1932

Abstract

Because of their high level of diversity and complex evolutionary histories, most studies on plant receptor-like kinase subfamilies have focused on their kinase domains. With the large amount of genome sequence data available today, particularly on basal land plants and Charophyta, more attention should be paid to primary events that shaped the diversity of the RLK gene family. We thus focus on the motifs and domains found in association with kinase domains to illustrate their origin, organization, and evolutionary dynamics. We discuss when these different domain associations first occurred and how they evolved, based on a literature review complemented by some of our unpublished results.

Keyword(s): diversitydomainkinaseoriginplantreceptorRKRLK
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-073019-025927
2020-04-29
2024-10-13
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-073019-025927.html?itemId=/content/journals/10.1146/annurev-arplant-073019-025927&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ahlquist RP. 1948. A study of the adrenotropic receptors. Am. J. Physiol. 153:586–600
    [Google Scholar]
  2. 2. 
    Arabidopsis Genome Initiative 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
    [Google Scholar]
  3. 3. 
    Ardourel M, Demont N, Debelle F, Maillet F, de Billy F et al. 1994. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6:1357–74
    [Google Scholar]
  4. 4. 
    Azevedo C, Santos-Rosa MJ, Shirasu K 2001. The U-box protein family in plants. Trends Plant Sci 6:354–58
    [Google Scholar]
  5. 5. 
    Bacete L, Mélida H, Miedes E, Molina A 2018. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:4614–36
    [Google Scholar]
  6. 6. 
    Baek D, Kim MC, Kumar D, Park B, Cheong MS et al. 2019. AtPR5K2, a PR5-like receptor kinase, modulates plant responses to drought stress by phosphorylating protein phosphatase 2Cs. Front. Plant Sci. 10:1146
    [Google Scholar]
  7. 7. 
    Becraft PW, Stinard PS, McCarty DR 1996. CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–9
    [Google Scholar]
  8. 8. 
    Bellande K, Bono JJ, Savelli B, Jamet E, Canut H 2017. Plant lectins and lectin receptor-like kinases: How do they sense the outside. Int. J. Mol. Sci. 18:E1164
    [Google Scholar]
  9. 9. 
    Bleecker AB. 1991. Genetic analysis of ethylene responses in Arabidopsis thaliana. Symp. Soc. Exp. Biol 45:149–58
    [Google Scholar]
  10. 10. 
    Boisson-Dernier A, Kessler SA, Grossniklaus U 2011. The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J. Exp. Bot. 62:1581–91
    [Google Scholar]
  11. 11. 
    Bonner TI, Oppermann H, Seeburg P, Kerby SB, Gunnell MA et al. 1986. The complete coding sequence of the human raf oncogene and the corresponding structure of the c-raf-1 gene. Nucleic Acids Res 14:1009–15
    [Google Scholar]
  12. 12. 
    Borassi C, Sede AR, Mecchia MA, Salgado Salter JD, Marzol E et al. 2016. An update on cell surface proteins containing extensin-motifs. J. Exp. Bot. 67:2477–87
    [Google Scholar]
  13. 13. 
    Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J et al. 2015. Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLOS Genet 11:7e1005373
    [Google Scholar]
  14. 14. 
    Bourne Y, Abergel C, Cambillau C, Frey M, Rouge P, Fontecilla-Camps JC 1990. X-ray crystal structure determination and refinement at 1.9 Å resolution of isolectin I from the seeds of Lathyrus ochrus. J. Mol. Biol 214:571–84
    [Google Scholar]
  15. 15. 
    Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304.e15
    [Google Scholar]
  16. 16. 
    Brown GD, Willment JA, Whitehead L 2018. C-type lectins in immunity and homeostasis. Nat. Rev. Immunol. 18:6374–89
    [Google Scholar]
  17. 17. 
    Brueggeman R, Druka A, Nirmala J, Cavileer T, Drader T et al. 2008. The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. PNAS 105:14970–75
    [Google Scholar]
  18. 18. 
    Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F et al. 2002. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. PNAS 99:9328–33
    [Google Scholar]
  19. 19. 
