biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 62:140-148, 2018 | DOI: 10.1007/s10535-017-0760-5

Freezing tolerance of chickpea: biochemical and molecular changes at vegetative stage

Ö. Arslan1,3, F. Eyidoğan2, Y. Ekmekçi1,*
1 Department of Biology, Faculty of Science, University of Hacettepe, Ankara, Turkey
2 Department of Elementary Education, Education Faculty, Başkent University, Ankara, Turkey
3 Department of Food Processing, University College of Espiye, University of Giresun, Giresun, Turkey

The aim of this study was to find a correlation between the freezing tolerance of three chickpea (Cicer arietinum L.) cultivars (İnci, Işik-05, and Sari-98) and their wild relative C. echinospermum and physiological responses. Chickpea plants (15-d-old) were subjected to cold acclimation (CA) (10 °C for 7 d), freezing (-3 or -5 °C for 2 h), and subsequent rewarming (25 °C for 7 d). In two separate experiments with three replications, we determined growth, water status, photosystem 2 photochemical activity, photosynthetic pigments, H2O2, malondialdehyde, and proline content, relative leakage ratio, antioxidant enzyme activities, and gene expressions in cultivars different in freezing tolerance. Freezing temperatures adversely affected all the physiological parameters of all cultivars. Rewarming did not lead to complete recovery. The cultivar İnci was more tolerant to the freezing temperatures than others.

Keywords: antioxidant enzymes; chlorophyll; Cicer arietinum; C. echinospermum; gene expression; malondialdehyde; photochemical activity
Subjects: freezing tolerance; chlorophyll a fluorescence; chlorophyll content; carotenoids; anthocyanins; flavonoids; hydrogen peroxide; electrolyte leakage; ascorbate peroxidase; catalase; glutathione reductase; proline; malondialdehyde; chickpea

Received: July 4, 2015; Revised: May 18, 2017; Accepted: May 25, 2017; Published: January 1, 2018  Show citation

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Arslan, Ö., Eyidoğan, F., & Ekmekçi, Y. (2018). Freezing tolerance of chickpea: biochemical and molecular changes at vegetative stage. Biologia plantarum, 62(1), 140-148. doi: 10.1007/s10535-017-0760-5
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    References

