Abstract
Identifying a potential crop wild relative (CWR) of legumes, especially one with high abiotic stress tolerance, has been a priority of plant breeders for many decades. Traditionally CWRs have been selected based on biometrical traits observed in the field, however this methodology is insufficient for research into nonmorphological traits such as stress tolerance. Biochemical and molecular analysis of potential CWRs allows for more informed selection. Specifically, we focus on Cicer microphyllum Benth, a CWR of cultivated chickpea Cicer arietinum L., which is distributed in Trans Himalayan ranges adjacent to glaciers of India and Pakistan at the alpine altitude gradient between 2700 to 6000 m. The objective of this study is to begin characterization of the biochemical and molecular bases of adaptation of C. microphyllum to cold stress and compare it to its cultivated relative (Cold susceptible genotype ILC533). Significant differences were recorded in terms of malondialdehyde (MDA) concentration, electrolyte leakage and proline accumulation in C. microphyllum, as compared to C. arietinum, upon cold exposure (4°C/24h). C. microphyllum exhibits more membrane stability under cold stress. Furthermore, proline overaccumulation and an increase in the enzymatic activities of antioxidants including superoxide dismutase, catalase, and ascorbate peroxidase were also observed in C. microphyllum under cold stress treatment. Expression of pyrroline-5-carboxylate synthetase, chalcone reductase, flavonoid 3',5'-hydroxylase and flavonoid 3'-monooxygenase are all upregulated under cold treatment in C. microphyllum. The characteristics recommend C. microphyllum both as a model for plant response to cold stress and as a potential source for abiotic stress resistant germplasm for chickpea breeding programs.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- CAT:
-
catalase
- CWR:
-
crop wild relative
- EL:
-
electrolyte leakage
- GR:
-
glutathione reductase
- GSSG:
-
oxidized glutathione
- MDA:
-
malondialdehyde
- OD:
-
optical density
- P5CS-D1:
-
pyrroline-5-carboxylate synthetase
- SOD:
-
superoxide dismutase
- GSSG:
-
oxidized glutathione
References
Chandra-Hioe, M.V., Wong, C.H.M., and Arcot, J., The potential use of fermented chickpea and faba bean flour as food ingredients, Plant Foods Hum. Nutr., 2016, vol. 71, pp. 90–95.
Shah, T.M., Atta, B.M., Sarwar, Alam, S., Ali, H., Haq, M.A., and Hassan, M., High yielding kabuli mutant chickpea (Cicer arietinum L.) variety “CM 2008,” Pak. J. Bot., 2010, vol. 42, pp. 3533–3545.
Jha, U.C., Chaturvedi, S.K., Bohra, A., Basu, P.S., Khan, M.S., and Barh, D., Abiotic stresses, constraints and improvement strategies in chickpea, Plant Breed., 2014, vol. 133, pp. 163–178.
Bohra, A., Pandey, M.K., Jha, U.C., Singh, B., Singh, I.P., Datta, D., Chaturvedi, S.K., Nadarajan, N., and Varshney, R.K., Genomics-assisted breeding in four major pulse crops of developing countries: present status and prospects, Theor. Appl. Genet., 2014, vol. 127, pp. 1263–1291.
Khoury, C.K., Castañeda-Alvarez, N.P., Achicanoy, H.A., Sosa, C.C., Bernau, V., Kassa, M.T., Norton, S.L., Crop wild relatives of pigeonpea [Cajanus cajan (L.) Millsp.]: distributions, ex situ conservation status, and potential genetic resources for abiotic stress tolerance, Biol. Conserv., 2015, vol. 184, pp. 259–270.
Dar, A.A., Rath, S.K., Qaudri, A., Singh, B., Tasduq, S.A., Kumar, A., and Sangwan, P.L., Isolation, cytotoxic evaluation, and simultaneous quantification of eight bioactive secondary metabolites from Cicer microphyllum by high-performance thin-layer chromatography, J. Sep. Sci., 2015, vol. 38, pp. 4021–4028.
Ma, L., Sun, X., Kong, X., Galvan, J.V., Li, X., Yang, S., Yang, Y., Yang, Y., and Hu, X., Physiological, biochemical and proteomics analysis reveals the adaptation strategies of the alpine plant Potentilla saundersiana at altitude gradient of the Northwestern Tibetan Plateau, J. Proteomics, 2015, vol. 112, pp. 63–82.
Bernal, M., Llorens, L., Julkunen-Tiitto, R., Badosa, J., and Verdaguer, D., Altitudinal and seasonal changes of phenolic compounds in Buxus sempervirens leaves and cuticles, Plant Physiol. Biochem., 2013, vol. 70, pp. 471–482.
Singh, R.K., Singh, S., Pandey, P., Anandhan, S., Goyary, D., Pande, V., and Ahmed, Z., Construction of cold induced subtracted cDNA library from Cicer microphyllum and transcript characterization of identified novel wound induced gene, Protoplasma, 2013, vol. 250, pp. 459–469.
