Genome-wide identification and evolutionary analysis of leucine-rich repeat receptor-like protein kinase genes in soybean

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  Zhou, Fulai ^a   Guo, Yong ^a   Qiu, Li Juan ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Evolutionary analysis; Expression profiling; Leucine rich repeat receptor like kinase (LRR RLK); Phylogenetic analysis; Soybean

Indexed keywords

LEUCINE-RICH REPEAT PROTEINS; PROTEIN; PROTEIN KINASE; TRANSCRIPTOME;

ARABIDOPSIS; CLASSIFICATION; CONSERVED SEQUENCE; ENZYMOLOGY; GENE DUPLICATION; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NUCLEOTIDE MOTIF; PHYLOGENY; PLANT GENOME; SOYBEAN;

ARABIDOPSIS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; MULTIGENE FAMILY; NUCLEOTIDE MOTIFS; PHYLOGENY; PROTEIN KINASES; PROTEINS; SOYBEANS; TRANSCRIPTOME;

EID: 84978710379     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-016-0744-1     Document Type: Article

References (83)

1. Walker JC. Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol. 1994;26(5):1599-609.
2. Afzal AJ, Wood AJ, Lightfoot DA. Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe In. 2008;21(5):507-17.
3. Gish LA, Clark SE. The RLK/Pelle family of kinases. Plant J. 2011;66(1):117-27.
4. Johnson KL, Ingram GC. Sending the right signals: regulating receptor kinase activity. Curr Opin Plant Biol. 2005;8(6):648-56.
5. Walker JC, Zhang R. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature. 1990;345(6277):743-6.
6. Braun DM, Walker JC. Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem Sci. 1996;21(2):70-3.
7. Torii KU. Transmembrane receptors in plants: receptor kinases and their ligands. Annu Plant Rev. 2008;33:1-29.
8. Shiu SH, Bleecker AB. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE. 2001;2001(113):re22.
9. Shiu SH, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A. 2001;98(19):10763-8.
10. Zhang XR. Leucine-rich repeat receptor-like kinases in plants. Plant Mol Biol Rep. 1998;16(4):301-11.
11. Dievart A, Clark SE. LRR-containing receptors regulating plant development and defense. Development. 2004;131(2):251-61.
12. Butenko MA, Aalen RB. Receptor ligands in development. In: Tax F, Kemmerling B, editors. Receptor-like kinases in plants: from development to defense. Berlin: Springer; 2012. p. 195-226.
13. Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES 1 and 2 control male sporogenesis. Plant Cell. 2005;17(12):3337-49.
14. Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell. 2005;17(12):3350-61.
15. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, et al. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science. 2007;317(5838):656-60.
16. Hord CLH, Chen CB, DeYoung BJ, Clark SE, Ma H. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell. 2006;18(7):1667-80.
17. Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, et al. Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 2007;50(5):751-66.
18. Zhao DZ, Wang GF, Speal B, Ma H. The EXCESS MICROSPOROCYTES 1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Gene Dev. 2002;16(15):2021-31.
19. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development. 2010;137(22):3911-20.
20. Muller R, Bleckmann A, Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell. 2008;20(4):934-46.
21. He K, Gou XP, Yuan T, Lin HH, Asami T, Yoshida S, et al. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid independent cell-death pathways. Curr Biol. 2007;17(13):1109-15.
22. Nam KH, Li JM. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell. 2002;110(2):203-12.
23. Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K. Leucine-rich repeat receptor-like kinase 1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell. 2005;17(4):1105-19.
24. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, et al. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell. 1996;8(4):735-46.
25. Godiard L, Sauviac L, Torii KU, Grenon O, Mangin B, Grimsley NH, et al. ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J. 2003;36(3):353-65.
26. Dievart A, Gilbert N, Droc G, Attard A, Gourgues M, Guiderdoni E, et al. Leucine-rich repeat receptor kinases are sporadically distributed in eukaryotic genomes. BMC Evol Biol. 2011;11:367.
27. Sun XL, Wang GL. Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS ONE. 2011;6(3):e16079.
28. Zan YJ, Ji Y, Zhang Y, Yang SH, Song YJ, Wang JH. Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genomics. 2013;14:318.
29. Shiu SH, Bleecker AB. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 2003;132(2):530-43.
30. Shiu SH, Karlowski WM, Pan RS, Tzeng YH, Mayer KFX, Li WH. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell. 2004;16(5):1220-34.
31. Hartman GL, West ED, Herman TK. Crops that feed the world 2. Soybean-worldwide production, use, and constraints caused by pathogens and pests. Food Secur. 2011;3(1):5-17.
32. Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278):178-83.
33. Kim KD, Shin JH, Van K, Kim DH, Lee SH. Dynamic rearrangements determine genome organization and useful traits in soybean. Plant Physiol. 2009;151(3):1066-76.
34. Kim S, Kim SJ, Shin YJ, Kang JH, Kim MR, Nam K, et al. An atypical soybean leucine-rich repeat receptor-like kinase, GmLRK1, may be involved in the regulation of cell elongation. Planta. 2009;229(4):811-21.
35. Li XP, Gan R, Li PL, Ma YY, Zhang LW, Zhang R, et al. Identification and functional characterization of a leucine-rich repeat receptor-like kinase gene that is involved in regulation of soybean leaf senescence. Plant Mol Biol. 2006;61(6):829-44.