    Buendia L, Girardin A, Wang T, Cottret L, Lefebvre B 2018. LysM receptor-like kinase and LysM receptor-like protein families: an update on phylogeny and functional characterization. Front. Plant Sci. 9:1531
    [Google Scholar]
  20. 20. 
    Buist G, Steen A, Kok J, Kuipers OP 2008. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68:838–47
    [Google Scholar]
  21. 21. 
    Chang C, Schaller GE, Patterson SE, Kwok SF, Meyerowitz EM, Bleecker AB 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]
  22. 22. 
    Chen Z. 2001. A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol 126:473–76
    [Google Scholar]
  23. 23. 
    Cheng S, Xian W, Fu Y, Marin B, Keller J et al. 2019. Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179:51057–67
    [Google Scholar]
  24. 24. 
    Choi J, Tanaka K, Cao Y, Qi Y, Qiu J et al. 2014. Identification of a plant receptor for extracellular ATP. Science 343:6168290–94
    [Google Scholar]
  25. 25. 
    Clark SE, Williams RW, Meyerowitz EM 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–85
    [Google Scholar]
  26. 26. 
    Cook DE, Mesarich CH, Thomma BPHJ 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63
    [Google Scholar]
  27. 27. 
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:9537–52
    [Google Scholar]
  28. 28. 
    Czyzewicz N, Nikonorova N, Meyer MR, Sandal P, Shah S et al 2016. The growing story of (ARABIDOPSIS) CRINKLY 4. J. Exp. Bot. 67:164835–47
    [Google Scholar]
  29. 29. 
    Dangl JL, Preuss D, Schroeder JI 1995. Talking through walls: signaling in plant development. Cell 83:1071–77
    [Google Scholar]
  30. 30. 
    Dardick C, Schwessinger B, Ronald P 2012. Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr. Opin. Plant Biol. 15:4358–66
    [Google Scholar]
  31. 31. 
    Day EK, Sosale NG, Lazzara MJ 2016. Cell signaling regulation by protein phosphorylation: a multivariate, heterogeneous, and context-dependent process. Curr. Opin. Biotechnol. 40:185–92
    [Google Scholar]
  32. 32. 
    de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS et al. 2006. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–65
    [Google Scholar]
  33. 33. 
    Deeken R, Kaldenhoff R. 1997. Light-repressible receptor protein kinase: a novel photo-regulated gene from Arabidopsis thaliana. Planta 202:479–86
    [Google Scholar]
  34. 34. 
    Delaux PM, Radhakrishnan GV, Jayaraman D, Cheem J, Malbreil M et al. 2015. Algal ancestor of land plants was preadapted for symbiosis. PNAS 112:13390–95
    [Google Scholar]
  35. 35. 
    Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ et al. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. PNAS 103:11647–52
    [Google Scholar]
  36. 36. 
    Dievart A, Gilbert N, Droc G, Attard A, Gourgues M et al. 2011. Leucine-rich repeat receptor kinases are sporadically distributed in eukaryotic genomes. BMC Evol. Biol. 11:367
    [Google Scholar]
  37. 37. 
    Du S, Qu LJ, Xiao J 2018. Crystal structures of the extracellular domains of the CrRLK1L receptor-like kinases ANXUR1 and ANXUR2. Protein Sci 27:4886–92
    [Google Scholar]
  38. 38. 
    Dufayard JF, Bettembourg M, Fischer I, Droc G, Guiderdoni E et al. 2017. New insights on leucine-rich repeats receptor-like kinase orthologous relationships in angiosperms. Front. Plant Sci. 8:381
    [Google Scholar]
  39. 39. 
    Ebina Y, Ellis L, Jarnagin K, Edery M, Graf L et al. 1985. The human insulin receptor cDNA: the structural basis for hormone-activated transmembrane signalling. Cell 40:747–58
    [Google Scholar]
  40. 40. 
    Fan J, Bai P, Ning Y, Wang J, Shi X et al. 2018. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice. Cell Host Microbe 23:4498–510.E5
    [Google Scholar]
  41. 41. 
    Feuillet C, Reuzeau C, Kjellbom P, Keller B 1998. Molecular characterization of a new type of receptor-like kinase (wlrk) gene family in wheat. Plant Mol. Biol. 37:943–53
    [Google Scholar]
  42. 42. 
