dovzhenko A, Ditengou FA. 145.  et al. 2008. A cysteine-rich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors. Plant J 53:909–23 [Google Scholar]
  146. Monaghan J, Matschi S, Shorinola O, Rovenich H, Matei A. 146.  et al. 2014. The calcium-dependent protein kinase CPK28 buffers plant immunity and regulates BIK1 turnover. Cell Host Microbe 16:605–15Describes a key role of CPK28 in regulating BIK1 turnover through the ubiquitin-proteasome system. [Google Scholar]
  147. Mora-Garcia S, Vert G, Yin Y, Cano-Delgado A, Cheong H, Chory J. 147.  2004. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis. Genes Dev 18:448–60 [Google Scholar]
  148. Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE. 148.  et al. 2006. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–806 [Google Scholar]
  149. Murase K, Shiba H, Lwano M, Che FS, Watanabe M. 149.  et al. 2004. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303:1516–19Discovers that MLPK controls self-incompatibility in Brassica; MLPK is the first RLCK known to act downstream of an RK. [Google Scholar]
  150. Muto H, Yabe N, Asami T, Hasunuma K, Yamamoto KT. 150.  2004. Overexpression of constitutive differential growth 1 gene, which encodes a RLCKVII-subfamily protein kinase, causes abnormal differential and elongation growth after organ differentiation in Arabidopsis. Plant Physiol 136:3124–33 [Google Scholar]
  151. Nam KH, Li J. 151.  2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–12 [Google Scholar]
  152. Ntoukakis V, Mucyn TS, Gimenez-Ibanez S, Chapman HC, Gutierrez JR. 152.  et al. 2009. Host inhibition of a bacterial virulence effector triggers immunity to infection. Science 324:784–87 [Google Scholar]
  153. Nühse TS, Peck SC, Hirt H, Boller T. 153.  2000. Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK6. J. Biol. Chem. 275:7521–26 [Google Scholar]
  154. Oh MH, Wang X, Kota U, Goshe MB, Clouse SD, Huber SC. 154.  2009. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. PNAS 106:658–63 [Google Scholar]
  155. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H. 155.  et al. 2009. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–61 [Google Scholar]
  156. Oldham WM, Hamm HE. 156.  2008. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9:60–71 [Google Scholar]
  157. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K. 157.  2005. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17:1105–19 [Google Scholar]
  158. Osakabe Y, Mizuno S, Tanaka H, Maruyama K, Osakabe K. 158.  et al. 2010. Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J. Biol. Chem. 285:9190–201 [Google Scholar]
  159. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. 159.  2013. Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J. Exp. Bot. 64:445–58 [Google Scholar]
  160. Park HS, Lee SH, Park D, Lee JS, Ryu SH. 160.  et al. 2004. Sequential activation of phosphatidylinositol 3-kinase, βPix, Rac1, and Nox1 in growth factor-induced production of H2O2. Mol. Cell. Biol. 24:4384–94 [Google Scholar]
  161. Qi J, Wang J, Gong Z, Zhou JM. 161.  2017. Apoplastic ROS signaling in plant immunity. Curr. Opin. Plant Biol. 38:92–100 [Google Scholar]
  162. Ramegowda V, Basu S, Gupta C, Pereira A. 162.  2015. Regulation of grain yield in rice under well-watered and drought stress conditions by GUDK. Plant Signal Behav 10:e1034421 [Google Scholar]
  163. Ramegowda V, Basu S, Krishnan A, Pereira A. 163.  2014. Rice GROWTH UNDER DROUGHT KINASE is required for drought tolerance and grain yield under normal and drought stress conditions. Plant Physiol 166:1634–45 [Google Scholar]
  164. Ranf S, Eschen-Lippold L, Frohlich K, Westphal L, Scheel D, Lee J. 164.  2014. Microbe-associated molecular pattern-induced calcium signaling requires the receptor-like cytoplasmic kinases, PBL1 and BIK1. BMC Plant Biol 14:374 [Google Scholar]
  165. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D. 165.  2011. Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68:100–13 [Google Scholar]
  166. Ranf S, Gisch N, Schaffer M, Illig T, Westphal L. 166.  et al. 2015. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol 16:426–33 [Google Scholar]
  167. Reiner T, Hoefle C, Huesmann C, Menesi D, Feher A, Huckelhoven R. 167.  2015. The Arabidopsis ROP-activated receptor-like cytoplasmic kinase RLCK VI_A3 is involved in control of basal resistance to powdery mildew and trichome branching. Plant Cell Rep 34:457–68 [Google Scholar]
  168. Robatzek S, Chinchilla D, Boller T. 168.  2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–42 [Google Scholar]
  169. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB. 169.  2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–74 [Google Scholar]
