Proteomic and Physiological Analyses of dl-Cyclopentane-1,2,3-triol-Treated Barley Under Drought Stress

  • Sertan ÇevikEmail author
  • Ayşin Güzel Değer
  • Aytunç Yıldızlı
  • Neslihan Doğanyiğit
  • Ayşe Gök
  • Serpil Ünyayar
Original Article


This study was conducted to determine the effect of exogenous cyclitol (dl-cyclopentane-1,2,3-triol) on barley (Hordeum vulgare L.) during the alleviation of drought stress by using proteomics and physiological approaches. With the relative water content, water potential declined in barley depending on time under drought stress. This decline was lower in cyclitol-treated plants than in untreated plants. The stomatal pore width and open stoma number were higher in cyclitol-treated barley than in untreated plants under drought stress. The abscisic acid (ABA) and proline levels increased with the severity of drought in most treatments. The ABA level was lower in cyclitol-treated plants than in untreated plants under drought stress. Cyclitol treatments reduced \( {O}_2^{.-} \)fluorescence in leaf cells under drought stress. Total differentially expressed proteins were identified in cyclitol treatment under stressful and unstressful conditions. Photosynthesis (approx. 49%) and energy metabolism (approx. 27%) were upregulated by cyclitol treatment under drought. Moreover, CML42, acting as a negative ABA regulator, also increased by cyclitol treatment. This increase may be important in controlling stomata movements under drought stress. Our results suggest that exogenous cyclitol enhances the drought tolerance of barley seedlings by modulating the photosynthesis, energy pathway, biosynthesis, and signal transduction.


Barley (Hordeum vulgare L.) Drought Proteomics Stomata Cyclitol Water status 



We thank Prof.Dr. M. Serdar GÜLTEKİN for kindly providing the dl-cyclopentane-1,2,3-triol. We also thank Prof.Dr. Bahar TAŞDELEN for the statistical analysis.

Authors’ Contributions

SÇ, S,Ü and AGD conceived and designed the experiments; SÇ, AGD, AY, ND, and AG performed the experiments; SÜ, SÇ, and AY analyzed the data; SÜ and SÇ wrote the paper.


The authors received financial support from The Scientific and Technological Research Council of Turkey (TÜBİTAK, grant no: 115Z032) and the Mersin University Scientific Research Foundation (grant no. BAP-2015-AP3-1073 and grant no BAP-2017-1-TP2-2204). This academic work was linguistically supported by the Mersin Technology Transfer Office Academic Writing Center of Mersin University.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11105_2019_1151_MOESM1_ESM.docx (5.1 mb)
ESM 1 (DOCX 5191 kb)