    Fischer I, Dievart A, Droc G, Dufayard JF, Chantret N 2016. Evolutionary dynamics of the leucine-rich repeat receptor-like kinase (LRR-RLK) subfamily in angiosperms. Plant Physiol 170:1595–610
    [Google Scholar]
  43. 43. 
    Ge Z, Dresselhaus T, Qu LJ 2019. How CrRLK1L receptor complexes perceive RALF signals. Trends Plant Sci 24:11978–81
    [Google Scholar]
  44. 44. 
    Goldberg JM, Manning G, Liu A, Fey P, Pilcher KE et al. 2006. The dictyostelium kinome–analysis of the protein kinases from a simple model organism. PLOS Genet 2:e38
    [Google Scholar]
  45. 45. 
    Guo Y, Peng D, Zhou J, Lin S, Wang C et al. 2019. iEKPD 2.0: an update with rich annotations for eukaryotic protein kinases, protein phosphatases and proteins containing phosphoprotein-binding domains. Nucleic Acids Res 47:D344–50
    [Google Scholar]
  46. 46. 
    Gust AA, Felix G. 2014. Receptor like proteins associate with SOBIR1-type of adaptors to form bimolecular receptor kinases. Curr. Opin. Plant Biol. 21:104–11
    [Google Scholar]
  47. 47. 
    Hanks SK, Hunter T. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–96
    [Google Scholar]
  48. 48. 
    Hanks SK, Quinn AM, Hunter T 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52
    [Google Scholar]
  49. 49. 
    Hardie DG. 1999. Plant protein serine/threonine kinases: classification and functions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:97–131
    [Google Scholar]
  50. 50. 
    Hashimoto C, Hudson KL, Anderson KV 1988. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52:269–79
    [Google Scholar]
  51. 51. 
    He Y, Zhou J, Shan L, Meng X 2018. Plant cell surface receptor-mediated signaling—a common theme amid diversity. J. Cell Sci. 131:jcs209353
    [Google Scholar]
  52. 52. 
    He ZH, Cheeseman I, He D, Kohorn BD 1999. A cluster of five cell wall-associated receptor kinase genes, Wak1–5, are expressed in specific organs of Arabidopsis. Plant Mol. Biol. 39:1189–96
    [Google Scholar]
  53. 53. 
    He ZH, Fujiki M, Kohorn BD 1996. A cell wall-associated, receptor-like protein kinase. J. Biol. Chem. 271:19789–93
    [Google Scholar]
  54. 54. 
    Hedges SB. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3:838–49
    [Google Scholar]
  55. 55. 
    Herve C, Dabos P, Galaud JP, Rouge P, Lescure B 1996. Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domain. J. Mol. Biol. 258:778–88
    [Google Scholar]
  56. 56. 
    Hirayama T, Oka A. 1992. Novel protein kinase of Arabidopsis thaliana (APK1) that phosphorylates tyrosine, serine and threonine. Plant Mol. Biol. 20:653–62
    [Google Scholar]
  57. 57. 
    Hohmann U, Lau K, Hothorn M 2017. The structural basis of ligand perception and signal activation by receptor kinases. Annu. Rev. Plant Biol. 68:109–37
    [Google Scholar]
  58. 58. 
    Hohmann U, Santiago J, Nicolet J, Olsson V, Spiga FM et al. 2018. Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors. PNAS 115:133488–93
    [Google Scholar]
  59. 59. 
    Hok S, Danchin EG, Allasia V, Panabieres F, Attard A, Keller H 2011. An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. Plant Cell Environ 34:1944–57
    [Google Scholar]
  60. 60. 
    Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978
    [Google Scholar]
  61. 61. 
    Kerk D, Bulgrien J, Smith DW, Gribskov M 2003. Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiol 131:1209–19
    [Google Scholar]
  62. 62. 
    Kim YS, Lee JH, Yoon GM, Cho HS, Park SW et al. 2000. CHRK1, a chitinase-related receptor-like kinase in tobacco. Plant Physiol 123:905–15
    [Google Scholar]
  63. 63. 
