Advertisement

Journal of Biosciences

, 44:20 | Cite as

Comparative physiological and leaf proteome analysis between drought-tolerant chickpea Cicer reticulatum and drought-sensitive chickpea C. arietinum

  • Sertan ÇevikEmail author
  • Gürler Akpinar
  • Aytunç Yildizli
  • Murat Kasap
  • Kübra Karaosmanoğlu
  • Serpil Ünyayar
Article
  • 100 Downloads

Abstract

Comparative physiological and proteomic analysis were performed to understand the stress responses of two chickpea species (C. reticulatum and C. arietinum) against drought. Our study revealed that drought stress reduced root length, leaf water content, and enhanced free proline content in both species. Effect of drought stress appeared to be greater in C. arietinum compared to C. reticulatum. A total of 24 differently expressed proteins were identified by using MALDI-TOF/TOF-MS/MS in response to drought. The proteins involved in photosynthesis and energy mechanisms were up-regulated in C. reticulatum and down-regulated in C. arietinum under drought. Our results suggest that the photosynthesis capacity of C. reticulatum is greater than that of C. arietinum under drought stress. Abundance of proline and sucrose biosynthesis related proteins, glutamine synthetase and cyctosolic fructose-bisphosphate aldolase, respectively, also increased in C. reticulatum under drought stress. The findings of this proteome analysis will help in understanding the mechanism of drought resistance in chickpea and may be also helpful in developing drought-resistant transgenic plants.

Keywords

Chickpea drought stress physiological analysis proteomics 

Abbreviations

APX

ascorbate peroxidase

COX

cytochrome c oxidase

FBA

fructose-bisphosphate aldolase

FNR

ferredoxin-NADP reductase

GME

GDP-mannose-epimerase

GS

glutamine synthetase

G3PDH

glyceraldehyde-3-phosphate dehydrogenase

IFR

ısoflavone reductase

LHCB

light-harvesting chlorophyll a/b-binding protein

LWP

leaf water potential

OEE1

oxygen evolving enhancer protein 1

OEE2

oxygen evolving enhancer protein 2

PGK

phosphoglycerate kinase

ROS

reactive oxygen species

RWC

relative water content

SBPase

sedoheptulose-1,7-bisphosphatase

2D-PAGE

two-dimensional polyacrylamide gel electrophoresis

Notes

Acknowledgements

The authors would like to thank Prof. Dr. Cengiz Toker (Department of Field Crops, Faculty of Agriculture, Akdeniz University, Antalya, Turkey) for providing the plant material. The manuscript was linguistically supported by the Technology Transfer Office Academic Writing Center of Mersin University. This work was supported by the University of Mersin; Project number is BAP-FBE BB (SÇ) 2012-4 DR.

Supplementary material

12038_2018_9836_MOESM1_ESM.docx (737 kb)
Supplementary material 1 (DOCX 737 kb)
12038_2018_9836_MOESM2_ESM.xlsx (32 kb)
Supplementary material 2 (XLSX 31 kb)

