1932

Abstract

Plants have evolved a family of unique membrane receptor kinases to orchestrate the growth and development of their cells, tissues, and organs. Receptor kinases also form the first line of defense of the plant immune system and allow plants to engage in symbiotic interactions. Here, we discuss recent advances in understanding, at the molecular level, how receptor kinases with lysin-motif or leucine-rich-repeat ectodomains have evolved to sense a broad spectrum of ligands. We summarize and compare the established receptor activation mechanisms for plant receptor kinases and dissect how ligand binding at the cell surface leads to activation of cytoplasmic signaling cascades. Our review highlights that one family of plant membrane receptors has diversified structurally to fulfill very different signaling tasks.

[Erratum, Closure]

An erratum has been published for this article:
The Structural Basis of Ligand Perception and Signal Activation by Receptor Kinases
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042916-040957
2017-04-28
2024-06-17
Loading full text...

Full text loading...

/deliver/fulltext/arplant/68/1/annurev-arplant-042916-040957.html?itemId=/content/journals/10.1146/annurev-arplant-042916-040957&mimeType=html&fmt=ahah

Literature Cited

  1. Albert I, Böhm H, Albert M, Feiler CE, Imkampe J. 1.  et al. 2015. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 1:15140 [Google Scholar]
  2. Antolín-Llovera M, Petutsching EK, Ried MK, Lipka V, Nürnberger T. 2.  et al. 2014. Knowing your friends and foes—plant receptor-like kinases as initiators of symbiosis or defence. New Phytol 204:791–802 [Google Scholar]
  3. Antolín-Llovera M, Ried MK, Binder A, Parniske M. 3.  2012. Receptor kinase signaling pathways in plant-microbe interactions. Annu. Rev. Phytopathol. 50:451–73 [Google Scholar]
  4. Aranda-Sicilia MN, Trusov Y, Maruta N, Chakravorty D, Zhang Y, Botella JR. 4.  2015. Heterotrimeric G proteins interact with defense-related receptor-like kinases in Arabidopsis. J. Plant Physiol. 188:44–48 [Google Scholar]
  5. Bateman A, Bycroft M. 5.  2000. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299:1113–19 [Google Scholar]
  6. Blaum BS, Mazzotta S, Nöldeke ER, Halter T, Madlung J. 6.  et al. 2014. Structure of the pseudokinase domain of BIR2, a regulator of BAK1-mediated immune signaling in Arabidopsis. J. Struct. Biol. 186:112–21 [Google Scholar]
  7. Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M. 7.  2014. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J 78:31–43 [Google Scholar]
  8. Borner GHH, Lilley KS, Stevens TJ, Dupree P. 8.  2003. Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–77 [Google Scholar]
  9. Botos I, Segal DM, Davies DR. 9.  2011. The structural biology of Toll-like receptors. Structure 19:447–59 [Google Scholar]
  10. Brandt B, Hothorn M. 10.  2016. SERK co-receptor kinases. Curr. Biol. 26:R225–26 [Google Scholar]
  11. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT. 11.  et al. 2012. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. PNAS 109:13859–64 [Google Scholar]
  12. Bücherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH. 12.  et al. 2013. Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol 162:1911–25 [Google Scholar]
  13. Buist G, Steen A, Kok J, Kuipers OP. 13.  2008. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68:838–47 [Google Scholar]
  14. Burr CA, Leslie ME, Orlowski SK, Chen I, Wright CE. 14.  et al. 2011. CAST AWAY, a membrane-associated receptor-like kinase, inhibits organ abscission in Arabidopsis. Plant Physiol 156:1837–50 [Google Scholar]
  15. Butenko MA, Patterson SE, Grini PE, Stenvik G-E, Amundsen SS. 15.  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]
  16. Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H. 16.  et al. 2014. Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26:1838–47 [Google Scholar]
  17. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S. 17.  et al. 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–51 [Google Scholar]
  18. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP. 18.  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:e03766 [Google Scholar]
