Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Tyrosine phosphorylation as a signaling component for plant improvement

  • Park, Youn-Il (Department of Biological Sciences, Chungnam National University) ;
  • Yang, Hyo-Sik (Department of Biology, College of Natural Science, Mokpo National University) ;
  • Oh, Man-Ho (Department of Biological Sciences, Chungnam National University)
  • Received : 2015.10.27
  • Accepted : 2015.11.07
  • Published : 2015.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Plant genome analyses, including Arabidopsis thaliana showed a large gene family of plant receptor kinases with various extracellular ligand-binding domain. Now intensively studies to understand physiological and cellular functions for higher plant receptor kinases in diverse and complex biological processes including plant growth, development, ligands perception including steroid hormone and plant-microbe interactions. Brassinosteroids (BRs) as a one of well know steroid hormone are plant growth hormones that control biomass accumulation and also tolerance to many biotic and abiotic stress conditions and hence are of relevance to agriculture. BRI1 receptor kinase, which is localized in plasma membrane in the cell sense BRs and it bind to a receptor protein known as BRASSINOSTEROID INSENSITIVE 1 (BRI1). Recently, we reported that BRI1 and its co-receptor, BRI1-ASSOCIATED KINASE (BAK1) autophosphorylated on tyrosine residue (s) in vitro and in vivo and thus are dual-specificity kinases. Other plant receptor kinases are also phosphorylated on tyrosine residue (s). Post-translational modifications (PTMs) can be studied by altering the residue modified by directed mutagenesis to mimic the modified state or to prevent the modification. These approaches are useful to not only characterize the regulatory role of a given modification, but may also provide opportunities for plant improvement.