References

  1. Andersson J, Walters RG, Horton P and Jansson S 2001 Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13 1193–1204PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ashraf M and O’leary JW 1996 Effect of drought stress on growth, water relations, and gas exchange of two lines of sunflower differing in degree of salt tolerance. Int. J. Plant Sci. 157 729–732CrossRefGoogle Scholar
  3. Bai Z, Wang T, Wu Y, Wang K, Liang Q, Pan YZ, Jiang BB, Zhang L, et al. 2017 Whole-transcriptome sequence analysis of differentially expressed genes in Phormium tenax under drought stress. Sci. Rep. 7 1–9CrossRefGoogle Scholar
  4. Basu PS, Berger JD, Turner NC, Chaturvedi SK, Ali M and Siddique KHM 2007 Osmotic adjustment of chickpea (Cicer arietinum) is not associated with changes in carbohydrate composition or leaf gas exchange under drought. Annals Appl. Biol. 150 217–225CrossRefGoogle Scholar
  5. Bates LS, Waldren RP and Teare ID 1973 Rapid determination of free proline for water-stress studies. Plant Soil 39 205–207CrossRefGoogle Scholar
  6. Bogeat-Triboulot MB, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, et al. 2007 Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol. 143 876–892PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bollenbach TJ, Tatman DA and Stern DB 2003 CSP41a, a multifunctional RNAbinding protein, initiates mRNA turnover in tobacco chloroplasts. Plant J. 36 842–852PubMedCrossRefGoogle Scholar
  8. Budak H, Akpinar BA, Unver T and Turktas M 2013 Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI–MS/MS. Plant Mol. Biol. 83 89–103PubMedCrossRefGoogle Scholar
  9. Canci H and Toker C 2009 Evaluation of yield criteria for drought and heat resistance in chickpea (Cicer arietinum L.). J. Agronomy Crop Sci. 195 47–54CrossRefGoogle Scholar
  10. Caruso G, Cavaliere C, Guarino C, Gubbiotti R, Foglia P and Laganà A 2008 Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Analyt. Bioanalyt. Chem. 391 381–390CrossRefGoogle Scholar
  11. Çevik S, Yıldızlı A, Yandım G, Göksu H, Gultekin MS, Değer AG, Çelik A, Kuş NŞ, et al. 2014 Some synthetic cyclitol derivatives alleviate the effect of water deficit in cultivated and wild-type chickpea species. J. Plant Physiol. 171 807–816PubMedCrossRefGoogle Scholar
  12. Çevik S and Unyayar S 2015 The effects of exogenous application of ascorbate and glutathione on antioxidant system in cultivated Cicer arietinum and wild type C. reticulatum under drought stress. SDU J. Nat. Appl. Sci. 19 91–97Google Scholar
  13. Chung PJ, Jung H, Jeong DH, Ha SH, Choi YD and Kim JK 2016 Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genomics 17 563–575PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dolatabadian A, Sanavy SAMM and Chashmi NA 2008 The effects of foliar application of as- corbic acid (vitamin C) on antioxidant enzymes activities, lipid peroxidation and proline accumulation of canola (Brassica napus L.) under conditions of salt stress. J. Agronomy Crop Sci. 194 206–213CrossRefGoogle Scholar
  15. Dong Y, Fan G, Deng M, Xu E and Zhao Z 2014 Genome-wide expression profiling of the transcriptomes of four Paulownia tomentosa accessions in response to drought. Genomics 104 295–305PubMedCrossRefGoogle Scholar
  16. Faghani E, Gharechahi J, Komatsu S, Mirzaei M, Khavarinejad RA, Najafi F, Farsad LK and Salekdeh GH 2015 Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. J. Proteomics 114 1–15PubMedCrossRefGoogle Scholar
  17. Fambuena NM, Mesejo C, Reig C, Agustí M, Tárraga S, Lisón P, Iglesias DJ, Millo EP, et al. 2013 Proteomic study of Moncada mandarin buds from onversus off-crop trees. Plant Physiol. Biochem. 73 41–55CrossRefGoogle Scholar
  18. Fan W, Zhang Z and Zhang Y 2009 Cloning and molecular characterization of fructose1,6-bisphosphate aldolase gene regulated by high salinity and drought in Sesuvium portulacastrum. Plant Cell Rep. 28 975–984PubMedCrossRefGoogle Scholar
  19. Fang X, Turner NC, Yan G, Li F and Siddique KHM 2010 Flower numbers, pod production, pollen viability, and pistil function are reduced and flower and pod abortion increased in chickpea (Cicer arietinum L.) under terminal drought. J. Exp. Bot. 61 335–345PubMedCrossRefGoogle Scholar
  20. Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, et al. 2016 Transcriptome analyses reveal genotype- and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci. Rep. 6 1–15CrossRefGoogle Scholar
