Abstract
Cold stress adversely affects the growth and development of seedling of spring soybean. Revealing responses in seedling to cold stress at proteomic level will help us to breed cold-tolerant spring soybean cultivars. In this study, to understand the responses, a proteomic analysis on the leaves of seedlings of one cold-tolerant soybean cultivar and one cold-sensitive soybean cultivar at 5 °C for different times (12 and 24 h) was performed, with some proteomic results being further validated by physiological and biochemical analysis. Our results showed that 57 protein spots were found to be significantly changed in abundance and identified by MALDI-TOF/TOF MS. All the identified proteins were found to be involved in 13 metabolic pathways and cellular processes, including photosynthesis, protein folding and assembly, cell rescue and defense, cytoskeletal proteins, transcription and translation regulation, amino acid and nitrogen metabolism, protein degradation, storage proteins, signal transduction, carbohydrate metabolism, lipid metabolism, energy metabolism, and unknown. Based on the majority of the identified cold-responsive proteins, the effect of cold stress on seedling leaves of the two spring soybean cultivars was discussed. The reason that soybean cv. Guliqing is more cold-tolerant than soybean cv. Nannong 513 was due to its more protein, lipid and polyamine biosynthesis, more effective sulfur-containing metabolite recycling, and higher photosynthetic rate, as well as less ROS production and lower protein proteolysis and energy depletion under cold stress. Such a result will provide more insights into cold stress responses and for further dissection of cold tolerance mechanisms in spring soybean.
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Abbreviations
- DAF-2DA:
-
4,5-Diaminofluorescein diacetate
- MOPS:
-
3-(Nmorpholino) propanesulfonic acid
- NO:
-
Nitric oxide
- PPP:
-
Pentose phosphate pathway
- PUT:
-
Putrescine
- ROS:
-
Reactive oxygen species
- SPD:
-
Spermidine
- SPM:
-
Spermine
- Unipro:
-
Unique protein
References
Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484–496
Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2013) Plant plasma membrane proteomics for improving cold tolerance. Front Plant Sci. doi:10.3389/fpls.2013.00090
Sehrawat A, Gupta R, Deswal R (2013) Nitric oxide-cold stress signalling cross-talk, evolution of a novel regulatory mechanism. Proteomics. doi:10.1002/pmic.201200445
Giraldo E, Díaz A, Corral JM, García A (2012) Applicability of 2-DE to assess differences in the protein profile between cold storage and not cold storage in nectarine fruits. J Proteomics 75(18):5774–5782
Rampitsch C, Bykova NV (2012) The beginnings of crop phosphoproteomics: exploring early warning systems of stress. Front Plant Sci 3:144
Zhang S, Feng L, Jiang H, Ma W, Korpelainen H, Li C (2012) Biochemical and proteomic analyses reveal that Populus cathayana males and females have different metabolic activities under chilling stress. J Proteome Res 11(12):5815–5826
Gharechahi J, Alizadeh H, Naghavi MR, Sharifi G (2014) A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.). Mol Biol Rep. doi:10.1007/s11033-014-3257-8
Tambussi EA, Bartoli CG, Guiamet JJ, Beltrano J, Araus JL (2004) Oxidative stress and photodamage at low temperatures in soybean (Glycine max L. Merr.) leaves. Plant Sci 167:19–26
Heerden PDR, Krüger G (2000) Photosynthetic limitation in soybean during cold stress. South Afr J Sci 96:201–206
Posmyk MM, Corbineau F, Vinel D, Bailly C, Come D (2001) Osmoconditioning reduces physiological and biochemical damage induced by chilling in soybean seeds. Physiol Plant 11:473–482
Balestrasse KB, Tomaro ML, Batlle A, Noriega GO (2010) The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71:2038–2045
Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng JR (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5:e1000440
Cui S, Huang F, Wang J, Ma X, Cheng YS, Liu JY (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172
Wang X, Yang P, Zhang X, Xu Y, Kuang TY, Shen SH, He YK (2009) Proteomic analysis of the cold stress response in the moss, Physcomitrella patens. Proteomics 9:4529–4538
Jin Y, Zhang C, Yang H, Yang Y, Huang CJ, Tian Y, Lu XY (2011) Proteomic analysis of cold stress responses in tobacco seedlings. Afr J Biotechnol 10:18991–189004
Rinalducci S, Egidi MG, Karimzadeh G, Jazii FR, Zolla L (2011) Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis 32:1807–1818
Cabané M, Vincens P, Boudet A (1992) Protein synthesis at low temperatures in two soybean cultivars differing by their cold sensitivity. Physiol Plant 85:573–580
Cabané M, Calvet P, Vincens P, Boudet AM (1993) Characterization of chilling-acclimation-related proteins in soybean and identification of one as a member of the heat shock protein (HSP 70) family. Planta 190:346–353