    1. Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
    2. Bergmeyer, H.U.: Methods of Enzymatic Analysis, Vol. II. Section C: Methods for Determination of Enzyme Activity. - Academic Press, New York 1974.
    3. Beyer, W.F., Fridovich, I.: Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. - Anal Biochem. 161: 559-566, 1987. Go to original source...
    4. Borawska-Jarmu³owicz, B., Mastalerczuk, G., Kalaji, H.M., Carpentier, R., Pietkiewicz, S., Allakhverdiev, S.I.: Photosynthetic efficiency and survival of Dactylis glomerata and Lolium perenne following low temperature stress. - Russ. J. Plant Physiol. 61: 281-288, 2014. Go to original source...
    5. Bradford, M.M.: 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, 1976. Go to original source...
    6. Burke, J.J., Oliver, M.J.: Differential temperature sensitivity of pea superoxide dismutase. - Plant Physiol. 100: 1595-1598, 1992. Go to original source...
    7. Cavender-Bares, J.: Chilling and freezing stress in live oaks (Quercus section Virentes): intra-and inter-specific variation in PS II sensitivity corresponds to latitude of origin. - Photosynth. Res. 94: 437-453, 2007. Go to original source...
    8. Chance, B., Maehly, A.C.: Assay of catalases and peroxidases. - Methods Enzymol. 2: 764-817, 1955. Go to original source...
    9. Chomczynski, P., Sacchi, N.: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. - Anal. Biochem. 162: 156-159, 1987. Go to original source...
    10. Croser, J., Clarke, H., Siddique, K., Khan, T.: Low-temperature stress: implications for chickpea (Cicer arietinum L.) improvement. - Crit. Rev. Plant Sci. 22: 185-219, 2003. Go to original source...
    11. Dai, F., Huang, Y., Zhou, M., Zhang, G.: The influence of cold acclimation on antioxidative enzymes and antioxidants in sensitive and tolerant barley cultivars. - Biol. Plant. 53: 257-262, 2009. Go to original source...
    12. Esterbauer, H., Cheeseman, K.H.: Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. - Methods Enzymol. 186: 407-431, 1990. Go to original source...
    13. Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Biochem. 48: 909-930, 2010. Go to original source...
    14. Hao, W., Arora, R., Yadav, A.K., Joshee, N.: Freezing tolerance and cold acclimation in guava (Psidium guajava L.). - HortScience 44: 1258-1266, 2009. Go to original source...
    15. Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999. Go to original source...
    16. Janda, T., Szalai, G., Rios-Gonzalez, K., Veisz, O., Páldi, E.: Comparative study of frost tolerance and antioxidant activity in cereals. - Plant Sci. 164: 301-306, 2003. Go to original source...
    17. Janská, A., Marıík, P., Zelenková, S., Ovesná, J.: Cold stress and acclimation-what is important for metabolic adjustment?. - Plant Biol. 12: 395-405, 2010. Go to original source...
    18. John, R., Anjum, N.A., Sopory, S.K., Akram, N.A., Ashraf, M.: Some key physiological and molecular processes of cold acclimation. - Biol. Plant. 60: 603-618, 2016. Go to original source...
    19. Kalaji, H.M.., Goltsev, V., Bosa, K., Allakverdiev, S.I., Strasser, R.J., Govindjee.: Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. - Photosynth. Res., 114: 69-96, 2012. Go to original source...
    20. Kalaji, H.M., Jajoo, A., Oukarroum, A., Brestic, M., Zivcak, M., Samborska, I.A., Center, M.D., £ukasik, I., Goltsev, V., Ladle, R.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102, 2016. Go to original source...
    21. Kaur, G., Kumar, S., Thakur, P., Malik, J.A., Bhandhari, K., Sharma, K.D., Nayyar, H.: Involvement of proline in response of chickpea (Cicer arietinum L.) to chilling stress at reproductive stage. - Sci. Hort. 128: 174-181, 2011. Go to original source...
    22. Kume, S., Kobayashi, F., Ishibashi, M., Ohno, R., Nakamura, C., Takumi, S.: Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. - Genes Genet. Syst. 80: 185-197, 2005. Go to original source...
    23. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T(4). - Nature 227: 680-685, 1970. Go to original source...
    24. Li, X.G., Duan, W., Meng, Q.W., Zou, Q., Zhao, S.J.: The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. - Plant Cell Physiol. 45: 103-108, 2004. Go to original source...
    25. Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
    26. Mancinelli, A.L., Yang, C.P.H., Lindquist, P., Anderson, O.R., Rabino, I.: Photocontrol of anthocyanin synthesis III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. - Plant Physiol. 55: 251-257, 1975. Go to original source...
    27. Medini, M., Baum, M., Hamza, S.: Transcript accumulation of putative drought responsive genes in drought-stressed chickpea seedlings. - Afr. J. Biotechnol. 8: 4441-4449, 2009.
    28. Mirecki, R.M., Teramura, A.H.: Effects of ultraviolet-B irradiance on soybean. V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. - Plant Physiol. 74: 475-480, 1984. Go to original source...
    29. Nayyar, H., Bains, T.S., Kumar, S.: Chilling stressed chickpea: effect of cold acclimation, calcium and abscisic acid on cryoprotective solutes and oxidative damage. - Environ. exp. Bot. 54: 275-285, 2005. Go to original source...
    30. Rao, V.M., Hale, B.A., Omrod, D.P.: Amelioration of ozone induced oxidative damage in wheat plants grown under high carbon dioxide. - Plant Physiol. 109: 421-432, 1995. Go to original source...
    31. Redmann, R.E., Haraldson, J., Gusta, L.V.: Leakage of UVabsorbing substances as a measure of salt injury in leaf tissue of woody species. - Physiol. Plant. 67: 87-91, 1986. Go to original source...
    32. Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V.: Cold signalling and cold acclimation in plants. - Adv. bot. Res. 49: 35-150, 2009. Go to original source...
    33. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y., Shinozaki, K.: Monitoring the expression of 7 000 Arabidopsis genes under drought, cold and high-salinity stresses using a full length cDNA microarray. - Plant J. 31: 279-292, 2002. Go to original source...
    34. Strasser, B.J., Strasser, R.J.: Measuring fast fluorescence transients to address environmental questions: the JIP-test. - In: Mathis, P. (ed.): Photosynthesis: From Light to Biosphere. Vol. 5. Pp. 977-980. Kluwer Academic Publisher, Dordrecht 1995. Go to original source...
    35. Strasser, R.J., Tsimilli-Michael, M., Srivastava, A.: Analysis of the fluorescence transient. - In: George, C., Papageorgiou, C., Govindjee. (ed.): Chlorophyll Fluorescence: A Signature of Photosynthesis. Pp. 321-362. Advances in Photosynthesis and Respiration. Springer, Dordrecht 2004. Go to original source...
    36. Thakur, P., Kumar, S., Malik, J.A., Berger, J.D., Nayyar, H.: Cold stress effects on reproductive development in grain crops: an overview. - Environ. exp. Bot. 67: 429-443, 2010. Go to original source...
    37. Thomashow, M.F.: Plant cold acclimation. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571-599, 1999. Go to original source...
    38. Toda, K., Takahashi, R., Iwashina, T., Hajika, M.: Difference in chilling-induced flavonoid profiles, antioxidant activity and chilling tolerance between soybean near-isogenic lines for the pubescence color gene. - J. Plant Res. 124: 173-182, 2011. Go to original source...
    39. Turan, Ö., Ekmekçi, Y.: Chilling tolerance of Cicer arietinum lines evaluated by photosystem II and antioxidant activities. - Turk. J. Bot. 38: 499-510, 2014. Go to original source...
    40. Wang, S.Y., Jiao, H.J., Faust, M.: Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. - Physiol. Plant. 82: 231-236, 1991. Go to original source...
    41. Weimberg, R.: Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. - Physiol. Plant. 70: 381-388, 1987. Go to original source...

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