Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Zan, Yanjun ^a   Ji, Yan ^a   Zhang, Yu ^a   Yang, Shaohui ^a   Song, Yingjin ^a   Wang, Jiehua ^a  

^a TIANJIN UNIVERSITY   (China)

Author keywords

Expression profiling; Leucine rich repeat receptor like kinase (LRR RLK); Motif elicitation; Phylogenetic analysis; Populus trichocarpa

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; LEUCINE-RICH REPEAT RECEPTOR-LIKE PROTEIN KINASE, POPULUS; PROTEIN TYROSINE KINASE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; EXON; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC VARIABILITY; INTRON; MULTIGENE FAMILY; NONHUMAN; PHYLOGENY; POPULUS; POPULUS TRICHOCARPA; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; GENE DUPLICATION; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE;

ARABIDOPSIS; FUNGI; POPULUS; POPULUS TRICHOCARPA;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EXONS; GENE DUPLICATION; GENE EXPRESSION PROFILING; INTRONS; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; PHYLOGENY; PLANT PROTEINS; POPULUS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84877266684     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-318     Document Type: Article

References (64)

1. van der Geer P, Hunter T, Lindberg RA. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 1994, 10:251-337. 10.1146/annurev.cb.10.110194.001343, 7888178.
2. Walker JC, Zhang R. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of brassica. Nature 1990, 345(6277):743-746. 10.1038/345743a0, 2163028.
3. Dievart A, Clark SE. Using mutant alleles to determine the structure and function of leucine-rich repeat receptor-like kinases. Curr Opin Plant Biol 2003, 6(5):507-516. 10.1016/S1369-5266(03)00089-X, 12972053.
4. Shiu SH, Bleecker AB. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001, 2001(113):re22.
5. Gou X, He K, Yang H, Yuan T, Lin H, Clouse SD, Li J. Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in arabidopsis thaliana. BMC Genomics 2010, 11:19. 10.1186/1471-2164-11-19, 2817689, 20064227.
6. Afzal AJ, Wood AJ, Lightfoot DA. Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe Interact 2008, 21(5):507-517. 10.1094/MPMI-21-5-0507, 18393610.
7. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y. The arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 1996, 8(4):735-746. 161133, 8624444.
8. Godiard L, Sauviac L, Torii KU, Grenon O, Mangin B, Grimsley NH, Marco Y. ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J 2003, 36(3):353-365. 10.1046/j.1365-313X.2003.01877.x, 14617092.
9. Dievart A, Clark SE. LRR-containing receptors regulating plant development and defense. Development 2004, 131(2):251-261.
10. Mayer KFX, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T. Role of WUSCHEL in regulating stem cell fate in the arabidopsis shoot meristem. Cell 1998, 95(6):805-815. 10.1016/S0092-8674(00)81703-1, 9865698.
11. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G, Laux T. The stem cell population of arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100(6):635-644. 10.1016/S0092-8674(00)80700-X, 10761929.
12. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. Dependence of stem cell fate in arabidopsis on a feedback loop regulated by CLV3 activity. Science 2000, 289(5479):617-619. 10.1126/science.289.5479.617, 10915624.
13. Deyoung BJ, Clark SE. BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 2008, 180(2):895-904. 10.1534/genetics.108.091108, 2567389, 18780746.
14. Walsh B. Population-genetic models of the fates of duplicate genes. Genetica 2003, 118(2-3):279-294.
15. Shiu SH, Bleecker AB. Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in arabidopsis. Plant Physiol 2003, 132(2):530-543. 10.1104/pp.103.021964, 166995, 12805585.
16. Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. Comparative analysis of the receptor-like kinase family in arabidopsis and rice. Plant Cell 2004, 16(5):1220-1234. 10.1105/tpc.020834, 423211, 15105442.
17. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, et al. The genome of black cottonwood, populus trichocarpa (torr. & Gray). Science 2006, 313(5793):1596-1604. 10.1126/science.1128691, 16973872.
18. Dievart A, Gilbert N, Droc G, Attard A, Gourgues M, Guiderdoni E, Perin C. Leucine-rich repeat receptor kinases are sporadically distributed in eukaryotic genomes. BMC Evol Biol 2012, 11:367.
19. Sun X, Wang GL. Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS One 2011, 6(3):e16079. 10.1371/journal.pone.0016079, 3050792, 21408199.
20. 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. 10.1104/pp.108.134353, 2675737, 19321712.
21. Shiu SH, Li WH. Origins, lineage-specific expansions, and multiple losses of tyrosine kinases in eukaryotes. Mol Biol Evol 2004, 21(5):828-840. 10.1093/molbev/msh077, 14963097.
22. Tanaka M, Takahata Y, Nakayama H, Nakatani M, Tahara M. Altered carbohydrate metabolism in the storage roots of sweet potato plants overexpressing the SRF1 gene, which encodes a Dof zinc finger transcription factor. Planta 2009, 230(4):737-746. 10.1007/s00425-009-0979-2, 19618208.
23. Eyuboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer KF, Schneitz K. 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. 10.1186/1471-2229-7-16, 1855328, 17397538.
24. Dolan L. Positional information and mobile transcriptional regulators determine cell pattern in the arabidopsis root epidermis. J Exp Bot 2006, 57(1):51-54.
25. Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 2005, 433(7022):167-171. 10.1038/nature03227, 15650741.
26. van Zanten M, Snoek LB, Proveniers MC, Peeters AJ. The many functions of ERECTA. Trends Plant Sci 2009, 14(4):214-218. 10.1016/j.tplants.2009.01.010, 19303350.
27. Sanchez-Rodriguez C, Estevez JM, Llorente F, Hernandez-Blanco C, Jorda L, Pagan I, Berrocal M, Marco Y, Somerville S, Molina A. The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in arabidopsis thaliana. Mol Plant Microbe Interact 2009, 22(8):953-963. 10.1094/MPMI-22-8-0953, 19589071.
28. Wang Z, Meng P, Zhang X, Ren D, Yang S. BON1 Interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in arabidopsis. Plant J 2011, 67(6):1081-1093. 10.1111/j.1365-313X.2011.04659.x, 21623975.
29. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, McAbee JM, Sarikaya M, Tamerler C, Torii KU. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 2012, 26(2):126-136. 10.1101/gad.179895.111, 3273837, 22241782.
30. 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):508-522. 10.1105/tpc.109.068874, 2845411, 20179141.
31. Krol E, Mentzel T, Chinchilla D, Boller T, Felix G, Kemmerling B, Postel S, Arents M, Jeworutzki E, Al-Rasheid KA, et al. Perception of the arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem 2010, 285(18):13471-13479. 10.1074/jbc.M109.097394, 2859507, 20200150.
32. Gomez-Gomez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in arabidopsis. Mol Cell 2000, 5(6):1003-1011. 10.1016/S1097-2765(00)80265-8, 10911994.
33. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts agrobacterium-mediated transformation. Cell 2006, 125(4):749-760. 10.1016/j.cell.2006.03.037, 16713565.
34. Zhao DZ, Wang GF, Speal B, Ma H. 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 2002, 16(15):2021-2031. 10.1101/gad.997902, 186413, 12154130.
35. Wang J, Tan S, Zhang L, Li P, Tian D. Co-variation among major classes of LRR-encoding genes in two pairs of plant species. J Mol Evol 2011, 72(5-6):498-509.
36. Karve R, Liu W, Willet SG, Torii KU, Shpak ED. The presence of multiple introns is essential for ERECTA expression in arabidopsis. RNA 2011, 17(10):1907-1921. 10.1261/rna.2825811, 3185922, 21880780.
37. Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 2006, 34(Web Server issue):W369-W373. 1538909, 16845028.