    Klymiuk V, Yaniv E, Huang L, Raats D, Fatiukha A et al. 2018. Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family. Nat. Commun. 9:3735
    [Google Scholar]
  64. 64. 
    Kohorn BD. 2016. Cell wall-associated kinases and pectin perception. J. Exp. Bot. 67:2489–94
    [Google Scholar]
  65. 65. 
    Kohorn BD, Lane S, Smith TA 1992. An Arabidopsis serine/threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. PNAS 89:10989–92
    [Google Scholar]
  66. 66. 
    Krattinger SG, Keller B. 2016. Molecular genetics and evolution of disease resistance in cereals. New Phytol 212:2320–32
    [Google Scholar]
  67. 67. 
    Krogh A, Larsson B, von Heijne G, Sonnhammer EL 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567–80
    [Google Scholar]
  68. 68. 
    Kroj T, Chanclud E, Michel-Romiti C, Grand X, Morel JB 2016. Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol 210:2618–26
    [Google Scholar]
  69. 69. 
    Krupa A, Abhinandan KR, Srinivasan N 2004. KinG: a database of protein kinases in genomes. Nucleic Acids Res 32:D153–55
    [Google Scholar]
  70. 70. 
    Krupa A, Anamika, Srinivasan N 2006. Genome-wide comparative analyses of domain organisation of repertoires of protein kinases of Arabidopsis thaliana and Oryza sativa. Gene 380:1–13
    [Google Scholar]
  71. 71. 
    Kutschera A, Dawid C, Gisch N, Schmid C, Raasch L et al. 2019. Bacterial medium-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364:6436178–81
    [Google Scholar]
  72. 72. 
    Kwon A, Scott S, Taujale R, Yeung W, Kochut KJ et al. 2019. Tracing the origin and evolution of pseudokinases across the tree of life. Sci. Signal. 12:578eaav3810
    [Google Scholar]
  73. 73. 
    Labbé J, Muchero W, Czarnecki O, Wang J, Wang X et al. 2019. Mediation of plant-mycorrhizal interaction by a lectin receptor-like kinase. Nat. Plants 5:7676–80
    [Google Scholar]
  74. 74. 
    Lang D, Ullrich KK, Murat F, Fuchs J, Jenkins J et al. 2018. The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93:515–33
    [Google Scholar]
  75. 75. 
    Lee DS, Kim YC, Kwon SJ, Ryu CM, Park OK 2017. The Arabidopsis cysteine-rich receptor-like kinase CRK36 regulates immunity through interaction with the cytoplasmic kinase BIK1. Front. Plant Sci. 8:1856
    [Google Scholar]
  76. 76. 
    Lee JH, Takei K, Sakakibara H, Sun Cho H, Kim DM et al. 2003. CHRK1, a chitinase related receptor-like kinase, plays a role in plant development and cytokinin homeostasis in tobacco. Plant Mol. Biol. 53:6877–90
    [Google Scholar]
  77. 77. 
    Lehti-Shiu MD, Shiu SH. 2012. Diversity, classification and function of the plant protein kinase superfamily. Philos. Trans. R. Soc. B 367:2619–39
    [Google Scholar]
  78. 78. 
    Lehti-Shiu MD, Zou C, Hanada K, Shiu SH 2009. Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26
    [Google Scholar]
  79. 79. 
    Lehti-Shiu MD, Zou C, Shiu SH 2012. Origin, diversity, expansion history, and functional evolution of the plant receptor-like kinase/pelle family. In Receptor-Like Kinases in Plants. Signaling and Communication in Plants 13 F Tax, B Kemmerling 1–22 Berlin: Springer
    [Google Scholar]
  80. 80. 
    Leliaert F, Verbruggen H, Zechman FW 2011. Into the deep: new discoveries at the base of the green plant phylogeny. Bioessays 33:683–92
    [Google Scholar]
  81. 81. 
    Lemieux C, Otis C, Turmel M 2007. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5:2
    [Google Scholar]
  82. 82. 
    Li B, Ferreira MA, Huang M, Camargos LF, Yu X et al. 2019. The receptor-like kinase NIK1 targets FLS2/BAK1 immune complex and inversely modulates antiviral and antibacterial immunity. Nat. Commun. 10:14996
    [Google Scholar]
  83. 83. 
