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Proteomic responses of drought-tolerant and drought-sensitive cotton varieties to drought stress

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Abstract

Drought, one of the most widespread factors reducing agricultural crop productivity, affects biological processes such as development, architecture, flowering and senescence. Although protein analysis techniques and genome sequencing have made facilitated the proteomic study of cotton, information on genetic differences associated with proteomic changes in response to drought between different cotton genotypes is lacking. To determine the effects of drought stress on cotton seedlings, we used two-dimensional polyacrylamide gel electrophoresis (2-DE) and matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) mass spectrometry to comparatively analyze proteome of drought-responsive proteins during the seedling stage in two cotton (Gossypium hirsutum L.) cultivars, drought-tolerant KK1543 and drought-sensitive Xinluzao26. A total of 110 protein spots were detected on 2-DE maps, of which 56 were identified by MALDI-TOF and MALDI-TOF/TOF mass spectrometry. The identified proteins were mainly associated with metabolism (46.4 %), antioxidants (14.2 %), and transport and cellular structure (23.2 %). Some key proteins had significantly different expression patterns between the two genotypes. In particular, 5-methyltetrahydropteroyltriglutamate-homocysteine methyltransferase, UDP-d-glucose pyrophosphorylase and ascorbate peroxidase were up-regulated in KK1543 compared with Xinluzao26. Under drought stress conditions, the vacuolar H+-ATPase catalytic subunit, a 14-3-3g protein, translation initiation factor 5A and pathogenesis-related protein 10 were up-regulated in KK1543, whereas ribosomal protein S12, actin, cytosolic copper/zinc superoxide dismutase, protein disulfide isomerase, S-adenosylmethionine synthase and cysteine synthase were down-regulated in Xinluzao26. This work represents the first characterization of proteomic changes that occur in response to drought in roots of cotton plants. These differentially expressed proteins may be related to biochemical pathways responsible for drought tolerance in KK1543. Although further studies are needed, this proteomic analysis underlines the role of post-translational events. The differentially expressed proteins and their corresponding genes may be used as markers for the breeding of drought tolerance in cotton.

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References

  • Alam I, Lee DG, Kim KH, Park CH, Sharmin SA, Lee H, Oh KW, Yun BW, Lee BH (2010) Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage. J Biosci 35(1):49–62

    Article  CAS  PubMed  Google Scholar 

  • Ali GM, Komatsu S (2006) Proteomic analysis of rice leaf sheath during drought stress. J Proteome Res 5(2):396–403

    Article  CAS  PubMed  Google Scholar 

  • Armbruster BL, Wunderli H, Turner BM, Raska I, Kellenberger E (1983) Immunocytochemical localizition of cytoskeletal proteins and his tone 2B in isolated membrane-depleted nuclei, metaphase chromatin, and whole chinese ham sterovary cells. J Histochem Cytochem 31(12):1358–1393

    Google Scholar 

  • Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes-intergrating cell survival and death. J Biosci 32(3):595–610

    Article  CAS  PubMed  Google Scholar 

  • Barkla BJ, Vera-Estrella R, Maldonado-Gama M, Pantoja O (1999) Abscisic acid induction of vacuolar H+-ATPase activity in mesembryanthemum crystallinum is developmentally regulated. Plant Physiol 120(3):811–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhushan D, Pandey A, Choudhary MK, Datta A, Chakraborty S, Chakraborty N (2007) Comparative proteomics analysis of differentially expressed proteins in chickpea extracellular matrix during dehydration stress. Mol Cell Proteomics 6(11):1868–1884

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (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

    Article  CAS  PubMed  Google Scholar 

  • Castillejo MÁ, Maldonado AM, Ogueta Samuel, Jorrín Jesús V (2008) Proteomic analysis of responses to drought stress in sunflower (Helianthus annuus) leaves by 2-DE gel electrophoresis and mass spectrometry. Open Proteomics J 1(1):59–71

    Article  CAS  Google Scholar 

  • Chelysheva VV, Smolenskaya IN, Trofimova MC, Babakov AV, Muromtsev GS (1999) Role of the 14-3-3 proteins in the regulation of H+-ATPase activity in the plasma membrane of suspension-cultured sugar beet cells under cold stress. FEBS Lett 456(1):22–26

    Article  CAS  PubMed  Google Scholar 

  • Chiang PK, Gordon RK, Tal J, Zeng GC, Doctor BP, Pardhasaradhi K, McCann PP (1996) S-Adenosylmethionine and methylation. FASEB J 10(4):471–480