  21. Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M, Mirzaei M, Amirkhani A, Novo JVJ and Salekdeh GH 2013 Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J. Proteomics 94 289–301PubMedCrossRefGoogle Scholar
  22. Gharechahi J, Hajirezaei MR and Salekdeh GH 2015 Comparative proteomic analysis of tobacco expressing cyanobacterial flavodoxin and its wild type under drought stress. J. Plant Physiol. 175 48–58PubMedCrossRefGoogle Scholar
  23. Görg A, Postel W and Günther S 1988 The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 9 531–546PubMedCrossRefGoogle Scholar
  24. Gunes A, Cicek A, Inal M, Alpaslan F, Eraslan E Guneri and T Guzelordu 2006 Genotypic response of chickpea (Cicer arietinum L.) cultivars to drought stress implemented at pre and post-anthesis stages and its relations with nutrient uptake and efficiency. Plant Soil Environ. 52 368–376CrossRefGoogle Scholar
  25. Haake V, Zrenner R, Sonnewald U and Stitt M 1998 A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J. 14 147–157PubMedCrossRefGoogle Scholar
  26. Hajirezaei MR, Peisker M, Tschiersch H, Palatnik JF, Valle EM, Carrillo N and Sonnewald U 2002 Small changes in the activity of chloroplastic NADP+-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants. Plant J. 29 281–293PubMedCrossRefGoogle Scholar
  27. Heide H, Kalisz HM and Follmann H 2004 The oxygen evolving enhancer protein 1 (OEE) of photosystem II in green algae exhibits thioredoxin activity. J. Plant Physiol. 161 139–149PubMedCrossRefGoogle Scholar
  28. Hu WJ, Chen J, Liu TW, Wu Q, Wang WH, Liu X, Shen ZJ, Simon M, et al. 2014 Proteome and calcium-related gene expression in Pinus massoniana needles in response to acid rain under different calcium levels. Plant Soil 380 285–303CrossRefGoogle Scholar
  29. Hu X, Lu M, Li C, Liu T, Wang W, Wu J, Tai F, Li X, et al. 2011 Differential expression of proteins in maize roots in response to abscisic acid and drought. Acta Physiologiae Plantarum 33 2437–2446CrossRefGoogle Scholar
  30. Jaiswal DK, Mishra P, Subba P, Rathi D, Chakraborty S and Chakraborty N 2014 Membrane-associated proteomics of chickpea identifies Sad1/UNC-84 protein (CaSUN1), a novel component of dehydration signalling. Sci. Rep. 4 4177–4187PubMedPubMedCentralCrossRefGoogle Scholar
  31. Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi MJ, Somasundaram R and Panneerselvam R 2009 Drought stress in plants: a review on morphological characteristics and pigments composition. Int. J. Agric. Biol. 11 100–105Google Scholar
  32. Jedmowski C, Ashoub A, Beckhaus T, Berberich T, Karas M and Brüggemann W 2014 Comparative analysis of Sorghum bicolor proteome in response to drought stress and following recovery. Int. J. Proteomics 2014 1–10CrossRefGoogle Scholar
  33. José VG, Raquel GF, Rafael MNC, Eustaquio GP and Jesús VJN 2013 Physiological and proteomic analyses of drought stress response in Holm Oak provenances. J. Proteome Res. 12 5110–5123CrossRefGoogle Scholar
  34. Kim EY, Choi YH, Lee JI, Kim IH and Nam TJ 2015 Antioxidant activity of oxygen evolving enhancer protein 1 purified from Capsosiphon fulvescens. J. Food Sci. 80 1412–1417CrossRefGoogle Scholar
  35. Kim ST, Cho KS, Jang YS and Kang KY 2001 Two-dimensional electrophoretic analysis of rice proteins by polyethylene glycol fractionation for protein arrays. Electrophoresis 22 2103–2109PubMedCrossRefGoogle Scholar
  36. Kim ST, Cho KS, Yu S, Kim SG, Hong JC, Han C, Bae DW, Nam MH, et al. 2003 Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3 2368–2378PubMedCrossRefGoogle Scholar
  37. Krouma A 2010 Plant water relations and photosynthetic activity in three Tunisian chickpeas (Cicer arietinum L.) genotypes subjected to drought. Turkish J. Agric. Forest. 34 257–264Google Scholar
  38. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680–685CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lawlor DW and Cornic G 2002 Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ. 25 275–294PubMedCrossRefGoogle Scholar
  40. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA and Fryer M 2005 Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol. 138 451–460PubMedPubMedCentralCrossRefGoogle Scholar
  41. Leport L, Turner NC, French RJ, Barr MD, Duda R, Davies SL, Tennant D and Siddique KHM 1999 Physiological responses of chickpea genotypes to terminal drought in a Mediterranean-type environment. Eur. J. Agronomy 11 279–291CrossRefGoogle Scholar