  170. Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE. 170.  et al. 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 17:295–310 [Google Scholar]
  171. Russinova E, Borst JW, Kwaaitaal M, Caño-Delgado A, Yin Y. 171.  et al. 2004. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–29 [Google Scholar]
  172. Salmeron JM, Oldroyd GE, Rommens CM, Scofield SR, Kim HS. 172.  et al. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–33 [Google Scholar]
  173. Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL. 173.  2009. Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 9:2655–71 [Google Scholar]
  174. Santiago J, Henzler C, Hothorn M. 174.  2013. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341:889–92 [Google Scholar]
  175. Schwizer S, Kraus CM, Dunham DM, Zheng Y, Fernandez-Pozo N. 175.  et al. 2017. The tomato kinase Pti1 contributes to production of reactive oxygen species in response to two flagellin-derived peptides and promotes resistance to Pseudomonas syringae infection. Mol. Plant Microbe Interact. 30:725–38 [Google Scholar]
  176. Scofield SR, Tobias CM, Rathjen JP, Chang J, Lavelle DT. 176.  et al. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063–65 [Google Scholar]
  177. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, Rathjen JP. 177.  2011. Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol 156:687–99 [Google Scholar]
  178. Seto D, Koulena N, Lo T, Menna A, Guttman DS, Desveaux D. 178.  2017. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nat. Plants 3:17027 [Google Scholar]
  179. Shan L, He P, Li J, Heese A, Peck SC. 179.  et al. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27 [Google Scholar]
  180. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. 180.  2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–33 [Google Scholar]
  181. Shen W, Gómez-Cadenas A, Routly EL, Ho T-HD, Simmonds JA, Gulick PJ. 181.  2001. The salt stress-inducible protein kinase gene, Esi47, from the salt-tolerant wheatgrass Lophopyrum elongatum is involved in plant hormone signaling. Plant Physiol 125:1429–41 [Google Scholar]
  182. Sherrier D, Prome TA, Dupree P. 182.  1999. Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis. Electrophoresis 20:2027–35 [Google Scholar]
  183. Shi H, Shen Q, Qi Y, Yan H, Nie H. 183.  et al. 2013. BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25:1143–57 [Google Scholar]
  184. Shinya T, Yamaguchi K, Desaki Y, Yamada K, Narisawa T. 184.  et al. 2014. Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J 79:56–66 [Google Scholar]
  185. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. 185.  2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–34 [Google Scholar]
  186. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. 186.  2005. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–93 [Google Scholar]
  187. Sreekanta S, Bethke G, Hatsugai N, Tsuda K, Thao A. 187.  et al. 2015. The receptor-like cytoplasmic kinase PCRK1 contributes to pattern-triggered immunity against Pseudomonas syringae in Arabidopsis thaliana. New Phytol 207:78–90 [Google Scholar]
  188. Sreeramulu S, Mostizky Y, Sunitha S, Shani E, Nahum H. 188.  et al. 2013. BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant J 74:905–19 [Google Scholar]
  189. Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A. 189.  et al. 2017. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–89 [Google Scholar]
  190. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W. 190.  et al. 2008. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–17 [Google Scholar]
  191. Stone SL, Anderson EM, Mullen RT, Goring DR. 191.  2003. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–98 [Google Scholar]
  192. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A. 192.  et al. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–44 [Google Scholar]
  193. Sun T, Zhang Y, Li Y, Zhang Q, Ding Y, Zhang Y. 193.  2015. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat. Commun. 6:10159 [Google Scholar]
  194. Sun X, Sun M, Luo X, Ding X, Cai H. 194.  et al. 2013. A Glycine soja ABA-responsive receptor-like cytoplasmic kinase, GsRLCK, positively controls plant tolerance to salt and drought stresses. Planta 237:1527–45 [Google Scholar]
  195. Sun Y, Han Z, Tang J, Hu Z, Chai C. 195.  et al. 2013. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 23:1326–29 [Google Scholar]
  196. Swanson S, Gilroy S. 196.  2010. ROS in plant development. Physiol. Plant. 138:384–92 [Google Scholar]
  197. Swiderski MR, Innes RW. 197.  2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–12 [Google Scholar]
  198. Takayama S, Shimosato H, Shiba H, Funato M, Che FS. 198.  et al. 2001. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–38 [Google Scholar]
  199. Takeuchi H, Higashiyama T. 199.  2016. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245–48 [Google Scholar]