    CAS  PubMed  Google Scholar 

  • Crowell DN, John ME, Russell D, Amasino RM (1992) Characterization of a stress-induced, developmentally regulated gene family from soybean. Plant Mol Biol 18(3):459–466

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5(12):3162–3172

    Article  CAS  PubMed  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17(1):268–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deeba F, Pandey AK, Ranjan S, Mishra A, Singh R, Sharma YK, Shirke PA, Pandey V (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol Biochem 53:6–18

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Heusdens C, Beullens S, Verreth C, Mulkers E, Proost P, Vanderleyden J, Michiels J (2005) Defence of Rhizobium etli bacteroids against oxidative stress involves a complexly regulated atypical 2-Cys peroxiredoxin. Mol Microbiol 55(4):1207–1221

    Article  CAS  PubMed  Google Scholar 

  • Dvoráková-HoláK Matusková A, Kubala M, Otyepka M, Kucera T, Vecer J, Herman P, Parkhomenko N, Kutejova E, Janata J (2010) Gycine-rich loop of mitochondrial processing peptidase alpha-subunit is responsible for substrate recognition by a mechanism analogous to mitochondrial receptor Tom20. J Mol Biol 396(5):1197–1210

    Article  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In: E. Lichtfouse, M. Navarrete, P. Debaeke, S. Véronique, C. Alberola (eds) Sustainable agriculture, vol 29. Springer, Netherlands, pp 153–188

  • Finni C, Andersen CH, Borch J, Gjetting S, Christensen AB, de Boer AH, Thordal-Christensen H, Collinge DB (2002) Do 14-3-3 proteins and plasma membrane H+-ATPases interact in the barley epidermis in response to the barley powdery mildew fungus? Plant Mol Biol 49(2):137–147

    Article  PubMed  Google Scholar 

  • Fischer G, Shah M, van Velthuizen H, Nachtergaele FO (2001) Global agro-ecological assessment for agriculture in the 21st century. IIASA and FAO, Laxenburg

    Google Scholar 

  • Greenbaum D, Colangelo C, Williams K, Gerstein M (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4(9):117

    Article  PubMed  PubMed Central  Google Scholar 

  • Grinstein S, Rotin D, Mason MJ (1989) Na+/H+ exchange and growth factor-induced cytosolic pH changes: role in cellular proliferation. Biochim Biophys Acta 988(1):73–97

    Article  CAS  PubMed  Google Scholar 

  • He Y, Meng X, Fan Q, Sun X, Xu Z, Song R (2009) Cloning and characterization of two novel chloroplastic glycerol-3-phosphate dehydrogenases from Dunaliella viridis. Plant Mol Biol 71(1–2):193–205

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK (1983) The plant cytoskeleton: the cytoskeleton in plant growth and development. Science 221(4611):641–642

    Article  CAS  PubMed  Google Scholar 

  • Hussey PJ, Hawkins TJ, Igarashi H, Kaloriti D, Smertenko A (2002) The plant cytoskeleton: recent advances in the study of the plant microtubule-associated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Mol Biol 50(6):915–924

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Yang B, Harri NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58(13):3591–3607

    Article  CAS  PubMed  Google Scholar 

  • Kirchhoff SR, Gupta S, Knowlton A (2002) Cytosolic heat shock protein 60, and myocardial injury. Circulation 105(24):2899–2904

    Article  CAS  PubMed  Google Scholar 

  • Li ZY, Chen SY (2000) Isolation and characterization of a salt and drought-inducible gene for S-adenosylmethionine decarboxylase from wheat (Triticum aestivum L.). J Plant Physiol 156(3):386–393

    CAS  Google Scholar 

  • Long SP, Ort DR (2010) More than taking the heat: crops and global change. Curr Opin Plant Biol 13(3):241–248

    Article  PubMed  Google Scholar 

  • Lu XK, Zhang DC, Yin ZJ, Wang DL, Wang JJ, Fan WL, Wang S, Ye WW (2013) Comparative analysis of proteomics in cotton (Gossypium hirsutum L.) leaves with different drought resistance levels under drought stress. Acta Bot Boreali Occidentalia Sin 33(12):2401–2409 (in Chinese)

    CAS  Google Scholar 

  • Luz JM, Lennarz WJ (1996) Protein disulfide isomerase: a multifunctional protein of the endoplasmic reticulum. EXS 77:97–117

    CAS  PubMed  Google Scholar 

  • Lv SL, Yang AF, Zhang KW, Wang L, Zhang JR (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed 20(3):233–248

    Article  CAS  Google Scholar 

  • Lv SL, Lian LJ, Tao PL, Li ZX, Zhang KW (2009) Overexpression of Thellungiella halophile H+-PPase (TsVP) in cotton enhances drought stress resistance of plants. Planta 229(4):899–910

