全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Identification of Differentially Expressed Proteins and Phosphorylated Proteins in Rice Seedlings in Response to Strigolactone Treatment

DOI: 10.1371/journal.pone.0093947

Full-Text   Cite this paper   Add to My Lib

Abstract:

Strigolactones (SLs) are recently identified plant hormones that inhibit shoot branching and control various aspects of plant growth, development and interaction with parasites. Previous studies have shown that plant D10 protein is a carotenoid cleavage dioxygenase that functions in SL biosynthesis. In this work, we used an allelic SL-deficient d10 mutant XJC of rice (Oryza sativa L. spp. indica) to investigate proteins that were responsive to SL treatment. When grown in darkness, d10 mutant seedlings exhibited elongated mesocotyl that could be rescued by exogenous application of SLs. Soluble protein extracts were prepared from d10 mutant seedlings grown in darkness in the presence of GR24, a synthetic SL analog. Soluble proteins were separated on two-dimensional gels and subjected to proteomic analysis. Proteins that were expressed differentially and phosphoproteins whose phosphorylation status changed in response to GR24 treatment were identified. Eight proteins were found to be induced or down-regulated by GR24, and a different set of 8 phosphoproteins were shown to change their phosphorylation intensities in the dark-grown d10 seedlings in response to GR24 treatment. Analysis of these proteins revealed that they are important enzymes of the carbohydrate and amino acid metabolic pathways and key components of the cellular energy generation machinery. These proteins may represent potential targets of the SL signaling pathway. This study provides new insight into the complex and negative regulatory mechanism by which SLs control shoot branching and plant development.