  200. Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K. 200.  et al. 2012. Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 70:599–613 [Google Scholar]
  201. Tang D, Wang G, Zhou JM. 201.  2017. Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell 29:618–37 [Google Scholar]
  202. Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z. 202.  et al. 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321:557–60Uses proteomic analysis to identify the RLCK-XII members BSKs as substrates of the RK BRI1 in BR signaling. [Google Scholar]
  203. Tang W, Yuan M, Wang R, Yang Y, Wang C. 203.  et al. 2011. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol. 13:124–31 [Google Scholar]
  204. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. 204.  1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–63 [Google Scholar]
  205. Torres MA, Dangl JL, Jones JD. 205.  2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99:517–22 [Google Scholar]
  206. Torres MA, Morales J, Sanchez-Rodriguez C, Molina A, Dangl JL. 206.  2013. Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Mol. Plant Microbe Interact. 26:686–94 [Google Scholar]
  207. Van Norman JM, Breakfield NW, Benfey PN. 207.  2011. Intercellular communication during plant development. Plant Cell 23:855–64 [Google Scholar]
  208. Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X. 208.  et al. 2006. The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18:257–73 [Google Scholar]
  209. Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK. 209.  2008. The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol. Plant 1:732–50 [Google Scholar]
  210. Wachsman G, Sparks EE, Benfey PN. 210.  2015. Genes and networks regulating root anatomy and architecture. New Phytol 208:26–38 [Google Scholar]
  211. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S. 211.  et al. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–81 [Google Scholar]
  212. Wang C, Wang G, Zhang C, Zhu P, Dai H. 212.  et al. 2017. OsCERK1-mediated chitin perception and immune signaling requires receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in rice. Mol. Plant 10:619–33 [Google Scholar]
  213. Wang G, Roux B, Feng F, Guy E, Li L. 213.  et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–95 [Google Scholar]
  214. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. 214.  2007. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73 [Google Scholar]
  215. Wang J, Grubb LE, Wang J, Liang X, Li L. 215.  et al. 2018. A regulatory module controlling homeostasis of a plant immune kinase. Mol. Cell. 69:493–504Shows that CPK28, heterotrimeric G proteins, and the E3 ligases PUB25 and PUB26 form a regulatory module for BIK1 homeostasis. [Google Scholar]
  216. Wang J, Shi H, Zhou L, Peng C, Liu D. 216.  et al. 2017. OsBSK1–2, an orthologous of AtBSK1, is involved in rice immunity. Front. Plant Sci. 8:908 [Google Scholar]
  217. Wang J, Wu G, Peng C, Zhou X, Li W. 217.  et al. 2015. The receptor-like cytoplasmic kinase OsRLCK102 regulates XA21-mediated immunity and plant development in rice. Plant Mol. Biol. Rep. 34:628–37 [Google Scholar]
  218. Wang T, Liang L, Xue Y, Jia PF, Chen W. 218.  et al. 2016. A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:241–44 [Google Scholar]
  219. Wang W, Bai MY, Wang ZY. 219.  2014. The brassinosteroid signaling network—a paradigm of signal integration. Curr. Opin. Plant Biol. 21:147–53 [Google Scholar]
  220. Wang X, Kota U, He K, Blackburn K, Li J. 220.  et al. 2008. Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev. Cell 15:220–35 [Google Scholar]
  221. Wang ZY, Nakano T, Gendron J, He J, Chen M. 221.  et al. 2002. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2:505–13 [Google Scholar]
  222. Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. 222.  2001. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–83 [Google Scholar]
  223. Warren RF, Merritt PM, Holub E, Innes RW. 223.  1999. Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152:410–12 [Google Scholar]
  224. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T. 224.  et al. 2007. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–34 [Google Scholar]
  225. Wymer CL, Bibikova TN, Gilory S. 225.  1997. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–39 [Google Scholar]
  226. Xiang T, Zong N, Zou Y, Wu Y, Zhang J. 226.  et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74–80 [Google Scholar]
  227. Xiao F, He P, Abramovitch RB, Dawson JE, Nicholson LK. 227.  et al. 2007. The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant J 52:595–614 [Google Scholar]
  228. Xu N, Luo X, Li W, Wang Z, Liu J. 228.  2017. The bacterial effector AvrB-induced RIN4 hyperphosphorylation is mediated by a receptor-like cytoplasmic kinase complex in Arabidopsis. Mol Plant Microbe Interact 30:502–12 [Google Scholar]
