Acta Physiologiae Plantarum

, 41:181 | Cite as

Cross-priming accentuates key biochemical and molecular indicators of defense and improves cold tolerance in chickpea (Cicer arietinum L.)

  • Rashmi Saini
  • Arindam Adhikary
  • Harsh Nayyar
  • Sanjeev KumarEmail author
Original Article


Cold environment favors long vegetative phase but also impose substantial loss by damaging reproductive functioning in chickpea. Field temperature below 10 °C is even more detrimental for reproductive development, enhances floral and pod abortion. In this study, contrasting chickpea varieties PDG3 and GPF2 were exposed to drought, recovered, and subsequently exposed to lethal cold stress ~ 4–5 °C with an aim to induce defense response against cold shock. Physiological, biochemical, and molecular signatures related to damage and defense, i.e., membrane damage, antioxidative enzymes, fatty acid desaturase (CaFAD2.1), and small HSPs (CaHSP18.5 and CaHSP22.7), were analyzed. Drought pretreatment/preconditioning maintained the membrane stability in the cold by managing malondialdehyde (MDA) content and lipoxygenase (LOX) activity. Improved mitochondrial functioning (TTC reduction), increased activity of catalase (CAT), ascorbate peroxidase (APX), and glutathione reductase (GR) proved better cellular functioning during cold exposure. The expression and activity of superoxide dismutase (CaSOD) were down-regulated in both varieties, but CaCAT, CaAPX, CaGR, and CaFAD2.1 expressions were up-regulated in GPF2. Small heat shock protein CaHSP22.7 was also up-regulated in drought preconditioned PDG3 and GPF2 and after cold shock. Drought pretreatment/preconditioning significantly improved membrane damage during cold exposure, induced antioxidative system, and up-regulated FAD2. This study also pointed the possible role of CaHSP22.7 in cold tolerance and CaHSP18.5 in drought stress. The sensitive variety (GPF2) was positively responsive to preconditioning as this variety showed improvement in defense-related parameters; however, genotypic variations were observed in PDG3.


Chickpea Cold stress Drought Antioxidants FAD2 and small heat shock proteins 



Authors are thankful to the Central University of Punjab for providing necessary infrastructure, University Grant Commission for funding the research (UGC-BSR grant) and Indian Council of Medical Research, New Delhi for financial assistance in the form of Junior Research Fellowship.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

11738_2019_2971_MOESM1_ESM.docx (1.1 mb)
Supplementary material 1 (DOCX 1077 kb)
11738_2019_2971_MOESM2_ESM.docx (32 kb)
Supplementary material 2 (DOCX 32 kb)