    Li J, Chory J. 1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–38
    [Google Scholar]
  84. 84. 
    Li W, Liu Y, Wang J, He M, Zhou X et al. 2016. The durably resistant rice cultivar Digu activates defence gene expression before the full maturation of Magnaporthe oryzae appressorium. Mol. Plant Pathol. 17:3354–68
    [Google Scholar]
  85. 85. 
    Liang X, Zhou JM. 2018. Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu. Rev. Plant Biol. 69:267–99
    [Google Scholar]
  86. 86. 
    Liebrand TW, van den Burg HA, Joosten MH 2014. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant. Sci. 19:2123–32
    [Google Scholar]
  87. 87. 
    Liener IE. 1964. Seed hemagglutinins. Econ. Bot. 18:27–33
    [Google Scholar]
  88. 88. 
    Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–33
    [Google Scholar]
  89. 89. 
    Limpens E, van Zeijl A, Geurts R 2015. Lipochitooligosaccharides modulate plant host immunity to enable endosymbioses. Annu. Rev. Phytopathol. 53:311–34
    [Google Scholar]
  90. 90. 
    Liu PL, Du L, Huang Y, Gao SM, Yu M 2017. Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evol. Biol. 17:47
    [Google Scholar]
  91. 91. 
    Loh YT, Martin GB. 1995. The disease-resistance gene PTO and the fenthion-sensitivity gene FEN encode closely related functional protein kinases. PNAS 92:4181–84
    [Google Scholar]
  92. 92. 
    Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M et al. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–40
    [Google Scholar]
  93. 93. 
    Maehle A-H. 2004. “Receptive substances”: John Newport Langley (1852–1925) and his path to a receptor theory of drug action. Med. Hist. 48:153–74
    [Google Scholar]
  94. 94. 
    Maehle A-H. 2009. A binding question: the evolution of the receptor concept. Endeavour 33:135–40
    [Google Scholar]
  95. 95. 
    Manning G, Plowman GD, Hunter T, Sudarsanam S 2002. Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 27:514–20
    [Google Scholar]
  96. 96. 
    Manning G, Reiner DS, Lauwaet T, Dacre M, Smith A et al. 2011. The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology. Genome Biol 12:R66
    [Google Scholar]
  97. 97. 
    Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S 2002. The protein kinase complement of the human genome. Science 298:1912–34
    [Google Scholar]
  98. 98. 
    Martin DM, Miranda-Saavedra D, Barton GJ 2009. Kinomer v. 1.0: a database of systematically classified eukaryotic protein kinases. Nucleic Acids Res 37:D244–50
    [Google Scholar]
  99. 99. 
    Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW et al. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–36
    [Google Scholar]
  100. 100. 
    Martinez M. 2016. Computational tools for genomic studies in plants. Curr. Genom. 17:509–14
    [Google Scholar]
  101. 101. 
    McCarty DR, Chory J. 2000. Conservation and innovation in plant signaling pathways. Cell 103:201–9
    [Google Scholar]
  102. 102. 
    Mitchell A, Chang HY, Daugherty L, Fraser M, Hunter S et al. 2015. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res 43:D213–21
    [Google Scholar]
  103. 103. 
    Moussu S, Augustin S, Roman AO, Broyart C, Santiago J 2018. Crystal structures of two tandem malectin-like receptor kinases involved in plant reproduction. Acta Crystallogr. D Struct. Biol. 74:Pt 7671–80
    [Google Scholar]
  104. 104. 
    Nasrallah JB, Kao TH, Chen CH, Goldberg ML, Nasrallah ME 1987. Amino-acid sequence of glycoproteins encoded by three alleles of the S locus of Brassica oleracea. Nature 326:617–19
    [Google Scholar]
  105. 105. 
    Nikonorova N, Vu LD, Czyzewicz N, Gevaert K, De Smet I 2015. A phylogenetic approach to study the origin and evolution of the CRINKLY4 family. Front. Plant Sci. 6:880
    [Google Scholar]
  106. 106. 
    Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:448–64.E24
    [Google Scholar]
  107. 107. 