References

[1]  Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, et al. (2008) Strigolactone inhibition of shoot branching. Nature 455: 189–194. doi: 10.1038/nature07271
[2]  Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, et al. (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200. doi: 10.1038/nature07272
[3]  Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, et al. (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46: 79–86. doi: 10.1093/pcp/pci022
[4]  Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, et al. (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51: 1019–1029. doi: 10.1111/j.1365-313x.2007.03210.x
[5]  Zou J, Zhang S, Zhang W, Li G, Chen Z, et al. (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48: 687–698. doi: 10.1111/j.1365-313x.2006.02916.x
[6]  Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59: 253–279. doi: 10.1146/annurev.arplant.59.032607.092902
[7]  Beveridge CA, Ross JJ, Murfet IC (1994) Branching mutant rms-2 in Pisum sativum (Grafting studies and endogenous indole-3-acetic acid levels). Plant Physiol 104: 953–959.
[8]  Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea (action of genes Rms3 and Rms4). Plant Physiol 110: 859–865.
[9]  Napoli C (1996) Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol 111: 27–37.
[10]  Morris SE, Turnbull CG, Murfet IC, Beveridge CA (2001) Mutational analysis of branching in pea. Evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol 126: 1205–1213. doi: 10.1104/pp.126.3.1205
[11]  Stirnberg P, van De Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131–1141.
[12]  Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, et al. (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17: 1469–1474. doi: 10.1101/gad.256603
[13]  Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, et al. (2005) The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17: 746–759. doi: 10.1105/tpc.104.027714
[14]  Zou J, Chen Z, Zhang S, Zhang W, Jiang G, et al. (2005) Characterizations and fine mapping of a mutant gene for high tillering and dwarf in rice (Oryza sativa L.). Planta 222: 604–612. doi: 10.1007/s00425-005-0007-0
[15]  Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, et al. (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50: 1416–1424. doi: 10.1093/pcp/pcp091
[16]  Simons JL, Napoli CA, Janssen BJ, Plummer KM, Snowden KC (2007) Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol 143: 697–706. doi: 10.1104/pp.106.087957
[17]  Gao Z, Qian Q, Liu X, Yan M, Feng Q, et al. (2009) Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71: 265–276. doi: 10.1007/s11103-009-9522-x
[18]  Lin H, Wang R, Qian Q, Yan M, Meng X, et al. (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512–1525. doi: 10.1105/tpc.109.065987
[19]  Liu W, Wu C, Fu Y, Hu G, Si H, et al. (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 23: 649–658. doi: 10.1007/s00425-009-0975-6
[20]  Booker J, Auldridge M, Wills S, McCarty D, Klee H, et al. (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14: 1232–1238. doi: 10.1016/j.cub.2004.06.061
[21]  Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, et al. (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348–1351. doi: 10.1126/science.1218094
[22]  Scaffidi A, Waters MT, Ghisalberti EL, Dixon KW, Flematti GR, et al. (2013) Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J 76: 1–9. doi: 10.1111/tpj.12265
[23]  Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, et al. (2013) Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactonesignaling DWARF14. Cell Res 23: 436–439. doi: 10.1038/cr.2013.19
[24]  Kagiyama M, Hirano Y, Mori T, Kim SY, Kyozuka J, et al. (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18: 147–160. doi: 10.1111/gtc.12025
[25]  Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, et al. (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22: 1–5. doi: 10.1016/j.cub.2012.08.007
[26]  Yamaguchi S, Kyozuka J (2010) Branching hormone is busy both underground and overground. Plant Cell Physiol 51: 1091–1094. doi: 10.1093/pcp/pcq088
[27]  Cardoso C, Ruyter-Spira C, Bouwmeester HJ (2011) Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci 180: 414–420. doi: 10.1016/j.plantsci.2010.11.007
[28]  Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host–parasitic plant interactions. Curr Opin Plant Biol 6: 358–364. doi: 10.1016/s1369-5266(03)00065-7
[29]  Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18: 72–83. doi: 10.1016/j.tplants.2012.10.003
[30]  Mayzlish-Gati E, De Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, et al. (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160: 1329–1341. doi: 10.1104/pp.112.202358
[31]  Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, et al. (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976–1987. doi: 10.1104/pp.111.187104