  19. Chang C, Schaller GE, Patterson SE, Kwok SF, Meyerowitz EM, Bleecker AB. 19.  1992. The TMK1 gene from Arabidopsis codes for a protein with structural and biochemical characteristics of a receptor protein kinase. Plant Cell 4:1263–71 [Google Scholar]
  20. Chen X, Zuo S, Schwessinger B, Chern M, Canlas PE. 20.  et al. 2014. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol. Plant 7:874–92 [Google Scholar]
  21. Cheng W, Munkvold KR, Gao H, Mathieu J, Schwizer S. 21.  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]
  22. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. 22.  2006. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–76 [Google Scholar]
  23. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T. 23.  et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500 [Google Scholar]
  24. Clark SE, Running MP, Meyerowitz EM. 24.  1993. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418 [Google Scholar]
  25. Clouse SD, Langford M, McMorris TC. 25.  1996. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–78 [Google Scholar]
  26. Couto D, Zipfel C. 26.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  27. Dai N, Wang W, Patterson SE, Bleecker AB. 27.  2013. The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLOS ONE 8:e60990 [Google Scholar]
  28. D'Andrea LD, Regan L. 28.  2003. TPR proteins: the versatile helix. Trends Biochem. Sci. 28:655–62 [Google Scholar]
  29. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y. 29.  et al. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–55 [Google Scholar]
  30. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE. 30.  2006. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16 [Google Scholar]
  31. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA. 31.  et al. 2003. The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. PNAS 100:10124–28 [Google Scholar]
  32. Etchells JP, Turner SR. 32.  2010. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137:767–74 [Google Scholar]
  33. Fisher K, Turner S. 33.  2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17:1061–66 [Google Scholar]
  34. Fliegmann J, Bono J-J. 34.  2015. Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors. Glycoconj. J. 32:455–64 [Google Scholar]
  35. Fliegmann J, Canova S, Lachaud C, Uhlenbroich S, Gasciolli V. 35.  et al. 2013. Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM receptor-like kinase LYR3 in the legume Medicago truncatula. ACS Chem. Biol. 8:1900–6 [Google Scholar]
  36. Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T. 36.  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]
  37. Gómez-Gómez L, Boller T. 37.  2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003–11 [Google Scholar]
  38. Gou X, Yin H, He K, Du J, Yi J. 38.  et al. 2012. Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLOS Genet 8:e1002452 [Google Scholar]
  39. Grütter C, Sreeramulu S, Sessa G, Rauh D. 39.  2013. Structural characterization of the RLCK family member BSK8: a pseudokinase with an unprecedented architecture. J. Mol. Biol. 425:4455–67 [Google Scholar]
  40. Halter T, Imkampe J, Mazzotta S, Wierzba M, Postel S. 40.  et al. 2014. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr. Biol. 24:134–43 [Google Scholar]
  41. Han BW, Herrin BR, Cooper MD, Wilson IA. 41.  2008. Antigen recognition by variable lymphocyte receptors. Science 321:1834–37 [Google Scholar]
  42. Hanai H, Matsuno T, Yamamoto M, Matsubayashi Y, Kobayashi T. 42.  et al. 2000. A secreted peptide growth factor, phytosulfokine, acting as a stimulatory factor of carrot somatic embryo formation. Plant Cell Physiol 41:27–32 [Google Scholar]
  43. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 43.  2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:1720–25 [Google Scholar]
  44. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M. 44.  et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. PNAS 111:E404–13 [Google Scholar]
  45. Hazak O, Hardtke CS. 45.  2016. CLAVATA 1-type receptors in plant development. J. Exp. Bot. 67:4827–33 [Google Scholar]