  42. Lhout FA, Zunzunegui M, Barradas MCD, Tirado R, Clavijo A and Novo FG 2001 Comparison of proline accumulation in two mediterranean shrubs subjected to natural and experimental water deficit. Plant Soil 230 175–183CrossRefGoogle Scholar
  43. Lisar SYS, Motafakkerazad R, Hossain MM and Rahman IMM 2012 Water Stress in Plants: Causes, Effects and Responses. (eds) Rahman IMM Rijeka, Croatia, pp 1–14Google Scholar
  44. Lum MS, Hanafi MM, Rafii YM and Akmar ASN 2014 Effect of drought stress on growth, proline and antioxidant enzyme activities of upland rice. J. Anim. Plant Sci. 24 1487–1493Google Scholar
  45. Ma L, Wang Y, Liu W and Liu Z 2014 Overexpression of an alfalfa GDP-mannose 3, 5- epimerase gene enhances acid, drought and salt tolerance in transgenic Arabidopsis by increasing ascorbate accumulation. Biotechnol. Lett. 36 2331–2341PubMedCrossRefGoogle Scholar
  46. Macar TK, Turan O and Ekmekci Y 2009 Effects of water deficit induced by PEG and NaCl on chickpea (Cicer arietinum L.) cultivars and lines at early seedling stages. Gazi Univ. J. Sci. 22 5–14Google Scholar
  47. Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC Sohrabi Y 2010 Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust. J. Crop Sci. 4 580–585Google Scholar
  48. Manac’h N and Kuntz M 1999 Stress induction of a nuclear gene encoding for a plastid protein is mediated by photo-oxidative events. Plant Physiol. Biochem. 37 859–868PubMedCrossRefGoogle Scholar
  49. Mantri NL, Ford R, Coram TE and Pang EC 2007 Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics. 8 303PubMedPubMedCentralCrossRefGoogle Scholar
  50. Nagy Z, Németh E, Guóth A, Bona L, Wodala B and Pécsváradi A 2013 Metabolic indicators of drought stress tolerance in wheat: Glutamine synthetase isoenzymes and Rubisco. Plant Physiol. Biochem. 67 48–54PubMedCrossRefGoogle Scholar
  51. Nayyar H and Chander S 2004 Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J. Agronomy Crop Sci. 190 355–365CrossRefGoogle Scholar
  52. Nedunchezhiyan M, Byju G and Ray RC 2012 Effect of tillage, irrigation, and nutrient levels on growth and yield of sweet potato in rice fallow. ISRN Agronomy 2012 1–13CrossRefGoogle Scholar
  53. Ngamhui NO, Akkasaeng C, Zhu YJ, Tantisuwichwong N, Roytrakul S and Sansayawichai T 2012 Differentially expressed proteins in sugarcane leaves in response to water deficit stress. Plant Omics 5 365–371Google Scholar
  54. Nouri MZ, Moumeni A and Komatsu S 2015 Abiotic Stresses: Insight into gene regulation and protein expression in photosynthetic pathways of plants. Int. J. Mol. Sci. 16 20392–20416PubMedPubMedCentralCrossRefGoogle Scholar
  55. Oh MW and Komatsu S 2015 Characterization of proteins in soybean roots under flooding and drought stresses. J. Proteomics 114 161–181PubMedCrossRefGoogle Scholar
  56. Pandey A, Chakraborty S, Datta A and Chakraborty N 2008 Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol. Cell. Proteomics 7 88–107PubMedCrossRefGoogle Scholar
  57. Pawłowski TA 2009 Proteome analysis of Norway maple (Acer platanoides L.) seeds dormancy breaking and germination: influence of abscisic and gibberellic acids. BMC Plant Biol. 9 48–61PubMedPubMedCentralCrossRefGoogle Scholar
  58. Rahbarian R, Nejad RK, Ganjeali A, Bagheri A and Najafi F 2011 Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietınum L.) genotypes. Acta Biologica Cracoviensia Series Botanica 53 47–56Google Scholar
  59. Raines CA 2003 The Calvin cycle revisited. Photosynthesis Res. 75 1–10CrossRefGoogle Scholar
  60. Roy A 2014 Proteomic analyses of alterations in plant proteome under drought stress; in Molecular approaches in plant abiotic stress (eds) Gaur RK and Sharma P 1st edition (Taylor & Francis Group, Florida) pp 232–247Google Scholar
  61. Sabaghpour SH, Mahmoudi AA, Saeed A, Kamel M and Malhotra RS 2006 Study of chickpea drought tolerance lines under dryland conditions of Iran. Indian J. Crop Sci. 1 70–73Google Scholar
  62. Sanda S, Yoshida K, Kuwano M, Kawamura T, Munekage YN, Akashi K and Yokota A 2011 Responses of the photosynthetic electron transport system to excess light energy caused by water deficit in wild watermelon. Physiologia Plantarum 142 247–264PubMedCrossRefGoogle Scholar
  63. Sankar B, Jaleel CA, Manivannan P, Kishorekumar A, Somasundaram R and Panneerselvam R 2007 Drought induced biochemical modifications and proline metabolism in Abelmoschus esculentus (L.) Moench. Acta Botanica Croatica 66 43–56Google Scholar