[32]  Yan H, Saika H, Maekawa M, Takamure I, Tsutsumi N, et al. (2007) Rice tillering dwarf mutant dwarf3 has increased leaf longevity during darkness-induced senescence or hydrogen peroxide-induced cell death. Genes Genet Syst 82: 361–366. doi: 10.1266/ggs.82.361
[33]  Mashiguchi K, Sasaki E, Shimada Y, Nagae M, Ueno K, et al. (2009) Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci Biotechnol Biochem 73: 2460–2465. doi: 10.1271/bbb.90443
[34]  Jones AM, Cochran DS, Lamerson PM, Evans ML, Cohen JD (1991) Red light-regulated growth: 1. Changes in the abundance of indoleacetic acid and a 22-kilodalton auxin-binding protein in the maize mesocotyl. Plant Physiol 97: 352–358. doi: 10.1104/pp.97.1.352
[35]  Sawers RJ, Linley PJ, Farmer PR, Hanley NP, Costich DE, et al. (2002) elongated mesocotyl1, a phytochrome-deficient mutant of maize. Plant Physiol 130: 155–163. doi: 10.1104/pp.006411
[36]  Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, et al. (2002) Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130: 1152–1161. doi: 10.1104/pp.007179
[37]  Choi D, Lee Y, Cho H, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15: 1386–1398. doi: 10.1105/tpc.011965
[38]  Hu Z, Yan H, Yang J, Yamaguchi S, Maekawa M, et al. (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51: 1136–1142. doi: 10.1093/pcp/pcq075
[39]  O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007–4021.
[40]  Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071–2077. doi: 10.1002/elps.1150181133
[41]  Lewis TS, Hunt JB, Aveline LD, Jonscher KR, Louie DF, et al. (2000) Identification of novel MAP kinase pathway signaling targets by functional proteomics and mass spectrometry. Mol Cell 6: 1343–1354. doi: 10.1016/s1097-2765(00)00132-5
[42]  Deng Z, Zhang X, Tang W, Oses-Prieto JA, Suzuki N, et al. (2007) A proteomics study of brassinosteroid response in Arabidopsis. Mol Cell Proteomics 6: 2058–2071. doi: 10.1074/mcp.m700123-mcp200
[43]  Tang W, Deng Z, Oses-Prieto JA, Suzuki N, Zhu S, et al. (2008a) Proteomics studies of brassinosteroid signal transduction using prefractionation and two-dimensional DIGE. Mol Cell Proteomics 7: 728–738. doi: 10.1074/mcp.m700358-mcp200
[44]  Tang W, Kim TW, Oses-Prieto JA, Sun Y, Deng Z, et al. (2008b) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321: 557–560. doi: 10.1126/science.1156973
[45]  Kaufmann H, Bailey JE, Fussenegger M (2001) Use of antibodies for detection of phosphorylated proteins separated by two-dimensional gel electrophoresis. Proteomics 1: 194–199. doi: 10.1002/1615-9861(200102)1:2<194::aid-prot194>3.3.co;2-b
[46]  Chen F, Jiang L, Zheng J, Huang R, Wang H, et al. (2013) Identification of a cosegregative protein with the tillering trait in rice (Oryza sativa L.). Plant Omics J 6: 36–45.
[47]  He H, Li J (2008) Proteomic analysis of phosphoproteins regulated by abscisic acid in rice leaves. Biochem Biophys Res Commun 371: 883–888. doi: 10.1016/j.bbrc.2008.05.001
[48]  Ke Y, Han G, He H, Li J (2009) Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochem Biophys Res Commun 379: 133–138. doi: 10.1016/j.bbrc.2008.12.067
[49]  Moffatt BA, Stevens YY, Allen MS, Snider JD, Pereira LA, et al. (2002) Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation. Plant Physiol 128: 812–821. doi: 10.1104/pp.010880
[50]  Chitteti BR, Peng ZH (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6: 1718–1727. doi: 10.1021/pr060678z
[51]  Roth JR, Lawrence JG, Bobik TA (1996) Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol 50: 137–181. doi: 10.1146/annurev.micro.50.1.137
[52]  Warren MJ, Raux E, Schubert HL, Escalante-Semerena JC (2002) The biosynthesis of adenosylcobalamin (vitamin B12). Nat Prod Rep19: 390–412. doi: 10.1039/b108967f
[53]  Hondorp ER, Matthews RG (2004) Oxidative stress inactivates cobalamin-independent methionine synthase (MetE) in Escherichia coli. PLoS Biol 2: e336. doi: 10.1371/journal.pbio.0020336
[54]  Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221–227. doi: 10.1093/jxb/erl164
[55]  Zegzouti H, Jones B, Marty C, Lelièvre JM, Latché A, et al. (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35: 847–854.
[56]  Komatsu S, Muhammad A, Rakwal R (1999) Separation and characterization of proteins from green and etiolated shoots of rice (Oryza sativa L.): Towards a rice proteome. Electrophoresis 20: 630–636. doi: 10.1002/(sici)1522-2683(19990301)20:3<630::aid-elps630>3.3.co;2-q
[57]  Capobianco L, Brandolin G, Palmieri F (1991) Transmembrane topography of the mitochondrial phosphate carrier explored by peptide-specific antibodies and enzymatic digestion. Biochem J 30: 4963–4969. doi: 10.1021/bi00234a018
[58]  Palmieri F, Bisaccia F, Capobianco L, Dolce V, Fiermonte G, et al. (1993) Transmembrane topology, genes and biogenesis of the mitochondrial phosphate and oxoglutarate carriers. J Bioenerg Biomembr 25: 493–501. doi: 10.1007/bf01108406
[59]  Stappen R, Kramer R (1994) Kinetic mechanism of phosphate/phosphate and phosphate/OH-antiport catalyzed by reconstituted phosphate carrier from beef heart mitochondria. J Biol Chem 269: 11240–11246.