  229. Yamada K, Yamaguchi K, Shirakawa T, Nakagami H, Mine A. 229.  et al. 2016. The Arabidopsis CERK1-associated kinase PBL27 connects chitin perception to MAPK activation. EMBO J 35:2468–83 [Google Scholar]
  230. Yamada K, Yamaguchi K, Yoshimura S, Terauchi A, Kawasaki T. 230.  2017. Conservation of chitin-induced MAPK signaling pathways in rice and Arabidopsis. Plant Cell Physiol 58:993–1002 [Google Scholar]
  231. Yamada K, Yamashita-Yamada M, Hirase T, Fujiwara T, Tsuda K. 231.  et al. 2016. Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1. EMBO J 35:46–61 [Google Scholar]
  232. Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N. 232.  et al. 2013. A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13:347–57 [Google Scholar]
  233. Yang L, Ji W, Zhu Y, Gao P, Li Y. 233.  et al. 2010. GsCBRLK, a calcium/calmodulin-binding receptor-like kinase, is a positive regulator of plant tolerance to salt and ABA stress. J. Exp. Bot. 61:2519–33 [Google Scholar]
  234. Yang T, Ali GS, Yang L, Reddy A, Poovaiah BW. 234.  2010. Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5:991–94 [Google Scholar]
  235. Yang T, Chaudhuri S, Yang L, Chen Y, Poovaiah BW. 235.  2004. Calcium/calmodulin up-regulates a cytoplasmic receptor-like kinase in plants. J. Biol. Chem. 279:42552–59 [Google Scholar]
  236. Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW. 236.  2010. A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J. Biol. Chem. 285:7119–26 [Google Scholar]
  237. Yeatman TJ.237.  2004. A renaissance for SRC. Nat. Rev. Cancer 4:470–80 [Google Scholar]
  238. Yan H, Zhao Y, Shi H, Li J, Wang Y. 238.  et al. 2018. BRASSINOSTEROID-SIGNALING KINASE1 phosphorylates MAPKKK5 to regulate immunity in Arabidopsis. Plant Physiol pii 01757
  239. Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S. 239.  et al. 2002. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–91 [Google Scholar]
  240. Yu F, Qian L, Nibau C, Duan Q, Kita D. 240.  et al. 2012. FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. PNAS 109:14693–98 [Google Scholar]
  241. Yu TY, Shi DQ, Jia PF, Tang J, Li HJ. 241.  et al. 2016. The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. PLOS Genet 12:e1005933 [Google Scholar]
  242. Yu X, Feng B, He P, Shan L. 242.  2017. From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 55:109–37 [Google Scholar]
  243. Yuan GL, Li HJ, Yang WC. 243.  2017. The integration of Gβ and MAPK signaling cascade in zygote development. Sci. Rep. 7:8732 [Google Scholar]
  244. Zhang B, Wang X, Zhao Z, Wang R, Huang X. 244.  et al. 2016. OsBRI1 activates BR signaling by preventing binding between the TPR and kinase domains of OsBSK3 via phosphorylation. Plant Physiol 170:1149–61 [Google Scholar]
  245. Zhang H, Han Z, Song W, Chai J. 245.  2016. Structural insight into recognition of plant peptide hormones by receptors. Mol. Plant 9:1454–63 [Google Scholar]
  246. Zhang H, Lin X, Han Z, Qu LJ, Chai J. 246.  2016. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Res 26:543–55 [Google Scholar]
  247. Zhang J, Li W, Xiang T, Liu Z, Laluk K. 247.  et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301BIK1 and PBL1 regulate immunity downstream of multiple PRRs and are targeted by a bacterial protease for virulence. [Google Scholar]
  248. Zhang J, Shao F, Li Y, Cui H, Chen L. 248.  et al. 2007. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–85 [Google Scholar]
  249. Zhang Y, Zhu H, Zhang Q, Li M, Yan M. 249.  et al. 2009. Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–77 [Google Scholar]
  250. Zhang Z, Liu Y, Huang H, Gao M, Wu D. 250.  et al. 2017. The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Rep 18:292–302 [Google Scholar]
  251. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q. 251.  et al. 2012. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–63 [Google Scholar]
  252. Zhou X, Wang J, Peng C, Zhu X, Yin J. 252.  et al. 2016. Four receptor-like cytoplasmic kinases regulate development and immunity in rice. Plant Cell Environ 39:1381–92 [Google Scholar]
  253. Zhu JK.253.  2016. Abiotic stress signaling and responses in plants. Cell 167:313–24 [Google Scholar]
  254. Zipfel C, Oldroyd GE. 254.  2017. Plant signalling in symbiosis and immunity. Nature 543:328–36 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040540
Loading
Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling
Annual Review of Plant Biology 69, 267 (2018); https://doi.org/10.1146/annurev-arplant-042817-040540
/content/journals/10.1146/annurev-arplant-042817-040540
/content/journals/10.1146/annurev-arplant-042817-040540
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error