  64. Siddique RB, Hamid A and Islam MS 2000 Drought stress effects on water relations of wheat. Bot. Bull. Acad. Sinica 41 35–39Google Scholar
  65. Smart RE and Bingham GE 1974 Rapid estimation of relative water content. Plant Physiol. 53 258–260PubMedPubMedCentralCrossRefGoogle Scholar
  66. Szabados L and Savoure A 2010 Proline: a multifunctional amino acid. Trends Plant Sci. 15 89–97PubMedCrossRefGoogle Scholar
  67. Talebi R, Ensafi MH, Baghebani N, Karami E and Mohammadi K 2013 Physiological responses of chickpea (Cicer arietinum) genotypes to drought stress. Environ. Exp. Biol. 11 9–15Google Scholar
  68. Tezara W, Mitchell VJ, Driscoll SD and Lawlor DW 1999 Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401 914–917CrossRefGoogle Scholar
  69. Toker C and Cagirgan MI 1998 Assessment of response to drought stress of chickpea (Cicer arietinum L.) lines under rainfed conditions. Turkish J. Agric. Forest. 22 615–621Google Scholar
  70. Turner NC, Abbo S, Berger JD, Chaturvedi SK, French RJ, Ludwig C, Mannur DM, Singh SJ, et al. 2007 Osmotic adjustment in chickpea (Cicer arietinum L.) results in no yield benefit under terminal drought. J. Exp. Bot. 58 187–194PubMedCrossRefGoogle Scholar
  71. Uematsu K, Suzuki N, Iwamae T, Inui M and Yukawa H 2012 Increased fructose 1,6- bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. J. Exp. Bot. 63 3001–3009PubMedCrossRefGoogle Scholar
  72. Unlu M, Morgan ME and Minden JS 1997 Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis 18 2071–2077PubMedCrossRefGoogle Scholar
  73. Vendruscolo ECG, Schuster I, Pileggi M, Scapimd CA, Molinarie HBC, Marure CJ and Vieira LGE 2007 Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J. Plant Physiol. 164 1367–1376PubMedCrossRefGoogle Scholar
  74. Wang L, Pana D, Lia J, Tane F, Benningc SH, Liangd W and Chen W 2015a Proteomic analysis of changes in the Kandelia candel chloroplast proteins reveals pathways associated with salt tolerance. Plant Sci. 231 159–172PubMedCrossRefGoogle Scholar
  75. Wang N, Zhao J, He X, Sun H, Zhang G, and Wu F 2015b Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. BMC Genomics 16 432PubMedPubMedCentralCrossRefGoogle Scholar
  76. Xiao XW, Yang F, Zhang S, Korpelainen H and Li CY 2009 Physiological and proteomic responses of two contrasting Populus cathayana populations to drought stress. Physiologia Plantarum 136 150–168PubMedCrossRefGoogle Scholar
  77. Xu YH, Liu R, Yan L, Liu ZQ, Jiang SC, Shen YY, Wang XF and Zhang DP 2012 Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in. Arabidopsis. J. Exp. Bot. 63 1095–1106PubMedCrossRefGoogle Scholar
  78. Yan W, Zhong Y and Shangguan Z 2016 A meta-analysis of leaf gas exchange and water status responses to drought. Sci. Rep. 6 1–9CrossRefGoogle Scholar
  79. Yang ZB, Eticha D, Führs H, Heintz D, Ayoub D, Dorsselaer AV, Schlingmann B, Rao IM, et al. 2013 Proteomic and phosphoproteomic analysis of polyethylene glycol-induced osmotic stress in root tips of common bean (Phaseolus vulgaris L.). J. Exp. Bot. 64 5569–5586PubMedPubMedCentralCrossRefGoogle Scholar
  80. Zadražnik T, Hollung K, Jacobsen WE, Megliča V and Vozliča JS 2013 Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J. Proteomics 78 254–272PubMedCrossRefGoogle Scholar
  81. Zhang Y, Zhang H, Zou ZR, Liu Y and Hua XH 2015 Deciphering the protective role of spermidine against saline–alkaline stress at physiological and proteomic levels in tomato. Phytochemistry 110 13–21PubMedCrossRefGoogle Scholar
  82. Zhao Y, Dua H, Wanga Z and Huang B 2011 Identification of proteins associated with water-deficit tolerance in C4 perennial grass species, Cynodon dactylon × Cynodon transvaalensis and Cynodon dactylon. Physiologia Plantarum 141 40–55PubMedCrossRefGoogle Scholar
  83. Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, et al. 2007 Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol. Biol. 63 591–608PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  1. 1.Vocational School of MutMersin UniversityMersinTurkey
  2. 2.Medical Biology Department/Dekart Proteomics LaboratoryKocaeli UniversityKocaeliTurkey
  3. 3.Biology Department, Art and Science FacultyMersin UniversityMersinTurkey
  4. 4.Biomedical Engineering Department, Technology FacultyKocaeliTurkey

Personalised recommendations