    Nissen KS, Willats WGT, Malinovsky FG 2016. Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci 21:6516–27
    [Google Scholar]
  108. 108. 
    Pan H, Stonoha-Arther C, Wang D 2018. Medicago plants control nodulation by regulating proteolysis of the receptor-like kinase DMI2. Plant Physiol 177:2792–802
    [Google Scholar]
  109. 109. 
    Pan J, Li Z, Wang Q, Yang L, Yao F, Liu W 2020. An S-domain receptor-like kinase, OsESG1, regulates early crown root development and drought resistance in rice. Plant Sci 290:110318
    [Google Scholar]
  110. 110. 
    Park J, Kim TH, Takahashi Y, Schwab R, Dressano K et al. 2019. Chemical genetic identification of a lectin receptor kinase that transduces immune responses and interferes with abscisic acid signaling. Plant J 98:3492–510
    [Google Scholar]
  111. 111. 
    Pelagio-Flores R, Muñoz-Parra E, Barrera-Ortiz S, Ortiz-Castro R, Saenz-Mata J et al. 2019. The cysteine-rich receptor-like protein kinase CRK28 modulates Arabidopsis growth and development and influences abscisic acid responses. Planta 251:12
    [Google Scholar]
  112. 112. 
    Pruitt RE, Hulskamp M, Kopczak SD, Ploense SE, Schneitz K 1993. Molecular genetics of cell interactions in Arabidopsis. Dev. Suppl 1993:77–84
    [Google Scholar]
  113. 113. 
    Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–92
    [Google Scholar]
  114. 114. 
    Rapp UR, Goldsborough MD, Mark GE, Bonner TI, Groffen J et al. 1983. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus. PNAS 80:4218–22
    [Google Scholar]
  115. 115. 
    Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV 2016. Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8
    [Google Scholar]
  116. 116. 
    Sasaki G, Katoh K, Hirose N, Suga H, Kuma K et al. 2007. Multiple receptor-like kinase cDNAs from liverwort Marchantia polymorpha and two charophycean green algae, Closterium ehrenbergii and Nitella axillaris: extensive gene duplications and gene shufflings in the early evolution of streptophytes. Gene 401:135–44
    [Google Scholar]
  117. 117. 
    Schellenberger R, Touchard M, Clément C, Baillieul F, Cordelier S et al. 2019. Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline. Mol. Plant Pathol. 20:111602–16
    [Google Scholar]
  118. 118. 
    Schlessinger J. 2014. Receptor tyrosine kinases: legacy of the first two decades. Cold Spring Harb. Perspect. Biol. 6:a008912
    [Google Scholar]
  119. 119. 
    Schulze-Muth P, Irmler S, Schröder G, Schröder J 1996. Novel type of receptor-like protein kinase from a higher plant (Catharanthus roseus). cDNA, gene, intramolecular autophosphorylation, and identification of a threonine important for auto- and substrate phosphorylation. J. Biol. Chem. 271:26684–89
    [Google Scholar]
  120. 120. 
    Sessa EB, Banks JA, Barker MS, Der JP, Duffy AM et al. 2014. Between two fern genomes. GigaScience 3:15
    [Google Scholar]
  121. 121. 
    Shiu SH, Bleecker AB. 2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. PNAS 98:10763–68
    [Google Scholar]
  122. 122. 
    Shiu SH, Bleecker AB. 2003. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–43
    [Google Scholar]
  123. 123. 
    Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH 2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–34
    [Google Scholar]
  124. 124. 
    Shumayla SS, Sharma S, Pandey AK, Singh K, Upadhyay SK 2016. Molecular characterization and global expression analysis of lectin receptor kinases in bread wheat (Triticum aestivum). PLOS ONE 11:e0153925
    [Google Scholar]
  125. 125. 
    Silva NF, Goring DR. 2002. The proline-rich, extensin-like receptor kinase-1 (PERK1) gene is rapidly induced by wounding. Plant Mol. Biol. 50:667–85
    [Google Scholar]
  126. 126. 
    Silverstein AM. 2002. Paul Ehrlich's Receptor Immunology: The Magnificent Obsession San Diego, CA: Academic
    [Google Scholar]
  127. 127. 
