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A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek

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Abstract

To understand the complex drought response mechanism in crop plants, a systematic root proteomics approach was adopted to identify and analyze the expression patterns of differentially expressed major root proteins of Vigna radiata during short-term (3 days) and consecutive long-term water-deficit (6 days) as well as during recovery (6 days after re-watering). Photosynthetic gas exchange parameters of the plant were measured simultaneously during the stress treatment and recovery period. A total of 26 major protein spots were successfully identified by mass spectrometry, which were grouped according to their expression pattern during short-term stress as significantly up-regulated (9), down-regulated (10), highly down-regulated, beyond detection level of the software (2) and unchanged (5). The subsequent changes in the expression patterns of these proteins during long-term stress treatment and recovery period was analyzed to focus on the dynamic regulation of these functionally important proteins during progressive drought and recovery period. Cytoskeleton-related proteins were down-regulated initially (3d) but regained their expression levels during subsequent water-deficit (6d) while glycoprotein like lectins, which were primarily known to be involved in legume–rhizobia symbiosis, maintained their enhanced expression levels during both short and long-term drought treatment indicating their possible role in drought stress response of legumes. Oxidative stress-related proteins including Cu/Zn superoxide dismutase, oxidoreductase and aldehyde reductase were also up-regulated. The analyses of the dynamic regulation of these root proteins during short- and long-term water-deficit as well as recovery period may prove crucial for further understanding of drought response mechanisms in food legumes.

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Abbreviations

CRBD:

Completely randomized block design

DAR:

Days after re-watering

DAS:

Days after onset of stress treatment

IEF:

Isoelectric focussing

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization time of flight mass spectrometry

PPFD:

Photosynthetic photon flux density

SOD:

Superoxide dismutase

References

  • Abdel-Waheb AM, Shabeb MSA, Younis MAM (2002) Studies on the effect of salinity drought stress and soil type on nodule activities of Lablab purpureus (L.) sweet (Kashrangeeg). J Arid Environ 51:587–602

    Article  Google Scholar 

  • Akcay UC, Eercan O, Kavas M, Yildiz L, Yilmaz C, Octem HA, Yucel M (2010) Drought-induced oxidative damage and antioxidant responses in peanut (Arachis hypogaea L.) seedlings. Plant Growth Regul 61:21–28

    Article  Google Scholar 

  • Asch F, Dingkuhn M, Sow A, Audebert A (2005) Drought-induced changes in rooting patterns and assimilate partitioning between root and shoot in upland rice. Field Crops Res 93:223–236

    Article  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 6:1868–1884

    Article  PubMed  CAS  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Cammue BPA, Broekaert WF, Kellens JTC, Raikhel NV, Peumans WJ (1989) Stress-induced accumulation of wheat germ agglutinin and abscisic acid in roots of wheat seedlings. Plant Physiol 91:1432–1435

    Article  PubMed  CAS  Google Scholar 

  • Cánovas FM, Gaudot ED, Recorbet G, Jorrin J, Mock HP, Rossingol M (2004) Plant proteome analysis. Proteomics 4:285–298

    Article  PubMed  Google Scholar 

  • Castillo FJ (1996) Antioxidative protection in the in the inducible CAM plant Sedum album L following the imposition of severe water stress and recovery. Oecologia 107:469–477

    Article  Google Scholar 

  • Cho SK, Kim JE, Park JA, Eom TJ, Kim WT (2006) Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett 580:3136–3144

    Article  PubMed  CAS  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plant in dry soil. Annu Rev Plant Physiol Plant Mol Biol 42:55–76

    Article  CAS  Google Scholar 

  • Eissenstat DM, Caldwell MM (1989) Invasive root growth into disturbed soil of two tussock grasses that differ in competitive effectiveness. Funct Ecol 3:345–353

    Article  Google Scholar 

  • Ennahli S, Earl HJ (2005) Physiological limitations to photosynthetic carbon assimilation in cotton under water stress. Crop Sci 45:2374–2382

