Skip to main content
SpringerLink
Log in

Growth and metabolic responses of contrasting chickpea (Cicer arietinum L.) genotypes to chilling stress at reproductive phase

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Chilling stress (<10°C) at reproductive phase of chickpea results in abortion of flowers and pods leading to poor yield. The metabolic causes associated with cold sensitivity of chickpea are not well understood. Hence, in the present study, we evaluated four chickpea genotypes (ICC 16348, ICC 16349, PBG1 and GPF2) having contrasting cold sensitivity for their reproductive growth and metabolism subjected to cold stress (average day temperature: 17.6°C; average night temperature: 4.9°C). Genotypes ICC 16348 and ICC 16349 showed flowering and set pods, while PBG1 and GPF2 failed to do so during the stress conditions indicating the former to be cold tolerant. The stress injury in the leaves such as increase in electrolyte leakage, decrease in chlorophyll content and relative leaf water content was significantly less in ICC 16348 and ICC 16349 genotypes. The analysis of carbohydrates indicated total sugars and starch to be present in greater content in ICC 16348 and ICC 16349 relative to PBG1 and GPF2 genotypes. The enzymes related to carbohydrate metabolism such as β-amylase, invertase and sucrose synthase showed significantly higher activity in the leaves of ICC 16348 and ICC 16349 compared to the other two genotypes. PBG1 and GPF2 genotypes experienced greater oxidative stress measured as malondialdehyde and hydrogen peroxide. ICCV 16348 and ICC 16349 possessed significantly higher levels of enzymatic (superoxide dismutase, catalase, ascorbate peroxidase) and non-enzymatic antioxidants (proline and ascorbic acid) relative to PBG1 and GPF2. Particularly, proline and ascorbic acid were markedly higher in cold-tolerant genotypes compared to the sensitive ones suggesting their deciding role in governing the cold tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Arnon DI (1949) Copper enzyme in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Tognoni F, Irigoyen JJ, Sánchez-Díaz M, Pardossi A (2001) Different root low temperature response of two maize genotypes differing in chilling sensitivity. Plant Physiol Biochem 39:1067–1073

    Article  CAS  Google Scholar 

  • Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity techniques for estimating water deficits in leaves. Aust J Biol Sci 15:413–428

    Google Scholar 

  • Bates LS, Woldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Bertin P, Bouharmont J, Kinet JM (1997) Somaclonal variation and improvement of chilling tolerance in rice: changes in chilling-induced chlorophyll fluorescence. Crop Sci 37:1727–1735

    Article  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    Article  CAS  Google Scholar 

  • Capell B, Dörffling K (1993) Genotype-specific differences in chilling tolerance of maize in relation to chilling-induced changes in water status and abscisic acid accumulation. Physiol Plant 88:638–646

    Article  CAS  Google Scholar 

  • Chen WP, Li PH (2002) Membrane stabilization by abscisic acid under cold aids proline in alleviating chilling injury in maize (Zea mays L.) cultured cells. Plant Cell Environ 25:955–962

    Article  CAS  Google Scholar 

  • Clarke HJ, Siddique KHM (2004) Response of chickpea genotypes to low temperature stress during reproductive development. Field Crops Res 90:323–334

    Article  Google Scholar 

  • Dhindsa RS, Dhindsa PP, Thorpe TA (1981) Leaf senescence: correlated with increased level of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Du YC, Nose A (2002) Effects of chilling temperature on the activity of enzymes of sucrose synthesis and the accumulation of saccharides in leaves of three sugarcane cultivars differing in cold sensitivity. Photosynthetica 40:389–395

    Article  CAS  Google Scholar 

  • Duncan DR, Widholm JM (1987) Proline accumulation and its implication in cold tolerance of regenerable maize callus. Plant Physiol 83:703–708

    Article  PubMed  CAS  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Grow Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hawker JS, Hatch MD (1965) Mechanism of sugar storage by mature stem tissue of sugarcane. Physiol Plant 18:444–453

