On the origin and evolution of plant brassinosteroid receptor kinases

Journal of Molecular Evolution

Volumn 78, Issue 2, 2014, Pages 118-129

  Wang, Hao ^a,b   Mao, Hongliang ^a  

^a FUDAN UNIVERSITY   (China)

^b University of Georgia   (United States)

Author keywords

Brassinosteroid; BRI1; Evolution; Gene family; Protein domain

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINOSTEROID; BRI1 PROTEIN, ARABIDOPSIS; PROTEIN KINASE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; EVOLUTION; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY; PLANT GENOME; PROTEIN DOMAIN; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; BRASSINOSTEROIDS; CLUSTER ANALYSIS; GENOME, PLANT; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN KINASES; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84894297954     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-013-9609-5     Document Type: Article

References (67)

1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104
2. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399
3. Andrade MA, Ponting CP, Gibson TJ, Bork P (2000) Homology-based method for identification of protein repeats using statistical significance estimates. J Mol Biol 298:521
4. Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027
5. Brosius J (1991) Retroposons - seeds of evolution. Science 251:753
6. Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341
7. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAL: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972
8. Ceserani T, Trofka A, Gandotra N, Nelson T (2009) VH1/BRL2 receptor-like kinase interacts with vascular-specific adaptor proteins VIT and VIK to influence leaf venation. Plant J 57:1000
9. Chen K, Durand D, Farach-Colton M (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7:429
10. Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D, Takeda K, Takatsuto S, Hoshino T, Watanabe Y (2003) A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol 133:1209
11. Clay NK, Nelson T (2002) VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell 14:2707
12. Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219
13. Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427
14. Derr LK (1998) The involvement of cellular recombination and repair genes in RNA-mediated recombination in Saccharomyces cerevisiae. Genetics 148:937
15. Dolan J, Walshe K, Alsbury S, Hokamp K, O'Keeffe S, Okafuji T, Miller SF, Tear G, Mitchell KJ (2007) The extracellular leucine-rich repeat superfamily; a comparative survey and analysis of evolutionary relationships and expression patterns. BMC Genomics 8:320
16. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792
17. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29
18. Gabaldon T, Koonin EV (2013) Functional and evolutionary implications of gene orthology. Nat Rev Genet 14:360
19. Gibbard RJ, Morley PJ, Gay NJ (2006) Conserved features in the extracellular domain of human toll-like receptor 8 are essential for pH-dependent signaling. J Biol Chem 281:27503
20. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117
21. Holton N, Cano-Delgado A, Harrison K, Montoya T, Chory J, Bishop GJ (2007) Tomato BRASSINOSTEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling. Plant Cell 19:1709
22. Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474:467
23. Kajava AV (1998) Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519
24. Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351
25. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681
26. Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167
27. Kobe B, Kajava AV (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725
28. Koka CV, Cerny RE, Gardner RG, Noguchi T, Fujioka S, Takatsuto S, Yoshida S, Clouse SD (2000) A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol 122:85
29. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309
30. 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
31. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929
32. Lynch VJ, Wagner GP (2008) Resurrecting the role of transcription factor change in developmental evolution. Evolution 62:2131
33. Mathews S (2009) Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. Am J Bot 96:228
34. Matsushima N, Mikami T, Tanaka T, Miyashita H, Yamada K, Kuroki Y (2009) Analyses of non-leucine-rich repeat (non-LRR) regions intervening between LRRs in proteins. Biochim Biophys Acta 1790:1217
35. Matsushima N, Miyashita H, Mikami T, Kuroki Y (2010) A nested leucine rich repeat (LRR) domain: the precursor of LRRs is a ten or eleven residue motif. BMC Microbiol 10:235
36. Matsuzaki M, Misumi O, Shin IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653
37. McCarrey JR, Thomas K (1987) Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326:501
38. Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ (2002) Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14:3163
39. Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460
40. Nakamura A, Fujioka S, Sunohara H, Kamiya N, Hong Z, Inukai Y, Miura K, Takatsuto S, Yoshida S, Ueguchi-Tanaka M, Hasegawa Y, Kitano H, Matsuoka M (2006) The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol 140:580
41. Nehrt NL, Clark WT, Radivojac P, Hahn MW (2011) Testing the ortholog conjecture with comparative functional genomic data from mammals. PLoS Comput Biol 7:e1002073
42. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418
43. Nomura T, Bishop GJ, Kaneta T, Reid JB, Chory J, Yokota T (2003) The LKA gene is a BRASSINOSTEROID INSENSITIVE 1 homolog of pea. Plant J 36:291
44. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253
45. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The PFAM protein families database. Nucleic Acids Res 40:D290
46. Qiu YL, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511
47. Roy SW, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7:211
48. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406
49. She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, Shi S, Yang M, Wang ZY, Chai J (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474:472
50. Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y (2007) Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J Biol Chem 282:124
51. Shiu SH, Bleecker AB (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001:re22
52. Shiu SH, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763
53. Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530
54. 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
55. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688
56. Stanke M, Diekhans M, Baertsch R, Haussler D (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637
57. Sun Y, Fokar M, Asami T, Yoshida S, Allen RD (2004) Characterization of the brassinosteroid insensitive 1 genes of cotton. Plant Mol Biol 54:221-232
58. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609
59. Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140:150
60. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731
61. 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
62. Wang X, Li X, Meisenhelder J, Hunter T, Yoshida S, Asami T, Chory J (2005) Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev Cell 8:855
63. Wang ZY, Bai MY, Oh E, Zhu JY (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701
64. Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106:835
65. Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12:1591
66. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586
67. Zhao DZ, Wang GF, 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 Dev 16:2021