36. Yang L, Wu KC, Gao P, Liu XJ, Li GP, Wu ZJ. GsLRPK, a novel cold-activated leucine-rich repeat receptor-like protein kinase from Glycine soja, is a positive regulator to cold stress tolerance. Plant Sci. 2014;215:19-28.
37. Kaul S, Koo HL, Jenkins J, Rizzo M, Rooney T, Tallon LJ, et al. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408(6814):796-815.
38. Mainali HR, Chapman P, Dhaubhadel S. Genome-wide analysis of Cyclophilin gene family in soybean (Glycine max). BMC Plant Biol. 2014;14:282.
39. Wang XB, Zhang HW, Gao YL, Sun GL, Zhang WM, Qiu LJ. A comprehensive analysis of the Cupin gene family in soybean (Glycine max). PLoS ONE. 2014;9(10):e110092.
40. Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet. 2011;7(2):e1001312.
41. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002;415(6875):977-83.
42. Fontes EPB, Santos AA, Luz DF, Waclawovsky AJ, Chory J. The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Gene Dev. 2004;18(20):2545-56.
43. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007;448(7152):497-500.
44. Dolan L. Positional information and mobile transcriptional regulators determine cell pattern in the Arabidopsis root epidermis. J Exp Bot. 2006;57(1):51-4.
45. Eyuboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer KFX, et al. Molecular characterisation of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol. 2007;7:16.
46. Kinoshita T, Cano-Delgado AC, Seto H, Hiranuma S, Fujioka S, Yoshida S, et al. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature. 2005;433(7022):167-71.
47. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 2006;45(1):1-16.
48. Etchells JP, Turner SR. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development. 2010;137(5):767-74.
49. Fisher K, Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol. 2007;17(12):1061-6.
50. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell. 2010;22(2):508-22.
51. Xu SL, Rahman A, Baskin TI, Kieber JJ. Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell. 2008;20(11):3065-79.
52. Uchida N, Shimada M, Tasaka M. ERECTA-family receptor kinases regulate stem cell homeostasis via buffering its cytokinin responsiveness in the shoot apical meristem. Plant Cell Physiol. 2013;54(3):343-51.
53. Xu GX, Guo CC, Shan HY, Kong HZ. Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci U S A. 2012;109(4):1187-92.
54. Moore RC, Purugganan MD. The early stages of duplicate gene evolution. Proc Natl Acad Sci U S A. 2003;100(26):15682-7.
55. Leister D. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet. 2004;20(3):116-22.
56. Yu J, Wang J, Lin W, Li SG, Li H, Zhou J, et al. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 2005;3(2):266-81.
57. Blanc G, Wolfe KH. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell. 2004;16(7):1679-91.
58. Yim WC, Lee BM, Jang CS. Expression diversity and evolutionary dynamics of rice duplicate genes. Mol Genet Genomics. 2009;281(5):483-93.
59. Lam HM, Xu X, Liu X, Chen WB, Yang GH, Wong FL, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 2010;42(12):1053-9.
60. Li YH, Zhao SC, Ma JX, Li D, Yan L, Li J, et al. Molecular footprints of domestication and improvement in soybean revealed by whole genome re-sequencing. BMC Genomics. 2013;14:579.
61. Funatsuki H, Ishimoto M, Tsuji H, Kawaguchi K, Hajika M, Fujino K. Simple sequence repeat markers linked to a major QTL controlling pod shattering in soybean. Plant Breed. 2006;125(2):195-7.
62. Zhang D, Cheng H, Wang H, Zhang HY, Liu CY, Yu DY. Identification of genomic regions determining flower and pod numbers development in soybean (Glycine max L.). J Genet Genomics. 2010;37(8):545-56.
63. Liu B, Fujita T, Yan ZH, Sakamoto S, Xu D, Abe J. QTL mapping of domestication-related traits in soybean (Glycine max). Ann Bot. 2007;100(5):1027-38.
64. Yang K, Jeong N, Moon JK, Lee YH, Lee SH, Kim HM, et al. Genetic analysis of genes controlling natural variation of seed coat and flower colors in soybean. J Hered. 2010;101(6):757-68.
65. Li YH, Guan RX, Liu ZX, Ma YS, Wang LX, Li LH, et al. Genetic structure and diversity of cultivated soybean (Glycine max (L.) Merr.) landraces in China. Theor Appl Genet. 2008;117(6):857-71.
66. Gou XP, He K, Yang H, Yuan T, Lin HH, Clouse SD, et al. Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana. BMC Genomics. 2010;11:19.
67. Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(D1):D1178-86.
68. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95-8.
69. Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015;43(D1):D257-60.
70. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(D1):D222-30.
71. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25(24):4876-82.
72. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-9.
73. Hu B, Jin JP, Guo AY, Zhang H, Luo JC, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015;31(8):1296-7.
74. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785-6.
75. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567-80.
76. Kall L, Krogh A, Sonnhammer ELL. Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Res. 2007;35:W429-32.
77. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011;39:W475-8.
78. Lehti-Shiu MD, Zou C, Hanada K, Shiu SH. Evolutionary history and stress regulation of plant receptor-like kinase/Pelle genes. Plant Physiol. 2009;150(1):12-26.
79. Lavin M, Herendeen PS, Wojciechowski MF. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol. 2005;54(4):575-94.
80. Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290(5494):1151-5.
81. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998;95(25):14863-8.
82. -∆∆CT method. Methods. 2001;25(4):402-8.
83. Rousset F. GENEPOP ' 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour. 2008;8(1):103-6.