Phosphoproteomic analysis of the non-seed vascular plant model Selaginella moellendorffii

Proteome Science

Volumn 12, Issue 1, 2014, Pages

  Chen, Xi ^a,b   Chan, Wai L ^a   Zhu, Fu Yuan ^a   Lo, Clive ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b Wuhan Institute of Biotechnology   (China)

Author keywords

IMAC; PEG fractionation; Phosphorylation motif; Phosphosites; Selaginella

Indexed keywords

MACROGOL; PHOSPHOPEPTIDE; SERINE; THREONINE; TYROSINE;

ARTICLE; GENETIC CONSERVATION; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; NONHUMAN; PHOTOSYNTHESIS; PHYLOGENY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEOMICS; REGULATORY MECHANISM; SELAGINELLA MOELLENDORFFII; TANDEM MASS SPECTROMETRY;

EID: 84899572145     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-12-16     Document Type: Article

References (76)

1. Kenrick P, Crane PR. The origin and early evolution of plants on land. Nature 1997, 389:33-39.
2. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 2011, 332:960-963. 10.1126/science.1203810, 3166216, 21551031.
3. Wang W, Tanurdzic M, Luo M, Sisneros N, Kim HR, Weng JK, Kudrna D, Mueller C, Arumuganathan K, Carlson J, Chapple C, de Pamphilis C, Mandoli D, Tomkins J, Wing RA, Banks JA. Construction of a bacterial artificial chromosome library from the spikemoss Selaginella moellendorffii: a new resource for plant comparative genomics. BMC Plant Biol 2005, 5:10. 10.1186/1471-2229-5-10, 1177970, 15955246.
4. Banks JA. Selaginella and 400 million years of separation. Annu Rev Plant Biol 2009, 60:223-238. 10.1146/annurev.arplant.59.032607.092851, 19575581.
5. Yin C, Richter U, Borner T, Weihe A. Evolution of phage-type RNA polymerases in higher plants: characterization of the single phage-type RNA polymerase gene from Selaginella moellendorffii. J Mol Evol 2009, 68:528-538. 10.1007/s00239-009-9229-2, 19407923.
6. Hedman H, Kallman T, Lagercrantz U. Early evolution of the MFT-like gene family in plants. Plant Mol Biol 2009, 70:359-369. 10.1007/s11103-009-9478-x, 19288213.
7. Alvarez-Venegas R, Avramova Z. Evolution of the PWWP-domain encoding genes in the plant and animal lineages. BMC Evol Biol 2012, 12:101. 10.1186/1471-2148-12-101, 3457860, 22734652.
8. Tegeder M, Ward JM. Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Sci 2012, 3:21. 3355764, 22645574.
9. Gomez-Porras JL, Riano-Pachon DM, Benito B, Haro R, Sklodowski K, Rodriguez-Navarro A, Dreyer I. Phylogenetic analysis of k(+) transporters in bryophytes, lycophytes, and flowering plants indicates a specialization of vascular plants. Front Plant Sci 2012, 3:167. 3410407, 22876252.
10. Pedersen CN, Axelsen KB, Harper JF, Palmgren MG. Evolution of plant p-type ATPases. Front Plant Sci 2012, 3:31. 3355532, 22629273.
11. Kopriva S, Wiedemann G, Reski R. Sulfate assimilation in basal land plants - what does genomic sequencing tell us?. Plant Biol (Stuttg) 2007, 9:556-564. 10.1055/s-2007-965430, 17853355.
12. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M. The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 2007, 19:3058-3079. 10.1105/tpc.107.051524, 2174699, 17965273.
13. Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K. The evolution of nuclear auxin signalling. BMC Evol Biol 2009, 9:126. 10.1186/1471-2148-9-126, 2708152, 19493348.
14. Rychel AL, Peterson KM, Torii KU. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J Plant Res 2010, 123:275-280. 10.1007/s10265-010-0330-9, 20336477.
15. Eklund DM, Svensson EM, Kost B. Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth. J Exp Bot 2010, 61:1917-1937. 10.1093/jxb/erq080, 20368308.