    Article  CAS  PubMed  Google Scholar 

  • Ma HY, Song LR, Shu YJ, Wang S, Niu J, Wang ZK, Yu T, Gu WH, Ma H (2012) Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J Proteomics 75(5):1529–1546

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158

    Article  CAS  PubMed  Google Scholar 

  • Martz F, Sutinen ML, Kiviniemi S, Palta JP (2006) Changes in freezing tolerance, plasma membrane H+-ATPase activity and fatty acid composition in Pinus resinosa needles during cold acclimation and de-acclimation. Tree Physiol 26(6):783–790

    Article  CAS  PubMed  Google Scholar 

  • Masuta C, Tanaka H, Uehara K, Kuwata S, Koiwai A, Noma M (1995) Broad resistance to plant viruses in transgenic plants conferred by antisense inhibition of a host gene essential in S-adenosylmethionine-dependent transmethylation reactions. Proc Natl Acad Sci USA 92(13):6117–6121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matityahu I, Kachan L, Bar Ilan I, Amir R (2006) Transgenic tobacco plants overexpressing the Met25 gene of Saccharomyces cerevisiae exhibit enhanced levels of cysteine and glutathione and increased tolerance to oxidative stress. Amino Acids 30(2):185–194

    Article  CAS  PubMed  Google Scholar 

  • Mitsui S, Wakasugi T, Sugiura M (1993) A cDNA encoding the 57 kDa subunit of a cytokinin-binding protein complex from tobacco: the subunit has high homology to S-adenosyl-l-homocysteine hydrolase. Plant Cell Physiol 34(7):1089–1096

    CAS  Google Scholar 

  • O’Farrell HP (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250(10):4007–4021

    PubMed  PubMed Central  Google Scholar 

  • Park W, Scheffler BE, Bauer PJ, Campbell BT (2012) Genome-wide identification of differentially expressed genes under water deficit stress in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 12:90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payton P, Kottapalli KR, Kebede H, Mahan JR, Wright RJ, Allen RD (2011) Examining the drought stress transcriptome in cotton leaf and root tissue. Biotechnol Lett 33(4):821–828

    Article  CAS  PubMed  Google Scholar 

  • Pitcher LH, Zilinska BA (1996) Overexpression of Copper/Zinc superoxide dismutase in the cytosol of transgenic tobacco confers partial resistance to ozone-induced foliar necrosis. Plant Physiol 110(2):583–588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326(5957):1208–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ranjan A, Nigam D, Asif MH, Singh R, Ranjan S, Mantri S, Pandey N, Trivedi I, Rai KM, Jena SN, Koul B, Tuli R, Pathre UV, Sawant SV (2012a) Genome wide expression profiling of two accession of G. herbaceum L. in response to drought. BMC Genom 13:94

    Article  CAS  Google Scholar 

  • Ranjan A, Pandey N, Lakhwani D, Dubey NK, Pathre UV, Sawant SV (2012b) Comparative transcriptomic analysis of roots of contrasting Gossypium herbaceum genotypes revealing adaptation to drought. BMC Genom 13:680

    Article  CAS  Google Scholar 

  • Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rébeillé F, Douce R (2004) Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J Biol Chem 279(21):22548–22557

    Article  CAS  PubMed  Google Scholar 

  • Riccardi F, Gazeau P, Vienne D, Zivy M (1998) Protein changes in response to progressive water deficit in maize: quantitative variation and polypeptide identification. Plant Physiol 117(4):1253–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 50(6):1031–1039

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Uribe L, Abdelraheem A, Tiwari R, Sengupta-Gapalan C, Hughs SE, Zhang JF (2014) Identification of drought response genes in a drought tolerant cotton (Gossypium hirsutum L.) under reduced irrigation field conditions and development of candidate gene markers for drought tolerance. Mol Breed 34(4):1776–1796

    Article  Google Scholar 

  • Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2(9):1131–1145

    Article  CAS  PubMed  Google Scholar 

  • Sanchez AI, Rodriguez JM, Garcia R, Torreblanca J, Pardo JM (2004) Salt stress enhances xylem development and expression of S-adenosyl-l-methionine synthase in lignifying tissues of tomato plants. Planta 220(2):278–285

    Article  Google Scholar 

  • Serrato AJ, Pérez-Ruiz JM, Spínola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279(42):43821–43827