  46. He Z, Wang Z-Y, Li J, Zhu Q, Lamb C. 46.  et al. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360–63 [Google Scholar]
  47. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K. 47.  et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22 [Google Scholar]
  48. Hink MA, Shah K, Russinova E, de Vries SC, Visser AJWG. 48.  2008. Fluorescence fluctuation analysis of Arabidopsis thaliana somatic embryogenesis receptor-like kinase and brassinosteroid insensitive 1 receptor oligomerization. Biophys. J. 94:1052–62 [Google Scholar]
  49. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP. 49.  et al. 2011. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467–71 [Google Scholar]
  50. Hothorn M, Dabi T, Chory J. 50.  2011. Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat. Chem. Biol. 7:766–68 [Google Scholar]
  51. Huang J, Zhang T, Linstroth L, Tillman Z, Otegui MS. 51.  et al. 2016. Control of anther cell differentiation by the small protein ligand TPD1 and its receptor EMS1 in Arabidopsis. PLOS Genet. 12:e1006147 [Google Scholar]
  52. Huffaker A, Pearce G, Ryan CA. 52.  2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. PNAS 103:10098–103 [Google Scholar]
  53. Iizasa E, Mitsutomi M, Nagano Y. 53.  2010. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 285:2996–3004 [Google Scholar]
  54. Ito Y, Kaku H, Shibuya N. 54.  1997. Identification of a high-affinity binding protein for N-acetylchitooligosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J 12:347–56 [Google Scholar]
  55. Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL. 55.  et al. 2011. Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev 25:232–37 [Google Scholar]
  56. Jeong S, Trotochaud AE, Clark SE. 56.  1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–34 [Google Scholar]
  57. Jia G, Liu X, Owen HA, Zhao D. 57.  2008. Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. PNAS 105:2220–25 [Google Scholar]
  58. Jiang J, Wang T, Wu Z, Wang J, Zhang C. 58.  et al. 2015. The intrinsically disordered protein BKI1 is essential for inhibiting BRI1 signaling in plants. Mol. Plant 8:1675–78 [Google Scholar]
  59. Jinn T-L, Stone JM, Walker JC. 59.  2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–17 [Google Scholar]
  60. Jordá L, Sopeña-Torres S, Escudero V, Nuñez-Corcuera B, Delgado-Cerezo M. 60.  et al. 2016. ERECTA and BAK1 receptor like kinases interact to regulate immune responses in Arabidopsis. Front. Plant Sci. 7:897 [Google Scholar]
  61. Kadota Y, Macho AP, Zipfel C. 61.  2016. Immunoprecipitation of Plasma Membrane Receptor-Like Kinases for identification of phosphorylation sites and associated proteins. Methods Mol. Biol. 1363:133–44 [Google Scholar]
  62. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. 62.  et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103:11086–91 [Google Scholar]
  63. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S. 63.  et al. 2010. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–20 [Google Scholar]
  64. Kobe B, Kajava AV. 64.  2001. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11:725–32 [Google Scholar]
  65. Konrad SSA, Ott T. 65.  2015. Molecular principles of membrane microdomain targeting in plants. Trends Plant Sci 20:351–61 [Google Scholar]
  66. Krol E, Mentzel T, Chinchilla D, Boller T, Felix G. 66.  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]
  67. Kumpf RP, Shi C-L, Larrieu A, Stø IM, Butenko MA. 67.  et al. 2013. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. PNAS 110:5235–40 [Google Scholar]
  68. Kwezi L, Meier S, Mungur L, Ruzvidzo O, Irving H, Gehring C. 68.  2007. The Arabidopsis thaliana brassinosteroid receptor (AtBRI1) contains a domain that functions as a guanylyl cyclase in vitro. PLOS ONE 2:e449 [Google Scholar]
  69. Lee JS, Hnilova M, Maes M, Lin Y-CL, Putarjunan A. 69.  et al. 2015. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:439–43 [Google Scholar]
  70. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM. 70.  et al. 2012. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26:126–36 [Google Scholar]
  71. Li J, Chory J. 71.  1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–38 [Google Scholar]