16. Hanada K, Hase T, Toyoda T, Shinozaki K, Okamoto M. Origin and evolution of genes related to ABA metabolism and its signaling pathways. J Plant Res 2011, 124:455-465. 10.1007/s10265-011-0431-0, 21626211.
17. Smith DR. Unparalleled GC content in the plastid DNA of Selaginella. Plant Mol Biol 2009, 71:627-639. 10.1007/s11103-009-9545-3, 19774466.
18. Shakirov EV, Shippen DE. Selaginella moellendorffii telomeres: conserved and unique features in an ancient land plant lineage. Front Plant Sci 2012, 3:161. 3400083, 22833748.
19. Chan AP, Melake-Berhan A, O'Brien K, Buckley S, Quan H, Chen D, Lewis M, Banks JA, Rabinowicz PD. The highest-copy repeats are methylated in the small genome of the early divergent vascular plant Selaginella moellendorffii. BMC Genomics 2008, 9:282. 10.1186/1471-2164-9-282, 2442089, 18549478.
20. Axtell MJ, Snyder JA, Bartel DP. Common functions for diverse small RNAs of land plants. Plant Cell 2007, 19:1750-1769. 10.1105/tpc.107.051706, 1955733, 17601824.
21. Hecht J, Grewe F, Knoop V. Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: the root of frequent plant mtDNA recombination in early tracheophytes. Genome Biol Evol 2011, 3:344-358. 10.1093/gbe/evr027, 21436122.
22. Novikova O, Smyshlyaev G, Blinov A. Evolutionary genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants. BMC Genomics 2010, 11:231. 10.1186/1471-2164-11-231, 2864245, 20377908.
23. Wang YH, Long CL, Yang FM, Wang X, Sun QY, Wang HS, Shi YN, Tang GH. Pyrrolidinoindoline alkaloids from Selaginella moellendorfii. J Nat Prod 2009, 72:1151-1154. 10.1021/np9001515, 19422203.
24. Wu B, Wang J. Phenolic compounds from Selaginella moellendorfii. Chem Biodivers 2011, 8:1735-1747. 10.1002/cbdv.201000340, 21922662.
25. Cao Y, Tan NH, Chen JJ, Zeng GZ, Ma YB, Wu YP, Yan H, Yang J, Lu LF, Wang Q. Bioactive flavones and biflavones from Selaginella moellendorffii Hieron. Fitoterapia 2010, 81:253-258. 10.1016/j.fitote.2009.09.007, 19775597.
26. Wang HS, Sun L, Wang YH, Shi YN, Tang GH, Zhao FW, Niu HM, Long CL, Li L. Carboxymethyl flavonoids and a monoterpene glucoside from Selaginella moellendorffii. Arch Pharm Res 2011, 34:1283-1288. 10.1007/s12272-011-0807-7, 21910049.
27. Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S. Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 2010, 9:6561-6577. 10.1021/pr100767k, 20923197.
28. Muir T. Posttranslational modification of proteins: expanding nature's inventory: by Christopher T Walsh. Chem Bio Chem 2006, 7:1623-1624.
29. Hubbard MJ, Cohen P. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem Sci 1993, 18:172-177. 10.1016/0968-0004(93)90109-Z, 8392229.
30. Zolnierowicz S, Bollen M. Protein phosphorylation and protein phosphatases: De Panne, Belgium, September 19-24, 1999. EMBO J 2000, 19:483-488. 10.1093/emboj/19.4.483, 305585, 10675316.
31. De la Fuente van Bentem S, Hirt H. Using phosphoproteomics to reveal signalling dynamics in plants. Trends Plant Sci 2007, 12:404-411. 10.1016/j.tplants.2007.08.007, 17765599.
32. Initiative TAG. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815. 10.1038/35048692, 11130711.
33. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934. 10.1126/science.1075762, 12471243.
34. Stone JM, Walker JC. Plant protein kinase families and signal transduction. Plant Physiol 1995, 108:451-457. 10.1104/pp.108.2.451, 157363, 7610156.
35. Des Francs CC, Thiellement H, De Vienne D. Analysis of leaf proteins by two-dimensional gel electrophoresis: protease action as exemplified by ribulose bisphosphate carboxylase/oxygenase degradation and procedure to avoid proteolysis during extraction. Plant Physiol 1985, 78:178-182. 10.1104/pp.78.1.178, 1064698, 16664194.