    Article  CAS  PubMed  Google Scholar 

  • Shu S, Mahadeo DC, Liu X, Liu WL, Parent CA, Korn ED (2006) S-adenosylhomocysteine hydrolase is localized at the front of chemotaxing cells, suggesting a role for transmethylation during migration. Proc Natl Acad Sci USA 103(52):19788–19793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sikorski MM, Biesiadka J, Kasperska AE, Kopcinska J, Lotocka B, Golinowski W, Legocki AB (1999) Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci 149(2):125–137

    Article  CAS  Google Scholar 

  • Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR, Motamed N, Komatsu S (2010) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Sci 8:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka H, Masuta C, Uehara K, Kataoka J, Koiwai A, Noma M (1997) Morphological changes and hypomethylation of DNA in transgenic tobacco expressing antisense RNA of the S-adenosyl-l-homocysteine hydrolase gene. Plant Mol Biol 35(6):981–986

    Article  CAS  PubMed  Google Scholar 

  • Vools W, Rottgers K (2002) Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochim Biophys Acta 1592(1):51–62

    Article  Google Scholar 

  • Wan XY, Liu JY (2008) Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol Cell Proteomics 7(8):1469–1488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang CC, Tsou CL (1993) Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J 7(15):1515–1517

    CAS  PubMed  Google Scholar 

  • Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresti M (2003) Protein Extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24(14):2369–2375

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vignani R, Scali M, Cresti M (2006) A universal and rapid Protocol for Protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27(13):2782–2786

    Article  CAS  PubMed  Google Scholar 

  • Wang FX, Ma YP, Yang CL, Zhao PM, Yao Y, Jian GL, Luo YM, Xia GX (2011) Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 11(22):4296–4309

    Article  CAS  PubMed  Google Scholar 

  • Wu YY, Zhang HP, Wu DY, Liu J, Li GX (2006) Relations between carbonic anhydrase activities and photosynthetic rates in the leaves and pods of plants. Acta Bot Boreali Occidentalia Sin 26(10):2094–2098 (in Chinese)

    CAS  Google Scholar 

  • Yang YW, Bian SM, Yao Y, Liu JY (2008) Comparative proteomic analysis provides new insights into the fiber elongating process in cotton. J Proteome Res 7(11):4623–4637

    Article  CAS  PubMed  Google Scholar 

  • Youssefian S, Nakamura M, Orudgev E, Kondo N (2001) Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an o-acetylserine(thiol)lyase modifies plant response to oxidative stress. Plant Physiol 126(3):1001–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanelli CF, Valentini SR (2007) Is there a role for eIF5A in translation? Amino Acids 33(2):351–358

    Article  CAS  PubMed  Google Scholar 

  • Zechmann B, Tomasić A, Horvat L, Fulgosi H (2010) Subcellular distribution of glutathione and cysteine in cyanobacteria. Protoplasma 246(1–4):65–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng XD, Yu LJ, Li W, Yang Y, Wu Y (2005) Stability of carbonic anhydrase in leaves of Vitex negundo in Karst areas of southwest China. Chin Bull Bot 22(2):169–174 (in Chinese)

    Google Scholar 

  • Zhang WH, Liu YL (2002) Relationship between tonoplast H+-ATPase activity, ion uptake and calcium in barley roots under NaCl stress. Acta Bot Sin 44(6):667–672 (in Chinese)

    CAS  Google Scholar 

  • Zhang XY, Liu CL, Wang JJ, Li FG, Ye WW (2007) Evaluation to the drought tolerance of cotton by PEG water-stress. Cotton Sci 19(3):205–209 (in Chinese)

    Google Scholar 

  • Zhang X, Zhen JB, Li ZH, Kang DM, Yang YM, Kong J, Hua JP (2011) Expression profile of early responsive genes under salt stress in Upland cotton (Gossypium hirsutum L.). Plant Mol Bio Rep 29(3):626–637

    Article  Google Scholar 

  • Zhu YN, Shi DQ, Ruan MB, Zhang LL, Meng ZH, Liu J, Yang WC (2013) Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PLoS One 8(11):e80218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was supported from the National Natural Science Foundation of China (30960201) and National Key Project for Transgenic Crops of China (2013X08005-004), and from the Xinjiang Agricultural University, for providing seeds of KK1543 and Xinluzao26.

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    1. College of Agronomy, Xinjiang Agricultural University, Urumqi, 830052, China

      Haiyan Zhang, Zhiyong Ni, Quanjia Chen, Zhongjun Guo, Wenwei Gao, Xiujuan Su & Yanying Qu

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    Zhang, H., Ni, Z., Chen, Q. et al. Proteomic responses of drought-tolerant and drought-sensitive cotton varieties to drought stress. Mol Genet Genomics 291, 1293–1303 (2016). https://doi.org/10.1007/s00438-016-1188-x

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