Abstract
The aim of this study was to find a correlation between the freezing tolerance of three chickpea (Cicer arietinum L.) cultivars (İnci, Işık-05, and Sarı-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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- APX:
-
ascorbate peroxidase
- CA:
-
cold acclimation
- CAT:
-
catalase
- Chl:
-
chlorophyll
- RLR:
-
relative leakage ratio
- GR:
-
glutathione reductase
- MDA:
-
malondialdehyde
- RT-qPCR:
-
reverse-transcription quantitative polymerase chain reaction
- PItot :
-
total performance index
- POD:
-
peroxidase
- PS:
-
photosystem
- ROS:
-
reactive oxygen species
- RWC:
-
relative water content
- SOD:
-
superoxide dismutase
References
Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. — Plant Soil 39: 205–207, 1973.
Bergmeyer, H.U.: Methods of Enzymatic Analysis, Vol. II. Section C: Methods for Determination of Enzyme Activity. - Academic Press, New York 1974.
Beyer, W.F., Fridovich, I.: Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. — Anal Biochem. 161: 559–566, 1987.
Borawska-Jarmułowicz, 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.
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.
Burke, J.J., Oliver, M.J.: Differential temperature sensitivity of pea superoxide dismutase. — Plant Physiol. 100: 1595–1598, 1992.
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.
Chance, B., Maehly, A.C.: Assay of catalases and peroxidases. — Methods Enzymol. 2: 764–817, 1955.
Chomczynski, P., Sacchi, N.: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. — Anal. Biochem. 162: 156–159, 1987.
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.
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.
Esterbauer, H., Cheeseman, K.H.: Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. — Methods Enzymol. 186: 407–431, 1990.
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.
Hao, W., Arora, R., Yadav, A.K., Joshee, N.: Freezing tolerance and cold acclimation in guava (Psidium guajava L.). — HortScience 44: 1258–1266, 2009.
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.
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.
Janská, A., Maršík, P., Zelenková, S., Ovesná, J.: Cold stress and acclimation-what is important for metabolic adjustment?. — Plant Biol. 12: 395–405, 2010.
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.
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.
Kalaji, H.M., Jajoo, A., Oukarroum, A., Brestic, M., Zivcak, M., Samborska, I.A., Center, M.D., Łukasik, 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.
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.
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.
Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T(4). — Nature 227: 680–685, 1970.
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.
Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Method. Enzymol. 148: 350–382, 1987.
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.
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.
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.
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.
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.
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.
Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V.: Cold signalling and cold acclimation in plants. — Adv. bot. Res. 49: 35–150, 2009.
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.
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.
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.
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.
Thomashow, M.F.: Plant cold acclimation. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571–599, 1999.
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.
Turan, Ö., Ekmekçi, Y.: Chilling tolerance of Cicer arietinum lines evaluated by photosystem II and antioxidant activities. — Turk. J. Bot. 38: 499–510, 2014.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: The authors gratefully acknowledge the financial support of the Scientific Research Unit (Project No. 801601007) of the Hacettepe University.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Arslan, Ö., Eyidoğan, F. & Ekmekçi, Y. Freezing tolerance of chickpea: biochemical and molecular changes at vegetative stage. Biol Plant 62, 140–148 (2018). https://doi.org/10.1007/s10535-017-0760-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-017-0760-5