    Simon A, Glockner G, Felder M, Melkonian M, Becker B 2006. EST analysis of the scaly green flagellate Mesostigma viride (Streptophyta): implications for the evolution of green plants (Viridiplantae). BMC Plant Biol 6:2
    [Google Scholar]
  128. 128. 
    Smakowska-Luzan E, Mott GA, Parys K, Stegmann M, Howton TC et al. 2018. An extracellular network of Arabidopsis leucine-rich repeat receptor kinases. Nature 553:7688342–46
    [Google Scholar]
  129. 129. 
    Snyders S, Kohorn BD. 1999. TAKs, thylakoid membrane protein kinases associated with energy transduction. J. Biol. Chem. 274:9137–40
    [Google Scholar]
  130. 130. 
    Soanes DM, Talbot NJ. 2010. Comparative genome analysis reveals an absence of leucine-rich repeat pattern-recognition receptor proteins in the kingdom Fungi. PLOS ONE 5:e12725
    [Google Scholar]
  131. 131. 
    Song WY, Han Z, Wang J, Lin G, Chai J 2017. Structural insights into ligand recognition and activation of plant receptor kinases. Curr. Opin. Struct. Biol. 43:18–27
    [Google Scholar]
  132. 132. 
    Song WY, Wang GL, Chen LL, Kim HS, Pi LY et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene. Xa21. Science 270:1804–6
    [Google Scholar]
  133. 133. 
    Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A et al. 2017. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:6322287–89
    [Google Scholar]
  134. 134. 
    Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB 1991. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. PNAS 88:8816–20
    [Google Scholar]
  135. 135. 
    Stillmark H. 1889. Uber Ricin. Arch. Pharmakol. Inst. Dorpat. 3:59
    [Google Scholar]
  136. 136. 
    Stracke S, Kistner C, Yoshida S, Mulder L, Sato S et al. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–62
    [Google Scholar]
  137. 137. 
    Takahashi T, Mu JH, Gasch A, Chua NH 1998. Identification by PCR of receptor-like protein kinases from Arabidopsis flowers. Plant Mol. Biol. 37:587–96
    [Google Scholar]
  138. 138. 
    Tamborski J, Krasileva KV. 2020. Evolution of plant NLRs: from natural history to precise modifications. Annu. Rev. Plant Biol. 71: 355–78
    [Google Scholar]
  139. 139. 
    Tang D, Wang G, Zhou JM 2017. Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell 29:618–37
    [Google Scholar]
  140. 140. 
    Teixeira PJ, Costa GG, Fiorin GL, Pereira GA, Mondego JM 2013. Novel receptor-like kinases in cacao contain PR-1 extracellular domains. Mol. Plant Pathol. 14:602–9
    [Google Scholar]
  141. 141. 
    Tobias CM, Howlett B, Nasrallah JB 1992. An Arabidopsis thaliana gene with sequence similarity to the S-locus receptor kinase of Brassica oleracea: sequence and expression. Plant Physiol 99:284–90
    [Google Scholar]
  142. 142. 
    Tordai H, Bányai L, Patthy L 1999. The PAN module: the N-terminal domains of plasminogen and hepatocyte growth factor are homologous with the apple domains of the prekallikrein family and with a novel domain found in numerous nematode proteins. FEBS Lett 461:63–67
    [Google Scholar]
  143. 143. 
    Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R et al. 1996. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8:735–46
    [Google Scholar]
  144. 144. 
    Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S et al. 1992. Acquired resistance in Arabidopsis. Plant Cell 4:645–56
    [Google Scholar]
  145. 145. 
    Ullrich A, Bell JR, Chen EY, Herrera R, Petruzzelli LM et al. 1985. Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes. Nature 313:756–61
    [Google Scholar]
  146. 146. 
    Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A et al. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature 309:418–25
    [Google Scholar]
  147. 147. 
    Vaattovaara A, Brandt B, Rajaraman S, Safronov O, Veidenberg A et al. 2019. Mechanistic insights into the evolution of DUF26-containing proteins in land plants. Commun. Biol. 2:56
    [Google Scholar]
  148. 148. 