36. Aryal UK, Krochko JE, Ross AR. Identification of phosphoproteins in Arabidopsis thaliana leaves using polyethylene glycol fractionation, immobilized metal-ion affinity chromatography, two-dimensional gel electrophoresis and mass spectrometry. J Proteome Res 2012, 11:425-437. 10.1021/pr200917t, 22092075.
37. Xi J, Wang X, Li S, Zhou X, Yue L, Fan J, Hao D. Polyethylene glycol fractionation improved detection of low-abundant proteins by two-dimensional electrophoresis analysis of plant proteome. Phytochemistry 2006, 67:2341-2348. 10.1016/j.phytochem.2006.08.005, 16973185.
38. Lee DG, Ahsan N, Lee SH, Kang KY, Lee JJ, Lee BH. An approach to identify cold-induced low-abundant proteins in rice leaf. C R Biol 2007, 330:215-225. 10.1016/j.crvi.2007.01.001, 17434115.
39. Acquadro A, Falvo S, Mila S, Giuliano Albo A, Comino C, Moglia A, Lanteri S. Proteomics in globe artichoke: protein extraction and sample complexity reduction by PEG fractionation. Electrophoresis 2009, 30:1594-1602. 10.1002/elps.200800549, 19425003.
40. Scanff P, Yvon M, Pelissier JP. Immobilized Fe3+ affinity chromatographic isolation of phosphopeptides. J Chromatogr 1991, 539:425-432. 10.1016/S0021-9673(01)83951-0, 2045452.
41. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJ, Slijper M, Menke FL. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 2007, 6:1198-1214. 10.1074/mcp.M600429-MCP200, 17317660.
42. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S. Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 2009, 150:889-903. 10.1104/pp.109.138677, 2689975, 19376835.
43. Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 2010, 153:1161-1174. 10.1104/pp.110.157347, 2899915, 20466843.
44. Meyer LJ, Gao J, Xu D, Thelen JJ. Phosphoproteomic analysis of seed maturation in Arabidopsis, rapeseed, and soybean. Plant Physiol 2012, 159:517-528. 10.1104/pp.111.191700, 3375983, 22440515.
45. Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, Sussman MR, Ane JM, Coon JJ. Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol 2010, 152:19-28. 10.1104/pp.109.149625, 2799343, 19923235.
46. Bi YD, Wang HX, Lu TC, Li XH, Shen Z, Chen YB, Wang BC. Large-scale analysis of phosphorylated proteins in maize leaf. Planta 2011, 233:383-392. 10.1007/s00425-010-1291-x, 21053013.
47. Rudrabhatla P, Reddy MM, Rajasekharan R. Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 2006, 60:293-319. 10.1007/s11103-005-4109-7, 16429265.
48. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189. 10.1101/gr.1224503, 403725, 12952885.
49. Chen F, Mackey AJ, Vermunt JK, Roos DS. Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS One 2007, 2:e383. 10.1371/journal.pone.0000383, 1849888, 17440619.
50. Villen J, Beausoleil SA, Gerber SA, Gygi SP. Large-scale phosphorylation analysis of mouse liver. Proc Natl Acad Sci U S A 2007, 104:1488-1493. 10.1073/pnas.0609836104, 1785252, 17242355.
51. Nuhse TS, Stensballe A, Jensen ON, Peck SC. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 2004, 16:2394-2405. 10.1105/tpc.104.023150, 520941, 15308754.
52. Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 2008, 4:193. 2424297, 18463617.
53. Schwartz D, Gygi SP. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat Biotechnol 2005, 23:1391-1398. 10.1038/nbt1146, 16273072.
54. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659. 10.1093/bioinformatics/btl158, 16731699.
55. Jansson S. The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1994, 1184:1-19. 10.1016/0005-2728(94)90148-1, 8305447.
