Abstract
Cell surface receptors located in the plasma membrane have a prominent role in the initiation of cellular signalling. Recent evidence strongly suggests that plant cells carry cell surface receptors with intrinsic protein kinase activity. The plant receptor-like protein kinases (RLKs) are structurally related to the polypeptide growth factor receptors of animals which consist of a large extracytoplasmic domain, a single membrane spanning segment and a cytoplasmic domain of the protein kinase gene family. Most of the animal growth factor receptor protein kinases are tyrosine kinases; however, the plant RLKs all appear to be serine/threonine protein kinases. Based on structural similarities in their extracellular domains the RLKs fall into three categories: the S-domain class, related to the self-incompatibility locus glycoproteins of Brassica; the leucine-rich repeat class, containing a tandemly repeated motif that has been found in numerous proteins from a variety of eukaryotes; and a third class that has epidermal growth factor-like repeats. Distinct members of these putative receptors have been found in both monocytyledonous plants such as maize and in members of the dicotyledonous Brassicaceae. The diversity among plant RLKs, reflected in their structural and functional properties, has opened up a broad new area of investigation into cellular signalling in plants with far-reaching implications for the mechanisms by which plant cells perceive and respond to extracellular signals.
Similar content being viewed by others
References
Ahn NG, Seger R, Krebs EG: The mitogen-activated protein kinase activator. Curr Biol 4: 992–999 (1992).
Banno H, Hirano K, Nakamura T, Irie K, Nomoto S, Matsumoto K, Machida Y: NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Mol Cell Biol 13: 4745–4752 (1993).
Benson D, Lipman DJ, Ostell J: GenBank. Nucl Acid Res 21: 2963–2965 (1993).
Chang C, Schaller GE, Patterson SE, Kwok SF, Meyerowitz EM, Bleecker AB: The TMK1 gene from Arabidopsis codes for a protein with structural and biochemical characteristics of a receptor protein kinase. Plant Cell 4: 1263–1271 (1992).
Crews CM, Erikson RL: Extracellular signals and reversible protein phosphorylation. What to Mek of it all. Cell 74: 215–217 (1993).
Davis CG: The many faces of epidermal growth factor repeats. New Biol 2: 410–419 (1990).
Duerr B, Gawienowski M, Ropp T, Jacobs T: MsERK1: A mitogen-activated protein kinase from a flowering plant. Plant Cell 5: 87–96 (1993).
Fantl WJ, Johnson DE, Williams LT: Signalling by receptor tyrosine kinases. Annu Rev Biochem 62: 453–481 (1993).
Feng GS, Hui CC, Pawson T: SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases. Science 259: 1607–1611 (1993).
Goring DR, Glavin TL, Schafer U, Rothstein SJ: An S receptor kinase gene in self-compatible Brassica napus has a 1-bp deletion. Plant Cell 5: 531–539 (1993).
Goring DR, Rothstein SJ: The S-locus receptor kinase gene in a self-incompatible Brassica napus line encodes a functional serine/threonine kinase. Plant Cell 4: 1273–1281 (1992).
Hanks SK, Quinn AM: Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family members. Meth Enzymol 200: 38–61 (1991).
Hanks SK, Quinn AM, Hunter T: The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52 (1988).
Harper JF, Sussman MR, Schaller GE, Putnam-Evans C, Charbonneau H, Harmon AC: A calcium-dependent protein-kinase with a regulatory domain similar to calmodulin. Science 252: 951–954 (1991).
Heldin C-H: SH2 domains: elements that control protein interactions during signal transduction. Trends Biochem Sci 16: 450–452 (1991).
Jonak C, Pay A, Bogre L, Hirt H, Heberle-Bors E: The plant homologue of MAP kinase is expressed in a cell-cycle dependent and organ-specific manner. Plant J 3: 611–617 (1993).
Kieber JJ, Ecker JR: Ethylene gas: it's not just for ripening any more. Trends Genet 9: 356–362 (1993).
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR: CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72: 427–441 (1993).
Kobe B, Deisenhofer J: Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 366: 751–756 (1993).
Kohorn BD, Fujiki M: A family of proteins containing a serine/threonine kinase and/or an EGF repeat hasmembers in the plasma membrane and chloroplast. Fifth International Conference on Arabidopsis Research (1993).