  72. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. 72.  2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–22 [Google Scholar]
  73. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R. 73.  2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–33 [Google Scholar]
  74. Liu L, Botos I, Wang Y, Leonard JN, Shiloach J. 74.  et al. 2008. Structural basis of Toll-like receptor 3 signaling with double-stranded RNA. Science 320:379–81 [Google Scholar]
  75. Liu P, Hu Z, Zhou B, Liu S, Chai J. 75.  2013. Crystal structure of an LRR protein with two solenoids. Cell Res 23:303–5 [Google Scholar]
  76. Liu S, Wang J, Han Z, Gong X, Zhang H, Chai J. 76.  2016. Molecular mechanism for fungal cell wall recognition by rice chitin receptor OsCEBiP. Structure 24:1192–200 [Google Scholar]
  77. Liu T, Liu Z, Song C, Hu Y, Han Z. 77.  et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–64 [Google Scholar]
  78. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M. 78.  et al. 2003. A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals. Nature 425:637–40 [Google Scholar]
  79. Malkov N, Fliegmann J, Rosenberg C, Gasciolli V, Timmers ACJ. 79.  et al. 2016. Molecular basis of lipo-chitooligosaccharide recognition by the lysin motif receptor-like kinase LYR3 in legumes. Biochem. J. 473:1369–78 [Google Scholar]
  80. Matsubayashi Y.80.  2014. Posttranslationally modified small-peptide signals in plants. Annu. Rev. Plant Biol. 65:385–413 [Google Scholar]
  81. Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y. 81.  2006. Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142:45–53 [Google Scholar]
  82. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. 82.  2002. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–72 [Google Scholar]
  83. Matsubayashi Y, Sakagami Y. 83.  1996. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. PNAS 93:7623–27 [Google Scholar]
  84. McAndrew R, Pruitt RN, Kamita SG, Pereira JH, Majumdar D. 84.  et al. 2014. Structure of the OsSERK2 leucine-rich repeat extracellular domain. Acta Crystallogr. D 70:3080–86 [Google Scholar]
  85. Meng X, Chen X, Mang H, Liu C, Yu X. 85.  et al. 2015. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr. Biol. 25:2361–72 [Google Scholar]
  86. Meng X, Zhou J, Tang J, Li B, de Oliveira MVV. 86.  et al. 2016. Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–38 [Google Scholar]
  87. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. 87.  et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. PNAS 104:19613–18 [Google Scholar]
  88. Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K. 88.  et al. 2007. Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 50:751–66 [Google Scholar]
  89. Morita J, Kato K, Nakane T, Kondo Y, Fukuda H. 89.  et al. 2016. Crystal structure of the plant receptor-like kinase TDR in complex with the TDIF peptide. Nat. Commun. 7:12383 [Google Scholar]
  90. Müller R, Bleckmann A, Simon R. 90.  2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–46 [Google Scholar]
  91. Nam KH, Li J. 91.  2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–12 [Google Scholar]
  92. Nimchuk ZL, Tarr PT, Meyerowitz EM. 92.  2011. An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23:851–54 [Google Scholar]
  93. Oh M-H, Clouse SD, Huber SC. 93.  2012. Tyrosine phosphorylation of the BRI1 receptor kinase occurs via a post-translational modification and is activated by the juxtamembrane domain. Front. Plant Sci. 3:175 [Google Scholar]
  94. Oh M-H, Wang X, Kota U, Goshe MB, Clouse SD, Huber SC. 94.  2009. Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. PNAS 106:658–63 [Google Scholar]
  95. Ou Y, Lu X, Zi Q, Xun Q, Zhang J. 95.  et al. 2016. RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res. 26:686–98 [Google Scholar]
  96. Park BS, Song DH, Kim HM, Choi B-S, Lee H, Lee J-O. 96.  2009. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458:1191–95 [Google Scholar]
  97. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V. 97.  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. 285:28902–11 [Google Scholar]
  98. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y. 98.  et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–92 [Google Scholar]