  1. Aroca R, Irigoyen JJ, Sánchez-Díaz M (2003) Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549CrossRefGoogle Scholar
  2. Banzet N, Richaud C, Deveaux Y, Kazmaier M, Gagnon J, Triantaphylidès C (1998) Accumulation of small heat shock proteins, including mitochondrial HSP22, induced by oxidative stress and adaptive response in tomato cells. Plant J 13:519–527CrossRefGoogle Scholar
  3. Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Cao S, Zheng Y, Wang K, Jin P, Rui H (2009) Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem 115:1458–1463CrossRefGoogle Scholar
  6. Cayuela E, Muñoz-Mayor A, Vicente-Agulló F, Moyano E, Garcia-Abellan JO, Estañ MT, Bolarín MC (2007) Drought pretreatment increases the salinity resistance of tomato plants. J Plant Nutr Soil Sci 170:479–484CrossRefGoogle Scholar
  7. Chakrabarty D, Verma AK, Datta SK (2009) Oxidative stress and antioxidant activity as the basis of senescence in Hemerocallis (day lily) flowers. J Hortic For 1:113–119Google Scholar
  8. Cloutier Y, Siminovitch D (1982) Correlation between cold-and drought-induced frost hardiness in winter wheat and rye varieties. Plant Physiol 69:256–258CrossRefGoogle Scholar
  9. Dong X, Bi H, Wu G, Ai X (2013) Drought-induced chilling tolerance in cucumber involves membrane stabilisation improved by antioxidant system. Int J Plant Prod 7:67–80Google Scholar
  10. Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297CrossRefGoogle Scholar
  11. Garcı́a-Limones C, Hervás A, Navas Cortés JA, Jiménez Dı́az RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris. Physiol Mol Plant Pathol 61:325–337CrossRefGoogle Scholar
  12. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101CrossRefGoogle Scholar
  13. Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266–1274CrossRefGoogle Scholar
  14. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  15. Hernandez J, Jimenez A, Mullineaux P, Sevilia F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  16. Hoffman L, DaCosta M, Ebdon JS, Zhao J (2012) Effects of drought preconditioning on freezing tolerance of perennial ryegrass. Enviro Exp Bot 79:11–20CrossRefGoogle Scholar
  17. Kargiotidou A, Deli D, Galanopoulou D, Tsaftaris A, Farmaki T (2008) Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). J Exp Bot 59:2043–2056CrossRefGoogle Scholar
  18. Kaur S, Jairath A, Singh I, Nayyar H, Kumar S (2016) Alternate mild drought stress (− 0.1 MPa PEG) immunizes sensitive chickpea cultivar against lethal chilling by accentuating the defense mechanisms. Acta Physiol Plant 38:189CrossRefGoogle Scholar
  19. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608CrossRefGoogle Scholar
  20. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406CrossRefGoogle Scholar
  21. Lutts S, Kinet J, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398CrossRefGoogle Scholar
  22. Mantyla E, Lang V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148CrossRefGoogle Scholar
  23. Miquel M, James D, Dooner H (1993) Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc Natl Acad Sci 90:6208–6212CrossRefGoogle Scholar
  24. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  25. Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875CrossRefGoogle Scholar
  26. Nayyar H, Bains T, Kumar S (2005a) Chilling stressed chickpea seedlings: effect of cold acclimation, calcium and abscisic acid on cryoprotective solutes and oxidative damage. Environ Exp Bot 54:275–285CrossRefGoogle Scholar
  27. Nayyar H, Bains TS, Kumar S, Kaur G (2005b) Chilling effects during seed filling on accumulation of seed reserves and yield of chickpea. J Sci Food Agric 85:1925–1930CrossRefGoogle Scholar
  28. Palma F, López Gómez M, Tejera N, Lluch C (2013) Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci 208:75–82CrossRefGoogle Scholar
  29. Pirzadah TB, Malik B, Rehman RU, Hakeem KR, Qureshi MI (2014) Signaling in response to cold stress. Plant signaling: understanding the molecular crosstalk. Springer, New York, pp 193–226CrossRefGoogle Scholar
  30. Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850CrossRefGoogle Scholar
  31. Porta H et al (1999) Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant Cell Physiol 40:850–858CrossRefGoogle Scholar
  32. Rejeb IB, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3:458–475CrossRefGoogle Scholar
  33. Saini R, Kumar S (2019) Genome-wide identification, characterization and in silico profiling of genes encoding FAD (fatty acid desaturase) proteins in chickpea (Cicer arietinum L.). Plant Gene 18:100180CrossRefGoogle Scholar
  34. Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta Gene Struct Expr 1577:1–9CrossRefGoogle Scholar
  35. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105CrossRefGoogle Scholar
  36. Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977CrossRefGoogle Scholar
  37. Verma S, Dubey R (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  38. Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B (2015) Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul 75:677–687CrossRefGoogle Scholar
  39. Zhang J-H, Wang L-J, Pan Q-H, Wang Y-Z, Zhan J-C, Huang W-D (2008) Accumulation and subcellular localization of heat shock proteins in young grape leaves during cross-adaptation to temperature stresses. Sci Hortic 117:231–240CrossRefGoogle Scholar
  40. Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, Zhang X (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166:851–861CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Centre for Biosciences, School of Basic and Applied SciencesCentral University of PunjabBathindaIndia
  2. 2.Department of BotanyPanjab UniversityChandigarhIndia
  3. 3.Department of Plant Sciences, School of Basic and Applied SciencesCentral University of PunjabBathindaIndia

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