Kohorn BD, Lane S, Smith TA: An Arabidopsis serine/threonine kinase homologue with an epidermal growth factor repeat selected in yeast for its specificity for a thylakoid membrane protein. Proc Natl Acad Sci USA 89: 10989–10992 (1992).
Kumar V, Trick M: Sequence complexity of the S-receptor kinase gene family in Brassica. Mol Gen Genet 241: 440–446 (1993).
Lawton MA, Yamamoto RT, Hanks SK, Lamb CJ: Molecular cloning of plant transcripts encoding protein kinase homologs. Proc Natl Acad Sci USA 86: 3140–3144 (1989).
Ma H: Protein phosphorylation in plants: enzymes, substrates and regulators. Trends Genet 9: 228–230 (1993).
Massague J: Receptors for the TGF-β family. Cell 69: 1067–1070 (1992).
Mizoguchi T, Gotoh Y, Nishida E, Yamaguchi-Shinozaki K, Hayashida N, Iwasaki T, Kamada H, Shinozaki K: Characterization of two cDNAs that encode MAP kinase homologues in Arabidopsis thaliana and analysis of the possible role of auxin in activating such kinase activities in cultured cells. Plant J 5: 111–122 (1994).
Moodie SA, Wolfman A: the 3Rs of life: Ras, Raf and growth regulation. Trends Genet 10: 44–48 (1994).
Nasrallah JB, Nasrallah ME: Pollen-stigma signalling in the sporophytic self-incompatibility response. Plant Cell 5: 1325–1335 (1993).
Nasrallah JB, Rundle SJ, Nasrallah ME: Genetic evidence for the requirement of the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J 5: 373–384 (1994).
Neiman AM: Conservation and reiteration of a kinase cascade. Trends Genet 9: 390–394 (1993).
Pawson T, Gish GD: SH2 and SH3 domains: from structure to function. Cell 71: 359–362 (1992).
Pearce G, Strydom D, Johnson S, Ryan CA: A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253: 895–898 (1991).
Schaller GE, Bleecker AB: Receptor-like kinase activity in membranes of Arabidopsis thaliana. FEBS Lett 333: 306–310 (1993).
Schlessinger J: How receptor tyrosine kinases activate ras. Trends Biochem Sci 18: 273–275 (1993).
Schneider R, Schweiger M: A novel modular mosaic of cell adhesion motifs in the extracellular domains of the neurogenic trk and trkB tyrosine kinase receptors. Oncogene 6: 1807–1811 (1991).
Siegelman MH, Cheng IC, Weissman IL, Wakeland EK: The mouse lymph node homing receptor is identical with the lymphocyte cell surface marker Ly22: role of the EGF domain in endothelial binding. Cell 61: 611–622 (1990).
Singer SJ: The structure and insertion of integral protein in membranes. Annu Rev Cell Biol 6: 247–296 (1990).
Smith RD, Walker JC: Isolation and expression of a maize type 1 protein phosphatase. Plant Physiol 97: 677–683 (1991).
Smith RS, Walker JC: Expression of multiple type 1 phosphoprotein phosphatases in Arabidopsis thaliana. Plant Mol Biol 21: 307–316 (1993).
Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB: Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 88: 8816–8820 (1991).
Stein JC, Nasrallah JB: A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol 101: 1103–1106 (1993).
Taylor SS, Knighton DR, Zheng J, TenEyck LF, Sowadski JM: Structural framework for the protein kinase family. Annu Rev Cell Biol 8: 429–462 (1992).
Tobias CM, Howlett B, Nasrallah JB: An Arabidopsis thaliana gene with sequence similarity to the S-Locus receptor kinase of Brassica oleracea. Plant Physiol 99: 284–290 (1992).
Ullrich A, Schlessinger J: Signal transduction by receptors with tyrosine kinase activity. Cell 61: 203–212 (1990).
Valon C, Smalle J, Goodman HM, Giraudat J: Characterization of an Arabidopsis thaliana gene (TMKL1) encoding a putative transmembrane protein with an unusual kinase-like domain. Plant Mol Biol 23: 415–421 (1993).
Walker JC: Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3: 451–456 (1993).
Walker JC, Zhang R: Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345: 743–746 (1990).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Walker, J.C. Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26, 1599–1609 (1994). https://doi.org/10.1007/BF00016492
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00016492