Cheng LB, Gao X, Li SY, Shi MJ, Javeed H, Jing XM, Yang GX, He GY (2010) Proteomic analysis of soybean [Glycine max (L.) Meer.] seeds during imbibition at chilling temperature. Mol Breed 26:1–17
Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209–221
Wang LQ, Ma H, Song LR, Shu YJ, Gu WH (2012) Comparative proteomics analysis reveals the mechanism of pre-harvest seed deterioration of soybean under high temperature and humidity stress. J Proteomics 75:2109–2127
Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatographyl. Plant Physiol 69:701–706
Smith MA, Davies PJ (1985) Separation and quantitation of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol 78:89–91
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Loewus FA (1952) Improvement in anthrone method for determination of carbohydrates. Anal Chem 24:219
Parker R, Flowers TJ, Moore AL, Harpham NVJ (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57:1109–1118
Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93–99
Yao Y, Yang YW, Liu JY (2006) An efficient protein preparation for proteomic analysis of developing cotton fibers by two-dimensional gel electrophoresis. Electrophoresis 27:4559–4569
Madsen O, Sandal L, Sandal NN, Marcker KA (1993) A soybean coproporphyrinogen oxidase gene is highly expressed in root nodules. Plant Mol Biol 23:35–43
Viret JF, Schantz ML, Schantz R (1993) A maize cDNA encoding a type II chlorophyll a/b-binding protein of photosystem II. Plant Physiol 102:1361–1362
Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. PNAS 103:477–482
Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582
Houtz RL, Poneleit L, Jones SB, Royer M, Stults JT (1992) Posttranslational modifications in the amino-terminal region of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase from several plant species. Plant Physiol 98:1170–1174
Hoang CV, Wessler HG, Local A, Turley RB, Benjamin RC, Chapma KD (1999) Identification and expression of cotton (Gossypium hirsutum L.) plastidial carbonic anhydrase. Plant Cell Physiol 40:1262–1270
Goldraij A, Polacco JC (1999) Arginase is inoperative in developing soybean embryos. Plant Physiol 119:297–304
Goldraij A, Polacco JC (2000) Arginine degradation by arginase in mitochondria of soybean seedling cotyledons. Planta 210:652–658
Chen H, McCaig BC, Melotto M, He SY, Howe GA (2004) Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. J Biol Chem 279:45998–46007
Cederbaum SD, Yu H, Grody WW, Kern RM, Yoo P, Iyer RK (2004) Arginases I and II: do their functions overlap? Mol Genet Metab 81(Suppl):S38–S44
Desikan R, Cheung M, Bright J, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212
Lei XY, Zhu RY, Zhang GY, Dai YR (2004) Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: the possible involvement of polyamines. J Pineal Res 36:126–131
Singh V, Evans GB, Lenz DH, Mason JM, Clinch K, Mee S, Painter GF, Tyler PC, Furneaux RH, Lee JE, Howell PL, Schramm VL (2005) Femtomolar transition state analogue inhibitors of 5′-methylthioadenosine/S- adenosylhomocysteine nucleosidase from Escherichia coli. J Biol Chem 280:18265–18273
Waduwara-Jayabahu I, Oppermann Y, Wirtz M, Hull ZT, Schoor S, Plotnikov AN, Hell R, Sauter M, Moffatt BA (2012) Recycling of methylthioadenosine is essential for normal vascular development and reproduction in Arabidopsis. Plant Physiol 158:1728–1744
Lee JE, Cornell KA, Riscoe MK, Howell PL (2001) Structure of E. coli 5′-methylthioadenosine/S- adenosylhomocysteine nucleosidase reveals similarity to the purine nucleoside phosphorylases. Structure 9:941–953
Cameron S, Fyffe SA, Goldie S, Hunter WN (2008) Crystal structures of Toxoplasma gondii pterin-4a-carbinolamine dehydratase and comparisons with mammalian and parasite orthologues. Mol Biochem Parasitol 158:131–138
Noiriel A, Naponelli V, Gregory JF III, Hanson AD (2007) Pterin and folate salvage. Plants and Escherichia coli lack capacity to reduce oxidized pterins. Plant Physiol 143:1101–1109
Gambonnet B, Jabrin S, Ravanel S, Karan M, Douce R, Rébeillé F (2001) Folate distribution during higher plant development. J Sci Food Agric 81:835–841
Ho SL, Tong WF, Yu SM (2000) Multiple mode regulation of a cysteine proteinase gene expression in rice. Plant Physiol 122:57–66
Solomon M, Belenghi B, Delledonne M, Menachem E, Levine A (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11:431–444
Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74
Botella MA, Xu Y, Prabha TN, Zhao Y, Narasimhan ML, Wilson KA, Nielsen SS, Bressan RA, Hasegawa PM (1996) Differential expression of soybean cysteine proteinase inhibitor genes during development and in response to wounding and methyl jasmonate. Plant Physiol 112:1201–1210