    Article  CAS  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345

    Article  CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought inhibition of photosynthesis in C3 plants: stomatal and non stomatal limitations revisited. Ann Bot 89:183–189

    Article  PubMed  CAS  Google Scholar 

  • Gazanchian A, Hajheidari M, Sima NK, Salekdeh GH (2007) Proteome response of Elymus elongatum to severe water stress and recovery. J Exp Bot 58:291–300

    Article  PubMed  CAS  Google Scholar 

  • Hafeez FY, Aslam Z, Malik KA (1988) Effect of salinity and inoculation on growth nitrogen fixation and nutrient uptake of Vigna radiata (L.) Wilczek. Plant Soil 106:3–8

    Article  Google Scholar 

  • Hajheidari M, Abdollahian-Noghabi N, Askari H, Heidari M, Sadeghiyan SY, Ober ES, Salekdeh GH (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950–960

    Article  PubMed  CAS  Google Scholar 

  • Hashiguchi A, Ahsan N, Komatsu S (2010) Proteomics application of crops in the context of climate changes. Food Res Int 43:1803–1813

    Article  CAS  Google Scholar 

  • Hegedüs A, Erdei S, Janda T, Tóth E, Horváth G, Dudits D (2004) Transgenic tobacco plants overproducing alfalfa aldose/aldehyde reductase show higher tolerance to low temperature and cadmium stress. Plant Sci 166:1329–1333

    Article  Google Scholar 

  • Hideg É, Nagy T, Oberschall A, Dudits D, Vass I (2003) Detoxification function of aldose/aldehyde reductase during drought and ultraviolet-B (280–320 nm) stresses. 26:513–522

    CAS  Google Scholar 

  • Huang B, Chu CH, Chen SL, Juan HF, Chen YM (2006) A proteomics study of the mung bean epicotyl regulated by brassinosteroids under conditions of chilling stress. Cell Mol Biol Lett 11:264–278

    Article  PubMed  CAS  Google Scholar 

  • Jacquot J-P, Eklund H, Rouhier N, Schürmann P (2009) Structural and evolutionary aspects of thioredoxin reductases in photosynthetic organisms. Trends Plant Sci 14:336–343

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Nandwal AS, Kundu BS, Kumar B, Sheoran IS, Kumar N, Mann A, Kukreja S (2006) Water relations, activities of antioxidants, ethylene evolution and membrane integrity of pigeonpea roots as affected by soil moisture. Biol Plant 50:303–306

    Article  CAS  Google Scholar 

  • Jaleel CA, Jayakumar K, Chang-Xing Z, Azooz MM (2009) Antioxidant potentials protect Vigna radiata (L.) Wilczek plants from soil cobalt stress and improve growth and pigment composition. Plant Omics J 2:120–126

    Google Scholar 

  • Jiang SY, Ma Z, Ramachandran S (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79

    Article  PubMed  Google Scholar 

  • Kottapalli KR, Rakwal R, Shibato J, Burow G, Tissue D, Burke J, Puppala N, Burow M, Payton P (2009) Physiology and proteomics of the water deficit stress response in three contrasting peanut genotypes. Plant Cell Environ 32:380–407

    Article  PubMed  CAS  Google Scholar 

  • Larrainzar E, Weinkoop S, Weckwerth W, Ladrera R, Arrese-Igor C, González EM (2007) Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol 144:1495–1507

    Article  PubMed  CAS  Google Scholar 

  • Lawn RJ, Ahn CS (1985) Mung bean (Vigna radiata (L.) Wilczek/Vigna mungo (L.) Hepper). In: Summerfield RJ, Roberts EH (eds) Grain legume crops. William Collins Sons & Co. Ltd, London, pp 584–623

  • Lee SC, Choi DS, Hwang IS, Hwang BK (2010) The pepper oxidoreductase Ca OXR1 interacts with the transcription factor CaRAV1 and is required for salt and osmotic stress tolerance. Plant Mol Biol 73:409–424

    Article  PubMed  CAS  Google Scholar 

  • Lüttge U, Fischer-Schliebs E, Ratajczak R (2001) The H+-pumping V-ATPase of higher plants: a versatile “eco-enzyme” in response to environmental stress. Cell Biol Mol Lett 6:356–361

    Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  PubMed  CAS  Google Scholar 

  • Manavalan LP, Guttikonda SK, Tran LSP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276

    Article  PubMed  CAS  Google Scholar 

  • Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, González EM (2007) Nitrogen fixation control under drought stress: localized or systemic? Plant Physiol 143:1968–1974

    Article  PubMed  CAS  Google Scholar 

  • Mckersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181

    PubMed  CAS  Google Scholar 

  • Mehta A, Magalhães BS, Souza DSL, Vasconcelos EAR, Silva LP, Grossi-deSa MF, Franco OL, da Costa PHA, Rocha TL (2008) Rooteomics: the challenge of discovering plant defense-related proteins in roots. Curr Protein Pept Sci 9:108–116

    Article  PubMed  CAS  Google Scholar 

  • Narita Y, Taguchi H, Nakamura T, Ueda A, Shi W, Takabe T (2004) Characterization of the salt-inducible methionine synthase from barley leaves. Plant Sci 167:1009–1016

    Article  CAS  Google Scholar 

  • Niini SS, Tarkka MK, Raudaskoski M (1996) Tubulin and actin protein patterns in scots pine (Pinus sylvestris) roots and developing ectomycorrhiza with Suillas bovines. Physiol Plant 96:186–192

    Article  CAS  Google Scholar 

  • Overpeck JT, Cole JE (2006) Abrupt change in earth’s climate system. Annu Rev Environ Res 31:1–31

    Article  Google Scholar 

  • Pedersen AL, Feldner HC, Rosendahl L (1996) Effect of proline on nitrogenase activity in symbiosomes from root nodules of soybean (Glycine max L.) subjected to drought stress. J Exp Bot 47:1533–1539

    Article  CAS  Google Scholar 

  • Pinheiro C, Passarinho JA, Ricardo CP (2004) Effect of drought and rewatering on the metabolism of Lupinus albus organs. J Plant Physiol 161:1203–1210

    Article  PubMed  CAS  Google Scholar 

  • Porcel RS, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescense. New Phytol 157:135–143

    Article  CAS  Google Scholar 

  • Rashid P, Karmoker JL, Chakrabortty S, Sarker BC (2004) The effect of salinity on ion accumulation and anatomical attributes in mungbean (Phaseolus radiatus L. cv. BARI-3) seedlings. Int J Agric Biol 6:495–498

    Google Scholar 

  • Rasineni GK, Chinnaboina M, Reddy AR (2010) Proteomic approach to study leaf proteins in a fast-growing tree species, Gmelina arborea Linn. Roxb. Trees 24:129–138

    Article  CAS  Google Scholar 

  • Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rébeillé F, Douce R (2004) Methionine metabolism in plants. J Biol Chem 279:22548–22557

    Article  PubMed  CAS  Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Saleh AAH, Abdel-Kader DZ, El Elish AM (2007) Role of heat shock and salicylic acid in antioxidant homeostasis in mungbean (Vigna radiata L.) plant subjected to heat stress. Am J Plant Physiol 2:344–355

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sarvanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4:2522–2532

    Article  Google Scholar 

  • Shakirova FM, Bezrukova MV, Khairullin RM (1993) The increase in lectin level in wheat shoots under the action of salt stress. Izv Russ Acad Sci 1:142–145

    Google Scholar 

  • Shakirova FM, Avalbaev AM, Bezrukova MV, Gimalov FR (2001) Induction of wheat germ agglutinin synthesis by abscisic and gibberellic acids in roots of wheat seedlings. Plant Growth Regul 33:111–115

    Article  CAS  Google Scholar 

  • Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351

    Article  PubMed  CAS  Google Scholar 

  • Shevchenko A, Wilm A, Vorm O, Mann M (1996) Mass spectrometric sequencing of protein from silver-stained polyacrylamide gels. Anal Chem 68:850–858