38. Padmanabhan M, Cournoyer P, Dinesh-Kumar SP. The leucine-rich repeat domain in plant innate immunity: a wealth of possibilities. Cell Microbiol 2009, 11(2):191-198. 10.1111/j.1462-5822.2008.01260.x, 2762402, 19016785.
39. Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 1994, 19(10):415-421. 10.1016/0968-0004(94)90090-6, 7817399.
40. Ellis J, Dodds P, Pryor T. The generation of plant disease resistance gene specificities. Trends Plant Sci 2000, 5(9):373-379. 10.1016/S1360-1385(00)01694-0, 10973092.
41. Hanks SK, Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 1995, 9(8):576-596.
42. Adams JA. Activation loop phosphorylation and catalysis in protein kinases: is there functional evidence for the autoinhibitor model?. Biochemistry 2003, 42(3):601-607. 10.1021/bi020617o, 12534271.
43. Krupa A, Preethi G, Srinivasan N. Structural modes of stabilization of permissive phosphorylation sites in protein kinases: distinct strategies in Ser/Thr and Tyr kinases. J Mol Biol 2004, 339(5):1025-1039. 10.1016/j.jmb.2004.04.043, 15178245.
44. Dardick C, Ronald P. Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2006, 2(1):e2. 10.1371/journal.ppat.0020002, 1331981, 16424920.
45. Hwang SG, Kim DS, Jang CS. Comparative analysis of evolutionary dynamics of genes encoding leucine-rich repeat receptor-like kinase between rice and arabidopsis. Genetica 2011, 139(8):1023-1032. 10.1007/s10709-011-9604-y, 21879323.
46. Holub EB. The arms race is ancient history in arabidopsis, the wildflower. Nat Rev Genet 2001, 2(7):516-527. 10.1038/35080508, 11433358.
47. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM. Expansion and diversification of the populus R2R3-MYB family of transcription factors. Plant Physiol 2009, 149(2):981-993. 2633813, 19091872.
48. Yim WC, Lee BM, Jang CS. Expression diversity and evolutionary dynamics of rice duplicate genes. Mol Genet Genomics 2009, 281(5):483-493. 10.1007/s00438-009-0425-y, 19184107.
49. Blanc G, Wolfe KH. Functional divergence of duplicated genes formed by polyploidy during arabidopsis evolution. Plant Cell 2004, 16(7):1679-1691. 10.1105/tpc.021410, 514153, 15208398.
50. Chen F, Mackey AJ, Stoeckert CJ, Roos DS. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 2006, 34(Database issue):D363-D368. 1347485, 16381887.
51. Sonnhammer EL, Koonin EV. Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 2002, 18(12):619-620. 10.1016/S0168-9525(02)02793-2, 12446146.
52. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 2012, 40(Database issue):D1178-D1186. 3245001, 22110026.
53. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 2000, 28(1):231-234. 10.1093/nar/28.1.231, 102444, 10592234.
54. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, et al. The pfam protein families database. Nucleic Acids Res 2008, 36(Database issue):D281-D288. 2238907, 18039703.
55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
56. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 2003, 31(13):3497-3500. 10.1093/nar/gkg500, 168907, 12824352.
57. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4(4):406-425.
58. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 1999, 112:531-552.
59. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8(10):785-786. 10.1038/nmeth.1701, 21959131.
60. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580. 10.1006/jmbi.2000.4315, 11152613.
61. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction--the phobius web server. Nucleic Acids Res 2007, 35(Web Server issue):W429-W432. 1933244, 17483518.
62. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190. 10.1101/gr.849004, 419797, 15173120.
63. Sjodin A, Street NR, Sandberg G, Gustafsson P, Jansson S. The populus genome integrative explorer (PopGenIE): a new resource for exploring the populus genome. New Phytol 2009, 182(4):1013-1025. 10.1111/j.1469-8137.2009.02807.x, 19383103.
64. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34(2):374-378.