56. Bellafiore S, Barneche F, Peltier G, Rochaix JD. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 2005, 433:892-895. 10.1038/nature03286, 15729347.
57. Bennett J. Chloroplast phosphoproteins: phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 1979, 99:133-137. 10.1111/j.1432-1033.1979.tb13239.x, 488114.
58. Vener AV, Harms A, Sussman MR, Vierstra RD. Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 2001, 276:6959-6966. 10.1074/jbc.M009394200, 11113141.
59. Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM. State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 2006, 62:779-793. 10.1007/s11103-006-9044-8, 16897465.
60. Vainonen JP, Hansson M, Vener AV. STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 2005, 280:33679-33686. 10.1074/jbc.M505729200, 16040609.
61. Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R. A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem 1995, 270:8474-8481. 10.1074/jbc.270.15.8474, 7721743.
62. Bergantino E, Sandona D, Cugini D, Bassi R. The photosystem II subunit CP29 can be phosphorylated in both C3 and C4 plants as suggested by sequence analysis. Plant Mol Biol 1998, 36:11-22. 10.1023/A:1005904527408, 9484458.
63. Aro EM, Ohad I. Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Signal 2003, 5:55-67. 10.1089/152308603321223540, 12626117.
64. Vener AV. Environmentally modulated phosphorylation and dynamics of proteins in photosynthetic membranes. Biochim Biophys Acta 2007, 1767:449-457. 10.1016/j.bbabio.2006.11.007, 17184728.
65. Rochaix JD. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 2007, 581:2768-2775. 10.1016/j.febslet.2007.04.038, 17470368.
66. Tikkanen M, Nurmi M, Kangasjarvi S, Aro EM. Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 2008, 1777:1432-1437. 10.1016/j.bbabio.2008.08.004, 18774768.
67. Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM. The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 2005, 280:16170-16174. 10.1074/jbc.M501550200, 15722336.
68. Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C. The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J 2007, 49:528-539. 10.1111/j.1365-313X.2006.02976.x, 17217465.
69. Yi X, Hargett SR, Frankel LK, Bricker TM. The PsbQ protein is required in Arabidopsis for photosystem II assembly/stability and photoautotrophy under low light conditions. J Biol Chem 2006, 281:26260-26267. 10.1074/jbc.M603582200, 16822865.
70. Kim ST, Cho KS, Jang YS, Kang KY. Two-dimensional electrophoretic analysis of rice proteins by polyethylene glycol fractionation for protein arrays. Electrophoresis 2001, 22:2103-2109. 10.1002/1522-2683(200106)22:10<2103::AID-ELPS2103>3.0.CO;2-W, 11465512.
71. Chen X, Wu D, Zhao Y, Wong BH, Guo L. Increasing phosphoproteome coverage and identification of phosphorylation motifs through combination of different HPLC fractionation methods. J Chromatogr B Analyt Technol Biomed Life Sci 2011, 879:25-34. 10.1016/j.jchromb.2010.11.004, 21130716.
72. Andrews GL, Simons BL, Young JB, Hawkridge AM, Muddiman DC. Performance characteristics of a new hybrid quadrupole time-of-flight tandem mass spectrometer (TripleTOF 5600). Anal Chem 2011, 83:5442-5446. 10.1021/ac200812d, 3138073, 21619048.
73. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567. 10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2, 10612281.
74. Keller A, Nesvizhskii AI, Kolker E, Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392. 10.1021/ac025747h, 12403597.
75. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003, 75:4646-4658. 10.1021/ac0341261, 14632076.
76. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 2006, 24:1285-1292. 10.1038/nbt1240, 16964243.