  99. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A. 99.  et al. 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 23:2440–55 [Google Scholar]
  100. Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA. 100.  et al. 2016. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5:e15075 [Google Scholar]
  101. Santiago J, Henzler C, Hothorn M. 101.  2013. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341:889–92 [Google Scholar]
  102. Schmidt ED, Guzzo F, Toonen MA, de Vries SC. 102.  1997. A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–62 [Google Scholar]
  103. Shan L, He P, Li J, Heese A, Peck SC. 103.  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]
  104. She J, Han Z, Kim T-W, Wang J, Cheng W. 104.  et al. 2011. Structural insight into brassinosteroid perception by BRI1. Nature 474:472–76 [Google Scholar]
  105. She J, Han Z, Zhou B, Chai J. 105.  2013. Structural basis for differential recognition of brassinolide by its receptors. Protein Cell 4:475–82 [Google Scholar]
  106. Shimizu N, Ishida T, Yamada M, Shigenobu S, Tabata R. 106.  et al. 2015. BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol 208:1104–13 [Google Scholar]
  107. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N. 107.  et al. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–14 [Google Scholar]
  108. Shinohara H, Matsubayashi Y. 108.  2015. Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. Plant J. 82:328–36 [Google Scholar]
  109. Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y. 109.  2016. Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. PNAS 113:3897–3902 [Google Scholar]
  110. Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y. 110.  2012. Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J 70:845–54 [Google Scholar]
  111. Shiu SH, Bleecker AB. 111.  2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. PNAS 98:10763–68 [Google Scholar]
  112. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. 112.  2005. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–93 [Google Scholar]
  113. Somssich M, Ma Q, Weidtkamp-Peters S, Stahl Y, Felekyan S. 113.  et al. 2015. Real-time dynamics of peptide ligand-dependent receptor complex formation in planta. Sci. Signal. 8:ra76 [Google Scholar]
  114. Song W, Han Z, Sun Y, Chai J. 114.  2013. Crystal structure of a plant leucine rich repeat protein with two island domains. Sci. China Life Sci. 57:137–44 [Google Scholar]
  115. Song W, Liu L, Wang J, Wu Z, Zhang H. 115.  et al. 2016. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res 26:674–85 [Google Scholar]
  116. Sreeramulu S, Mostizky Y, Sunitha S, Shani E, Nahum H. 116.  et al. 2013. BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant J 74:905–19 [Google Scholar]
  117. Stenvik G-E, Tandstad NM, Guo Y, Shi C-L, Kristiansen W. 117.  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]
  118. Sun W, Cao Y, Labby KJ, Bittel P, Boller T, Bent AF. 118.  2012. Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24:1096–113 [Google Scholar]
  119. Sun Y, Han Z, Tang J, Hu Z, Chai C. 119.  et al. 2013. Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 23:1326–29 [Google Scholar]
  120. Sun Y, Li L, Macho AP, Han Z, Hu Z. 120.  et al. 2013. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–28 [Google Scholar]
  121. Szczyglowski K, Shaw RS, Wopereis J, Copeland S, Hamburger D. 121.  et al. 1998. Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant-Microbe Interact. 11:684–97 [Google Scholar]
  122. Tang J, Han Z, Sun Y, Zhang H, Gong X, Chai J. 122.  2015. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res 25:110–20 [Google Scholar]
  123. Tang W, Kim T-W, Oses-Prieto JA, Sun Y, Deng Z. 123.  et al. 2008. BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321:557–60 [Google Scholar]
  124. Tunc-Ozdemir M, Urano D, Jaiswal DK, Clouse SD, Jones AM. 124.  2016. Direct modulation of heterotrimeric G protein-coupled signaling by a receptor kinase complex. J. Biol. Chem. 291:13918–25 [Google Scholar]
  125. van der Hoorn RAL, Wulff BBH, Rivas S, Durrant MC, van der Ploeg A. 125.  et al. 2005. Structure-function analysis of CF-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17:1000–15 [Google Scholar]