    Article  PubMed  CAS  Google Scholar 

  • Smucker AJM (1993) Soil environmental modifications of root dynamics and measurement. Annu Rev Phytopathol 31:191–216

    Article  Google Scholar 

  • Spadoro-Tank PJ, Etzler MM (1988) Heath shock enhances the synthesis of a lectin-related protein in Dolichos biflorus cell suspension cultures. Plant Physiol 88:1131–1135

    Article  PubMed  CAS  Google Scholar 

  • Stafford HA (1997) Role of flavonoids in symbiotic and defense functions in legume roots. Bot Rev 63:27–39

    Article  Google Scholar 

  • Sumithra K, Jutur PP, Carmel BD, Reddy AR (2006) Salinity-induced changes in two cultivars of Vigna radiate: responses of antioxidative and praline metabolism. Plant Growth Regul 50:11–22

    Article  CAS  Google Scholar 

  • Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16:341–349

    Article  CAS  Google Scholar 

  • Van Damme EJM, Barre A, Rougé P, Peumans WJ (2004) Cytoplasmic/nuclear plant lectins: a new story. Trends Plant Sci 9:484–489

    Article  PubMed  Google Scholar 

  • Van der Straeten D, Rodrigues-Pousada RA, Goodman HM, van Montagu M (1991) Plant enolase: gene structure, expression, and evolution. Plant Cell 3:719–735

    Article  PubMed  Google Scholar 

  • Van Sandt VST, Suslov D, Verbelen JP, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473

    Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Zhang H, Li Z (2007a) Analysis of gene expression profile induced by water stress in upland rice (Oryza sativa L. var.IRAT109) seedlings using subtractive expressed sequence tags library. J Integr Plant Biol 49:1455–1463

    Article  CAS  Google Scholar 

  • Wang X, Li X, Li Y (2007b) A modified Commassie Brilliant Blue staining method at nanogram sensitivity compatible with proteomic analysis. Biotechnol Lett 29:1599–1603

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Cosgrove DJ (2000) Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. J Exp Bot 51:1543–1553

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi M, Valliyodan B, Zhang J, Lenoble ME, Yu O, Rogers EE, Nguyen HT, Sharp RE (2010) Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant Cell Environ 33:223–243

    Article  PubMed  CAS  Google Scholar 

  • Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K, Masuda A, Kuwano M, Yokota A, Akashi K (2008) Programmed proteome response for drought avoidance/tolerance in the root of a C3 xerophyte (wild watermelon) under water deficits. Plant Cell Physiol 49:226–241

    Article  PubMed  CAS  Google Scholar 

  • Zayed MA, Zeid IM (1998) Effect of water and salt stress on growth, chlorophyll, mineral ions and organic solutes contents and enzyme activities in mungbean seedlings. Biol Plant 40:351–356

    Article  Google Scholar 

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Acknowledgments

We are thankful to Mr. Anirban Guha and Mr. Girish Rasineni for their critical reading of our manuscript. We thank Prof. N. Nadarajan, Tamil Nadu Agricultural University (TNAU), Coimbatore, India for providing Vigna radiata seeds. Our thanks are also to the Proteomics Facility (CREBB) of School of Life Sciences, University of Hyderabad and DST-FIST facility of our department. Debashree Sengupta acknowledges the fellowship from Council of Scientific and Industrial Research (CSIR), New Delhi, India.

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  1. Photosynthesis and Plant Stress Biology Laboratory, Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Debashree Sengupta, Monica Kannan & Attipalli R. Reddy

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  1. Debashree Sengupta
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  2. Monica Kannan
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  3. Attipalli R. Reddy
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Correspondence to Attipalli R. Reddy.

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Suppl. Fig. 1 Enlarged version of the few identified spots from the three triplicate gels of the control sample

Suppl. Fig. 2 Expression patterns of the identified spots showing significant changes during 3 DAS, 6 DAS and 6 DAR

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Supplementary material 2 (TIFF 184 kb)

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Sengupta, D., Kannan, M. & Reddy, A.R. A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek. Planta 233, 1111–1127 (2011). https://doi.org/10.1007/s00425-011-1365-4

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