  1. Ahn C, Park U, Park PB (2011) Increased salt and drought tolerance by D-ononitol production in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 415:669–674CrossRefGoogle Scholar
  2. Ali M, Jensen CR, Mogensen VO, Andersen MN, Henson IE (1999) Root signaling and osmotic adjustment during intermittent soil drying sustain grain yield of field grown wheat. Field Crop Res 62:35–52CrossRefGoogle Scholar
  3. Arndt SK, Livesley SJ, Merchant A, Bleby TM, Grierson PF (2008) Quercitol and osmotic adaptation of field-grown Eucalyptus under seasonal drought stress. Plant, Cell Environ 31(7):915–924CrossRefGoogle Scholar
  4. Assmann SM, Wang XQ (2001) From milliseconds to millions of years: guard cells and environmental responses. Curr Opin Plant Biol 4:421–428CrossRefGoogle Scholar
  5. Ayoub A, Khalil M, Grace J (1992) Acclimation to drought in Acer pseudoplatanus L. (sycamore) seedlings. J Exp Bot 43:1591–1602CrossRefGoogle Scholar
  6. Baier M, Dietz KJ (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119(4):1407–1414CrossRefGoogle Scholar
  7. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  8. Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crop Res 112:119–123CrossRefGoogle Scholar
  9. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan B, Gruissem W and Jones R (eds), Biochemistry and molecular biology of plants, 1158–1203, Rockville: American Society of Plant PhysiologyGoogle Scholar
  10. Çevik S, Yıldızlı A, Yandım G, Göksu H, Gultekin MS, Değer AG, Çelik A, Kuş NŞ, Ünyayar S (2014) Some synthetic cyclitol derivatives alleviate the effect of water deficit in cultivated and wild-type chickpea species. J Plant Physiol 171:807–816CrossRefGoogle Scholar
  11. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103(4):551–560CrossRefGoogle Scholar
  12. Clifford SC, Arndt SK, Corlett JE, Joshi S, Sankhla N, Popp M, Jones HG (1998) The role of solute accumulation, osmotic adjustment and changes in cell wall elasticity in drought tolerance in Ziziphus mauritiana (Lamk.). J Exp Bot 49(323):967–977CrossRefGoogle Scholar
  13. Corpas FJ, Fernandez-Ocana A, Carreras A, Valderrama R, Luque F, Esteban FJ, Rodriguez-Serrano M, Chaki M, Pedrajas JR, Sandalio LM, Del Rio LA, Barrosa JB (2006) The expression of different superoxide dismutase forms is cell-type dependent in olive (Olea europea L.) leaves. Plant Cell Physiol 47(7):984–994CrossRefGoogle Scholar
  14. Dodd IC, Stikic R, Davies WJ (1996) Chemical regulation of gas exchange and growth of plants in drying soil in the field. J Exp Bot 47:1475–1490CrossRefGoogle Scholar
  15. Görg A, Postel W, Günther S (1988) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 9:531–546CrossRefGoogle Scholar
  16. Gültekin MS, Çelik M, Balcı M (2004) Cyclitols and Related Compounds, Current Organic Chemistry 8:1159Google Scholar
  17. Hein JA, Sherrard ME, Manfredi KP, Abebe T (2016) The fifth leaf and spike organs of barley (Hordeum vulgare L.) display different physiological and metabolic responses to drought stress. BMC Plant Biol 16.
  18. Hu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI (2010) Carbonic anhydrases are upstream regulators in guard cells of CO2-controlled stomatal movements. Nat Cell Biol 12:87–98CrossRefGoogle Scholar
  19. Hu WJ, Chen J, Liu TW, Wu Q, Wang WH, Liu X, Wu Q, Wang WH, Liu X, Shen ZJ, Simon M, Chen J, Wu FH, Pei ZM, Zheng HL (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
  20. Kim ST, Cho KS, Jang YS, Kang KY (2001) Two-dimensional electrophoretic analysis of rice proteins by polyethyleneglycol fractionation for protein arrays. Electrophoresis 22:2103–2109CrossRefGoogle Scholar
  21. Klein T, Shpringer I, Fikler B, Elbaz G, Cohen S, Yakir D (2013) Relationship between stomatal regulation, water-use, and water-use efficiency of two coexisting key Mediterranean tree species. For Ecol Manag 302:34–42CrossRefGoogle Scholar
  22. Kopyra M, Gwodz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017CrossRefGoogle Scholar