Keywords

References

  1. Albrecht C, Russinova E, Kemmerling B, Kwaaitaal M, and de Vries SC (2008) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE proteins serve brassinosteroid-Dependent and -independent signaling pathways. Plant Physiol 148:611-619 https://doi.org/10.1104/pp.108.123216
  2. Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18:163-192 https://doi.org/10.1146/annurev.cellbio.18.012502.083431
  3. Bentem SF, Hirt H (2009) Protein tyrosine phosphorylation in plants: more abundant than expected? Trends in Plant Science 14:71-76
  4. Blume Y, Yemets A, Sulimenko V, Sulimenko T, Chan J, Lloyd C, Draber P (2008) Tyrosine phosphorylation of plant tubulin. Planta 229:143-150 https://doi.org/10.1007/s00425-008-0816-z
  5. Boller T, Felix, G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379-406 https://doi.org/10.1146/annurev.arplant.57.032905.105346
  6. Cock JM, Vanoosthuyse V, Gaude, T (2002) Receptor kinase signalling in plants and animals: distinct molecular systems with mechanistic similarities. Curr Opin Cell Biol, 14:230-236 https://doi.org/10.1016/S0955-0674(02)00305-8
  7. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629-15634 https://doi.org/10.1073/pnas.0805539105
  8. 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 4:1263-1271 https://doi.org/10.1105/tpc.4.10.1263
  9. Clouse SD (2011) Brassinosteroid signal transduction: From receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219-1230 https://doi.org/10.1105/tpc.111.084475
  10. Clouse SD (2002) Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol Cell 10:973-982 https://doi.org/10.1016/S1097-2765(02)00744-X
  11. Clouse SD, Sasse JM (1998) Brassinosteroids: Essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Bio 49:427-451. https://doi.org/10.1146/annurev.arplant.49.1.427
  12. de Lorenzo L, Merchan F, Laporte P, Thompson R, Clarke J, Sousa C, Crespi M (2009) A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress. Plant Cell 21:668-680 https://doi.org/10.1105/tpc.108.059576
  13. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1-16 https://doi.org/10.1111/j.1365-313X.2005.02592.x
  14. Deeken R, Kaldenhoff R (1997) Light-repressible receptor protein kinase: A novel photo-regulated gene from Arabidopsis thaliana. Planta 202:479-486 https://doi.org/10.1007/s004250050152
  15. Fedina E, Karimova F, Tarchevsky I, Toropygin I, Khripach V. Effect of epibrassinolide on tyrosine phosphorylation of the calvin cycle enzymes. Russ J Plant Physiol 2008; 55:193-200 https://doi.org/10.1134/S1021443708020052
  16. Gendron JM, Wang ZY (2007) Multiple mechanisms modulate brassinosteroid signaling. Curr Opin Plant Biol 10:436-441 https://doi.org/10.1016/j.pbi.2007.08.015
  17. Going DR, Rothstein SJ (1992) The S-locus receptor kinase gene in a self-incompatible Brassica napus line encodes a functional serine/threonine kinase. Plant Cell 4:1273-1281 https://doi.org/10.1105/tpc.4.10.1273
  18. Heldin, C (1995) Dimerization of cell surface receptors in signal transduction. Cell 80:213-224 https://doi.org/10.1016/0092-8674(95)90404-2
  19. He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109-1115 https://doi.org/10.1016/j.cub.2007.05.036
  20. Huang H-J, Lin Y-M, Huang D-D, Takuya Takahashi, Sugiyama M (2003) Protein tyrosine phosphorylation during phytohormonestimulated cell proliferation in Arabidopsis hypocotyls. Plant Cell Physiol 44:770-775 https://doi.org/10.1093/pcp/pcg082
  21. Jinn TL, Stone JM,Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108-117
  22. Karlova R, Boeren S, van Dongen W, Kwaaitaal M, Aker J, Vervoort J, de Vries S (2009) Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 9:368-379 https://doi.org/10.1002/pmic.200701059
  23. Li J, Nam KH (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science 2002; 295:1299-1301
  24. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213-222 https://doi.org/10.1016/S0092-8674(02)00812-7
  25. Matsubayashi Y, Sakagami Y (2006) Peptide hormones in plants. Annu Rev Plant Biol 57:649-674 https://doi.org/10.1146/annurev.arplant.56.032604.144204
  26. Kulaeva ON, Burakhanova EA, Fedina AB (1989) Brassinosteroids regulate protein synthesis in wheat leaves. Dokl Akad Nauk SSSR 305:1277-1279
  27. Mundy J, Schneitz K (2002) Protein phosphorylation in and around signal transduction. Trends in Plant Science 7:54-55
  28. Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C, Roy S, Kadota Y, Oh M-H, Sklenar J, Derbyshire P, Lozano-Duran R, Malinovsky FG, Monaghan J, Menke FL, Huber SC, He SY, Zipfel C (2014) A Bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343:1509-1512 https://doi.org/10.1126/science.1248849
  29. Mu JH, Lee HS, Kao TH (1994) Characterization of a pollenexpressed receptor-like kinase gene of Petunia inflate and the activity of its encoded kinase. Plant Cell 6:709-721 https://doi.org/10.1105/tpc.6.5.709
  30. Nito K, Wong C, Yates III J, Chory J (2013) Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors. Cell Reports 3:1970-1979 https://doi.org/10.1016/j.celrep.2013.05.006
  31. Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for arabidopsis embryonic pattern formation. Dev Cell 12:943-956 https://doi.org/10.1016/j.devcel.2007.04.003
  32. Clay NK, Nelson T (2002) VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell 14:2707-2722. https://doi.org/10.1105/tpc.005884
  33. Oh MH, Wang X, Kota U, Goshe MB, Clouse SD, Huber SC (2009a) Tyrosine phosphorylation of the BRI1 receptor kinase emerges as a component of brassinosteroid signaling in Arabidopsis. Proc Natl Acad Sci USA 106:658-663 https://doi.org/10.1073/pnas.0810249106
  34. Oh MH, Clouse SD, Huber SC (2009) Tyrosine phosphorylation in brassinosteroid signaling. Plant Signaling & Behav 4:1182-1185 https://doi.org/10.4161/psb.4.12.10046
  35. Oh MH, Wang X, Wu X, Zhao Y, Clouse SD, Huber SC (2010) Autophosphorylation of Tyr-610 in the receptor kinase BAK1 plays a role in brassinosteroid signaling and basal defense gene expression. Proc Natl Acad Sci USA 107:17827-17832 https://doi.org/10.1073/pnas.0915064107
  36. Oh MH, Wu X, Clouse SD, Huber SC (2011) Functional importance of BAK1 tyrosine phosphorylation in vivo. Plant Signal and Behav 63:400-405
  37. Oh MH, Ray WK, Huber SC, Asara JM, Gage DA, Clouse SD (2000) Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol 124:751-766 https://doi.org/10.1104/pp.124.2.751
  38. Oh MH, Wu X, Kim SK, Harper JF, Zielinski RE, Clouse SD, and Steven C. Huber (2012) CDPKs are dual-specificity protein kinases and tyrosine autophosphorylation attenuates kinase activity. FEBS Letter 586:4070-4075 https://doi.org/10.1016/j.febslet.2012.09.040
  39. Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/ threonine/ tyrosine-specific protein kinases. Plant Mol Biol 60:293-319. https://doi.org/10.1007/s11103-005-4109-7
  40. Schlessinger J (2000) Cell signaling by receptor tyrosine kinases. Cell 103:211-225 https://doi.org/10.1016/S0092-8674(00)00114-8
  41. Shiu SH, Bleecker AB (2001a) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases.
  42. Shiu SH, Bleecker AB (2001b) Plant receptor-like kinase gene family: Diversity, function and signaling. Sci STKE 113:re22
  43. Shah K, Vervoort J, de Vries SC (2001) Role of threonine in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation. J Biol Chem 276:41263-41269 https://doi.org/10.1074/jbc.M102381200
  44. Shah K, de Vries SC (2001) Role of threonine in the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phosphorylation. J Bio Chem 276:41263-41269 https://doi.org/10.1074/jbc.M102381200
  45. Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama, Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol, 4:193
  46. Tor M, Lotze MT, Holton N (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. J Exp Bot 60:3645-3654. https://doi.org/10.1093/jxb/erp233
  47. Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234:1-46 https://doi.org/10.1016/S0074-7696(04)34001-5
  48. Vert, G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177-201 https://doi.org/10.1146/annurev.cellbio.21.090704.151241
  49. Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis BRASSINOSTEROID-INSENSITIVE1 receptor kinase. Plant Cell 17:1685-1703 https://doi.org/10.1105/tpc.105.031393
  50. Yaffe MB (2002) Phosphotyrosine-binding domains in signal transduction. Nat Rev Mol Cell Biol 3:177-186 https://doi.org/10.1038/nrm759
  51. Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15:220-235 https://doi.org/10.1016/j.devcel.2008.06.011
  52. Zhao D-Z, Wang Z-F, Speal B, Ma H (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 & Development 16:2021-2031 https://doi.org/10.1101/gad.997902