Stoddard, F.L., Balko, C., Erskine, W., Khan, H.R., Link, W., and Sarker, A., Screening techniques and sources of resistance to abiotic stresses in cool-season food legumes, Euphytica, 2006, vol. 147, pp. 167–186.
Roorkiwal, M., von Wettberg, E.J., Upadhyaya, H.D., Warschefsky, E., Rathore, A., Varshney, R.K., and Zhang, T., Exploring germplasm diversity to understand the domestication process in Cicer spp. using SNP and DArT markers, PLoS One, 2014, vol. 9: e102016.
Heath, R.L. and Packer, L., Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.
Bates, L.S., Waldren, R.P., and Teare, I.D., Rapid determination of free proline for water-stress studies, Plant Soil, 1973, vol. 39, pp. 205–207.
Beyer, W.F. and Fridovich, I., Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions, Anal. Biochem., 1987, vol. 161, pp. 559–566.
Aebi, H., Catalase in vitro, Methods Enzymol., 1984, vol. 105, pp. 121–126.
Foyer, C.H. and Halliwell, B., The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism, Planta, 1976, vol. 133, pp. 21–25.
Bartoli, C.G., Casalongué, C.A., Simontacchi, M., Marquez-Garcia, B., and Foyer, C.H., Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress, Environ. Exp. Bot., 2013, vol. 94, pp. 73–88.
Shao, H., Chu, L.Y., Shao, M.A., Jaleel, C.A., and Hong-Mei, M., Higher plant antioxidants and redox signaling under environmental stresses, C. R. Biol., 2008, vol. 331, pp. 433–441.
Chen, Y., Jiang, J., Chang, Q., Gu, C., Song, A., Chen, S., Dong, B., and Chen, F., Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species, Mol. Biol. Rep., 2014, vol. 41, pp. 815–822.
Zheng, L., Dang, Z., Li, H., Zhang, H., Wu, S., and Wang, Y., Isolation and characterization of a Δ1-pyrroline-5-carboxylate synthetase (NtP5CS) from Nitraria tangutorum Bobr. and functional comparison with its Arabidopsis homologue, Mol. Biol. Rep., 2014, vol. 41, pp. 563–572.
Asada, K., The water–water cycle in chloroplast: scavenging of active oxygens and dissipation of excess photons, Annu. Rev. Plant Biol., 1999, vol. 50, pp. 601–639.
Torres, M.A., ROS in biotic interactions, Physiol. Plant., 2010, vol. 138, pp. 414–429.
Van Breusegem, F., Vranová, E., Dat, J.F., and Inzé, D., The role of active oxygen species in plant signal transduction, Plant Sci., 2001, vol. 161, pp. 405–414.
Mittler, R., Oxidative stress, antioxidants and stress tolerance, Trends Plant Sci., 2002, vol. 7, pp. 405–410.
Zobayed, S.M.A., Afreen, F., and Kozai, T., Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s wort, Plant Physiol. Biochem., 2005, vol. 43, pp. 977–984.
Guillet, G., Podeszfinski, C., Regnault-Roger, C., Arnason, J.T., and Philogène, B.J.R., Behavioral and biochemical adaptations of generalist and specialist herbivorous insects feeding on Hypericum perforatum (Guttiferae), Environ. Entomol., 2000, vol. 29, pp. 135–139.
Pan, H., Li, X., Cheng, X., Wang, X., Fang, C., Zhou, T., and Chen, J., Evidence of calycosin-7-O- β-d-glucoside’s role as a major antioxidant molecule of Astragalus membranaceus Bge. var. mongholicus (Bge.) Hsiao plants under freezing stress, Environ. Exp. Bot., 2015, vol. 109, pp. 1–11.
Xu, J., Li, Y., Sun, J., Du, L., Zhang, Y., Yu, Q., and Liu, X., Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance, Plant Biol., 2013, vol. 15, pp. 292–303.
Ahmed, I.M., Nadira, U.A., Bibi, N., Cao, F., He, X., Zhang, G., and Wu, F., Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley, Environ. Exp. Bot., 2015, vol. 111, pp. 1–12.
Rana, J.C., Pradheep, K., Chaurasia, O.P., Sood, S., Sharma, R.M., Singh, A., and Negi, R., Genetic resources of wild edible plants and their uses among tribal communities of cold arid region of India, Genet. Resour. Crop Evol., 2012, vol. 59, pp. 135–149.
Author information
Authors and Affiliations
Corresponding author
Additional information
The article is published in the original.
Rights and permissions
About this article
Cite this article
Singh, R.K., Singh, S., Anandhan, S. et al. First insights into the biochemical and molecular response to cold stress in Cicer microphyllum, a crop wild relative of chickpea (Cicer arietinum). Russ J Plant Physiol 64, 758–765 (2017). https://doi.org/10.1134/S1021443717050120
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1021443717050120