Golich FC, Han M, Crowder MW (2006) Over-expression, purification, and characterization of aminopeptidase N from Escherichia coli. Protein Expr Purif 47:634–639
Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Biophys Acta 1699:35–44
Kim J, Mayfield SP (1997) Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 278:1954
Takahashi N, Hayano T, Suzuki M (1989) Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337:473–475
Mills ENC, Marigheto NA, Wellner N, Fairhurst SA, Jenkins JA, Mann R, Belton PS (2003) Thermally induced structural changes in glycinin, the 11S globulin of soya bean (Glycine max)—an in situ spectroscopic study. Biochim Biophys Acta 1648:105–114
Mason HS, Guerrero FD, Boyer JS, Mullet JE (1988) Proteins homologous to leaf glycoproteins are abundant in stems of dark-grown soybean seedlings. analysis of proteins and cDNAs. Plant Mol Biol 11:845–856
Sanabria NM, Dubery IA (2006) Differential display profiling of the Nicotiana response to LPS reveals elements of plant basal resistance. Biochem Biophys Res Commun 344:1001–1007
Xu C, Garrett WM, Sullivan J, Caperna TJ, Natarajan S (2006) Separation and identification of soybean leaf proteins by two-dimensional gel electrophoresis and mass spectrometry. Phytochemistry 67:2431–2440
Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defense responses to the soybean aphid. New Phytol 179:185–195
Thompson JE, Hopkins MT, Taylor C, Wang TW (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 9:174–179
Navaratnam N, Bhattacharya S, Fujino T, Patel D, Jarmuz AL, Scott J (1995) Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell 81:187–195
Bentolila S, Chateigner-Boutin AL, Hanson MR (2005) Ecotype allelic variation in C-to-U editing extent of a mitochondrial transcript identifies RNA-editing quantitative trait loci in Arabidopsis. Plant Physiol 139:2006–2016
Henriques BJ, Fisher MT, Bross P, Gomes CM (2011) A polymorphic position in electron transfer flavoprotein modulates kinetic stability as evidenced by thermal stress. FEBS Lett 585:505–510
Kirkpatrick AS, Yokoyama T, Choi KJ, Yeo HJ (2009) Campylobacter jejuni fatty acid synthase II: structural and functional analysis of [beta]-hydroxyacyl-ACP dehydratase (FabZ). Biochem Biophys Res Commun 380:407–412
Wu Q, Wu J, Sun H, Zhang D, Yu D (2011) Sequence and expression divergence of the AOC gene family in soybean: insights into functional diversity for stress responses. Biotechnol Lett 33:1351–1359
Jeon YH, Bhoo SH, Hahn TR (1998) Molecular characterization of a cDNA encoding chloroplastic fructose-1,6-bisphosphatase from soybean. Mol Cells 8:113–116
Chueca A, Sahrawy M, Pagano EA, Gorgé JL (2002) Chloroplast fructose-1,6-bisphosphatase: structure and function. Photosynth Res 74:235–249
Michelson AM, Markham AF, Orkin SH (1983) Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase. Proc Natl Acad Sci 80:472
Ravelli RB, Gigant B, Curmi PA, Jourdain I, Lachkar S, Sobel A, Knossow M (2004) Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 428:198–202
Briat JF, Lobreaux S, Grignon N, Vansuyt G (1999) Regulation of plant ferritin synthesis: how and why. Cell Mol Life Sci 56:155–166
Attieh J, Djiana R, Koonjul P, Étienne C, Sparace SA, Saini HS (2002) Cloning and functional expression of two plant thiol methyltransferases: a new class of enzymes involved in the biosynthesis of sulfur volatiles. Plant Mol Biol 50:511–521
Acknowledgments
We gratefully acknowledge the partial financial support from the projects supported by the National Natural Science Foundation of China (30971840, 31171572, 31101212, 91117006), the National Key Basic Research Program of China (2010CB134403), the Specialized Research Fund for the Doctoral Program of Higher Education of China (20100097110030, 20120097110025), the Science and Technology Development Foundation of Shanghai Agricultural Academy, China (2000-04-06-3), the Agriculture Science and Technology Fund of the Ministry of Science and Technology, China (02EFN216901241, 04EFN213100094), the Shanghai Committee of Science and Technology, China (093919N1400, 12391900900), and the Priority Academic Program Development of Jiangsu Higher Education Institution for this research.
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Xin Tian, Ying Liu, Zhigang Huang have contributed equally to this work.
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Supplementary 1 2-DE image analysis of seedling leaf proteome of the two soybean cvs Guliqing and Nannong 513 under cold stress and control. (DOCX 2248 kb)
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Tian, X., Liu, Y., Huang, Z. et al. Comparative proteomic analysis of seedling leaves of cold-tolerant and -sensitive spring soybean cultivars. Mol Biol Rep 42, 581–601 (2015). https://doi.org/10.1007/s11033-014-3803-4
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DOI: https://doi.org/10.1007/s11033-014-3803-4