  126. Walker JC.126.  1993. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3:451–56 [Google Scholar]
  127. Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S. 127.  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]
  128. Wang J, Jiang J, Wang J, Chen L, Fan S-L. 128.  et al. 2014. Structural insights into the negative regulation of BRI1 signaling by BRI1-interacting protein BKI1. Cell Res. 24:1328–41 [Google Scholar]
  129. Wang J, Li H, Han Z, Zhang H, Wang T. 129.  et al. 2015. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–68 [Google Scholar]
  130. Wang X, Kota U, He K, Blackburn K, Li J. 130.  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]
  131. Wang X, Li X, Meisenhelder J, Hunter T, Yoshida S. 131.  et al. 2005. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell 8:855–65 [Google Scholar]
  132. Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. 132.  2001. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–83 [Google Scholar]
  133. Wolf S, van der Does D, Ladwig F, Sticht C, Kolbeck A. 133.  et al. 2014. A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling. PNAS 111:15261–66 [Google Scholar]
  134. Wong JEMM, Midtgaard SR, Gysel K, Thygesen MB, Sørensen KK. 134.  et al. 2015. An intermolecular binding mechanism involving multiple LysM domains mediates carbohydrate recognition by an endopeptidase. Acta Crystallogr. D 71:592–605 [Google Scholar]
  135. Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM. 135.  et al. 2000. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23:97–114 [Google Scholar]
  136. Xing W, Zou Y, Liu Q, Liu J, Luo X. 136.  et al. 2007. The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243–47 [Google Scholar]
  137. Xu T, Dai N, Chen J, Nagawa S, Cao M. 137.  et al. 2014. Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025–28 [Google Scholar]
  138. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. 138.  2010. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–22 [Google Scholar]
  139. Yamaguchi Y, Pearce G, Ryan CA. 139.  2006. The cell surface leucine-rich repeat receptor for AtPEP1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. PNAS 103:10104–9 [Google Scholar]
  140. Yan L, Ma Y, Liu D, Wei X, Sun Y. 140.  et al. 2012. Structural basis for the impact of phosphorylation on the activation of plant receptor-like kinase BAK1. Cell Res 22:1304–8 [Google Scholar]
  141. Yang M, Sack FD. 141.  1995. The too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 7:2227–39 [Google Scholar]
  142. Zhang B, Ramonell K, Somerville S, Stacey G. 142.  2002. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15:963–70 [Google Scholar]
  143. Zhang B, Wang X, Zhao Z, Wang R, Huang X. 143.  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]
  144. Zhang H, Lin X, Han Z, Qu L-J, Chai J. 144.  2016. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Res 26:543–55 [Google Scholar]
  145. Zhang H, Lin X, Han Z, Wang J, Qu L-J, Chai J. 145.  2016. SERK family receptor-like kinases function as co-receptors with PXY for plant vascular development. Mol. Plant 9:1406–14 [Google Scholar]
  146. Zhang X, Gureasko J, Shen K, Cole PA, Kuriyan J. 146.  2006. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125:1137–49 [Google Scholar]
  147. Zhang X, Pickin KA, Bose R, Jura N, Cole PA, Kuriyan J. 147.  2007. Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450:741–44 [Google Scholar]
  148. Zhao D-Z, Wang G-F, Speal B, Ma H. 148.  2002. The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–31 [Google Scholar]
  149. Zhao X, de Palma J, Oane R, Gamuyao R, Luo M. 149.  et al. 2008. OsTDL1a binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–87 [Google Scholar]
  150. Zhou A, Wang H, Walker JC, Li J. 150.  2004. BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J 40:399–409 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042916-040957
Loading
/content/journals/10.1146/annurev-arplant-042916-040957
Loading

Data & Media loading...

  • Article Type: Review Article
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