  23. Krapp AR, Tognetti VB, Carrillo N, Acevedo A (1997) The role of ferredoxin-NADP+ reductase in the concerted cell defense against oxidative damage. Eur J Biochem 249:556–563CrossRefGoogle Scholar
  24. Król A, Weidner S (2017) Changes in the proteome of grapevine leaves (Vitis vinifera L.) during long-term drought stress. J Plant Physiol 211:114–126CrossRefGoogle Scholar
  25. Kuli A, Wamer I, Krzywinska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. J Integr Biol 15(12):859–871Google Scholar
  26. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  27. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570CrossRefGoogle Scholar
  28. Li M, Li Y, Mrozowski RM, Sandusky ZM, Shan M, Song X, Wu X, Wu B, Zhang Q, Lannigan DA, O’Doherty GA (2015) Synthesis and structure-activity relationship study of 5a-carbasugar analogues of SL0101. Med Chem Lett 6:95–99CrossRefGoogle Scholar
  29. Mao D, Yu F, Li J, Van de Poel B, Tan D, Li J, Liu Y, Li X, Dong M, Chen L et al (2015) Feronia receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant Cell Environ 38:2566–2574CrossRefGoogle Scholar
  30. Mechri B, Tekaya M, Cheheb H, Hammami M (2015) Determination of mannitol, sorbitol and myo-inositol in olive tree roots and rhizospheric soil by gas chromatography and effect of severe drought conditions on their profiles. J Chromatogr Sci 53(10):1631–1638CrossRefGoogle Scholar
  31. Piotrowicz AI, Michalczyk DJ, Adamos B, Gorecki RJ (2007) Different effects of soil drought on soluble carbohydrates of developing Lupinus pilopus and Lupinus luteus embryos. Acta Soc Bot Pol 76(2):119–125CrossRefGoogle Scholar
  32. Roelfsema MRG, Hedrich R (2016) Do stomata of evolutionary distant species differ in sensitivity to environmental signals. New Phytol 211:767–770CrossRefGoogle Scholar
  33. Saradadevi R, Bramley H, Siddique KHM, Edwards E, Palta JA (2014) Contrasting stomatal regulation and leaf ABA concentrations in wheat genotypes when split root systems were exposed to terminal drought. Field Crop Res 162:77–86CrossRefGoogle Scholar
  34. Scholz SS, Reichelt M, Vadassery J, Mithöfer A (2015) Calmodulin-like protein CML37 is a positive regulator of ABA during drought stress in Arabidopsis. Plant Signal Behav 10(6):e1011951CrossRefGoogle Scholar
  35. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658CrossRefGoogle Scholar
  36. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260CrossRefGoogle Scholar
  37. Stimler K, Berry JA, Yakir D (2012) Effects of carbonyl sulfide and carbonic anhydrase on stomatal conductance. Plant Physiol 158:524–530CrossRefGoogle Scholar
  38. Studer AJ, Gandin A, Kolbe AR, Wang L, Cousins AB, Brutnell TP (2014) A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant Physiol 165:608–617CrossRefGoogle Scholar
  39. Tiwari A, Kumar P, Singh S, Ansari S (2005) Carbonic anhydrase in relation to higher plants. Photosynthetica 43:1–11CrossRefGoogle Scholar
  40. Vabulas RM, Raychaudhuri S, Hayer-Hartl M, Hartl U (2010) Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb Perspect Biol 2(12):a004390CrossRefGoogle Scholar
  41. Wang WW, Xia MX, Chen J, Yuan R, Deng FN, Shen FF (2016) Gene expression characteristics and regulation mechanisms of superoxide dismutase and its physiological roles in plants under stress. Biochem Mosc 81(5):465–480CrossRefGoogle Scholar
  42. Zhang M, Jin ZQ, Zhao J, Zhang G, Wu F (2015) Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley. Plant Growth Regul 75:567–574CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Sertan Çevik
    • 1
    Email author
  • Ayşin Güzel Değer
    • 2
  • Aytunç Yıldızlı
    • 3
  • Neslihan Doğanyiğit
    • 3
  • Ayşe Gök
    • 4
  • Serpil Ünyayar
    • 3
  1. 1.Vocational School of MutMersin UniversityMersinTurkey
  2. 2.Vocational School of Technical SciencesMersin UniversityMersinTurkey
  3. 3.Faculty of Science and Letters, Department of Biology, Ciftlikkoy CampusMersin UniversityMersinTurkey
  4. 4.Faculty of Science and Letters, Department of Biotechnology, Ciftlikkoy CampusMersin UniversityMersinTurkey

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