[60]  Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51: 1118–1126. doi: 10.1093/pcp/pcq084
[61]  Komatsu S, Hirano H (1993) Protein kinase activity and protein phosphorylation in rice (Oryza sativa L.) leaf. Plant Sci 94: 127–137. doi: 10.1016/0168-9452(93)90014-q
[62]  Gomi K, Matsuoka M (2003) Gibberellin signalling pathway. Curr Opin Plant Biol 6: 489–493. doi: 10.1016/s1369-5266(03)00079-7
[63]  Khan M, Jan A, Karibe H, Komatsu S (2005) Identification of phosphoproteins regulated by gibberellin in rice leaf sheath. Plant Mol Biol 58: 27–40. doi: 10.1007/s11103-005-4013-1
[64]  Qian W, Yu C, Qin H, Liu X, Zhang A, et al. (2007) Molecular and functional analysis of phosphomannomutase (PMM) from higher plants and genetic evidence for the involvement of PMM in ascorbic acid biosynthesis in Arabidopsis and Nicotiana benthamiana. Plant J 49: 399–413. doi: 10.1111/j.1365-313x.2006.02967.x
[65]  Hoeberichts FA, Vaeck E, Kiddle G, Coppens E, van-de-Cotte B, et al. (2008) A temperature-sensitive mutation in the Arabidopsis thaliana phosphomannomutase gene disrupts protein glycosylation and triggers cell death. J Biol Chem 283: 5708–5718. doi: 10.1074/jbc.m704991200
[66]  Rate DN, Greenberg JT (2001) The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J 27: 203–211. doi: 10.1046/j.0960-7412.2001.1075umedoc.x
[67]  Song JT, Lu H, Greenberg JT (2004) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16: 353–366. doi: 10.1105/tpc.019372
[68]  Gao J, Agrawal GK, Thelen JJ, Xu D (2009) P3DB: a plant protein phosphorylation database. Nucleic Acids Res 37: D960–D962. doi: 10.1093/nar/gkn733
[69]  Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, et al. (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153: 1161–1174. doi: 10.1104/pp.110.157347
[70]  Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, et al. (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4: 193. doi: 10.1038/msb.2008.32
[71]  Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, et al. (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150: 889–903. doi: 10.1104/pp.109.138677
[72]  Engelsberger WR, Schulze WX (2012) Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings. Plant J 69: 978–995. doi: 10.1111/j.1365-313x.2011.04848.x
[73]  Rose CM, Venkateshwaran M, Volkening JD, Grimsrud PA, Maeda J, et al. (2012) Rapid phosphoproteomic and transcriptomic changes in the rhizobia-legume symbiosis. Mol Cell Proteomics 11: 724–744. doi: 10.1074/mcp.m112.019208
[74]  Mayank P, Grossman J, Wuest S, Boisson-Dernier A, Roschitzki B, et al. (2012) Characterization of the phosphoproteome of mature Arabidopsis pollen. Plant J 72: 89–101. doi: 10.1111/j.1365-313x.2012.05061.x
[75]  Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, et al. (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol 152: 19–28. doi: 10.1104/pp.109.149625
[76]  Melo-Braga MN, Verano-Braga T, León IR, Antonacci D, Nogueira FC, et al. (2012) Modulation of protein phosphorylation, N-glycosylation and Lys-acetylation in grape (Vitis vinifera) mesocarp and exocarp owing to Lobesia botrana infection. Mol Cell Proteomics 11: 945–956. doi: 10.1074/mcp.m112.020214
[77]  Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11: e1001474. doi: 10.1371/journal.pbio.1001474
[78]  Delaux P, Xie X, Timme R, Peuech-Pages V, Dunand C, et al. (2012) Origin of strigolactones in the green lineage. New Phytol 195: 857–871. doi: 10.1111/j.1469-8137.2012.04209.x
[79]  Waters MT, Smith SM, Nelson DC (2011) Smoke signals and seed dormancy: where next for MAX2? Plant Sig Behav 6: 1418–1422. doi: 10.4161/psb.6.9.17303
[80]  Somers DE, Fujiwara S (2009) Thinking outside the F-box: novel ligands for novel receptors. Trends Plant Sci 14: 206–213. doi: 10.1016/j.tplants.2009.01.003
[81]  Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21: R338–R345. doi: 10.1016/j.cub.2011.02.036
[82]  Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, et al. (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108: 8897–8902. doi: 10.1073/pnas.1100987108
[83]  Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, et al. (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285–1295. doi: 10.1242/dev.074567
[84]  Jiang L, Liu X, Xiong G, Liu H, Chen F, et al. (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401–405. doi: 10.1038/nature12870
[85]  Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, et al. (2013) D14-SCFD3-dependent degradation of D53 regulates strigolactone signaling. Nature 504: 406–410. doi: 10.1038/nature12878
[86]  Hsu YT, Kao CH (2005) Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiol Plant 124: 71–80. doi: 10.1111/j.1399-3054.2005.00490.x
[87]  Damerval C, de Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic-variation detected in wheat-seedling proteins. Electrophoresis 7: 52–54. doi: 10.1002/elps.1150070108

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133