    Vaid N, Pandey PK, Tuteja N 2012. Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Mol. Biol. 80:365–88
    [Google Scholar]
  149. 149. 
    Valon C, Smalle J, Goodman HM, Giraudat J 1993. Characterization of an Arabidopsis thaliana gene (TMKL1) encoding a putative transmembrane protein with an unusual kinase-like domain. Plant Mol. Biol. 23:415–21
    [Google Scholar]
  150. 150. 
    van der Wel H, Loeve K 1972. Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth. Eur. J. Biochem. 31:221–25
    [Google Scholar]
  151. 151. 
    Vernié T, Camut S, Camps C, Rembliere C, de Carvalho-Niebel F et al. 2016. PUB1 interacts with the receptor kinase DMI2 and negatively regulates rhizobial and arbuscular mycorrhizal symbioses through its ubiquitination activity in Medicago truncatula. Plant Physiol 170:42312–24
    [Google Scholar]
  152. 152. 
    Vigneron N, Radhakrishnan GV, Delaux PM 2018. What have we learnt from studying the evolution of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 44:49–56
    [Google Scholar]
  153. 153. 
    Walker JC. 1993. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3:451–56
    [Google Scholar]
  154. 154. 
    Walker JC, Zhang R. 1990. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743–46
    [Google Scholar]
  155. 155. 
    Wang C, Huang X, Li Q, Zhang Y, Li JL, Mou Z 2019. Extracellular pyridine nucleotides trigger plant systemic immunity through a lectin receptor kinase/BAK1 complex. Nat. Commun. 10:14810
    [Google Scholar]
  156. 156. 
    Wang X, Zafian P, Choudhary M, Lawton M 1996. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. PNAS 93:2598–602
    [Google Scholar]
  157. 157. 
    Wang Y, Bouwmeester K. 2017. L-type lectin receptor kinases: new forces in plant immunity. PLOS Pathog 13:8e1006433
    [Google Scholar]
  158. 158. 
    Whitewoods C, Cammarata J, Nemec Venza Z, Sang S, Crook A et al. 2018. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr. Biol. 28:2365–76
    [Google Scholar]
  159. 159. 
    Wu F, Chi Y, Jiang Z, Xu Y, Xie L et al. 2020. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578:577–81
    [Google Scholar]
  160. 160. 
    Xi L, Wu XN, Gilbert M, Schulze WX 2019. Classification and interactions of LRR receptors and co-receptors within the Arabidopsis plasma membrane—an overview. Front. Plant Sci. 10:472
    [Google Scholar]
  161. 161. 
    Xiao Y, Stegmann M, Han Z, DeFalco TA, Parys K et al. 2019. Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572:7768270–74
    [Google Scholar]
  162. 162. 
    Xing S, Li M, Liu P 2013. Evolution of S-domain receptor-like kinases in land plants and origination of S-locus receptor kinases in Brassicaceae. BMC Evol. Biol. 13:69
    [Google Scholar]
  163. 163. 
    Yang Y, Labbe J, Muchero W, Yang X, Jawdy SS et al. 2016. Genome-wide analysis of lectin receptor-like kinases in Populus. BMC Genom 17:699
    [Google Scholar]
  164. 164. 
    Yeh YH, Panzeri D, Kadota Y, Huang YC, Huang PY et al. 2016. The Arabidopsis malectin-like/LRR-RLK IOS1 is critical for BAK1-dependent and BAK1-independent pattern-triggered immunity. Plant Cell 28:71701–21
    [Google Scholar]
  165. 165. 
    Zebisch A, Troppmair J. 2006. Back to the roots: the remarkable RAF oncogene story. Cell Mol. Life Sci. 63:1314–30
    [Google Scholar]
  166. 166. 
    Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA et al. 2016. iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol. Plant 9:1667–70
    [Google Scholar]
  167. 167. 
    Zulawski M, Schulze G, Braginets R, Hartmann S, Schulze WX 2014. The Arabidopsis Kinome: phylogeny and evolutionary insights into functional diversification. BMC Genom 15:548
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-073019-025927
Loading
/content/journals/10.1146/annurev-arplant-073019-025927
Loading

Data & Media loading...

Supplementary Data

  • 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