    Article  Google Scholar 

  • Hawker JS, Walker RR, Ruffner HP (1976) Invertase and sucrose synthase in flowers. Phytochemistry 15:1411–1443

    Article  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Huang M, Guo Z (2005) Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity. Biol Plant 49:81–84

    Article  CAS  Google Scholar 

  • Ismail MA, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann Bot 103:197–209

    Article  PubMed  CAS  Google Scholar 

  • Janda T, Kósa EI, Szalai G, Páldi E (2005) Investigation of antioxidant activity in maize during low temperature stress. Acta Biol Szegediensis I49:53–54

    Google Scholar 

  • Janowiak F, Dorffling K (1996) Chilling tolerance of 10 maize genotypes as related to chilling-induced changes in ACC and MACC contents. J Agron Crop Sci 177:175–184

    Article  CAS  Google Scholar 

  • Janowiak F, Markowski A (2008) Changes in leaf water relations and injuries in maize seedlings induced by different chilling conditions. J Agron Crop Sci 172:19–28

    Article  Google Scholar 

  • Kaur S, Gupta AK, Kaur N, Sandhu JS, Gupta SK (2009) Antioxidative enzymes and sucrose synthase contribute to cold stress tolerance in chickpea. J Agron Crop Sci 195:393–397

    Article  CAS  Google Scholar 

  • Kocsy G, Brunner M, Rüegsegger A, Stamp P, Brunold C (1996) Glutathione synthesis in maize genotypes with different sensitivity to chilling. Planta 198:365–370

    Article  CAS  Google Scholar 

  • Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117

    Article  CAS  Google Scholar 

  • McReedy RM, Guggolz J, Silviera V, Owens HS (1950) Determination of starch and amylose in vegetables. Anal Chem 22:1156

    Article  Google Scholar 

  • Mitter R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  Google Scholar 

  • Morsy MR, Jouve L, Hausman JF, Hoffmann L, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nayyar H, Gupta D (2006) Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. Environ Exp Bot 58:106–113

    Article  CAS  Google Scholar 

  • Nayyar H, Bains T, Kumar S (2005) Low temperature induced floral abortion in chickpea: relationship to abscisic acid and cryoprotectants in reproductive organs. Environ Exp Bot 53:39–47

    Article  CAS  Google Scholar 

  • Nygaard P (1977) Utilization of exogenous carbohydrates for the growth and starch synthesis in pine pollen suspension cultures. Physiol Plant 39:206–210

    Article  CAS  Google Scholar 

  • Patton AJ, Cunningham SM, Volenec JJ, Reicher ZJ (2007) Differences in freeze tolerance of Zoysia grasses. II. Carbohydrate and proline accumulation. Crop Sci 47:2170–2181

    Article  CAS  Google Scholar 

  • Premchandra GS, Sameoka H, Ogata S (1990) Cell osmotic membrane-stability, an indication of drought tolerance, as affected by applied nitrogen in soil. J Agric Res 115:63–66

    Google Scholar 

  • Sairam RK, Saxena DC (2000) Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. J Agron Crop Sci 184:55–61

    Article  CAS  Google Scholar 

  • Santoiani CS, Tognetti JA, Pontis HG, Salerno GL (2006) Sucrose and fructan metabolism in wheat roots at chilling temperatures. Physiol Plant 87:84–88

    Article  Google Scholar 

  • Saruyama H, Tanida M (1995) Effect of chilling on activated oxygen-scavenging enzymes in low temperature-sensitive and -tolerant cultivars. Plant Sci 109:105–113

    Article  CAS  Google Scholar 

  • Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211

    PubMed  CAS  Google Scholar 

  • Shen W, Nada K, Tachibana S (1999) Effect of chilling treatment on enzymic and non-enzymic antioxidant activities in leaves of chilling tolerant and chilling sensitive cucumber (Cucumis sativus L.). J Jpn Soc Hort Sci 68:967–973

    Article  CAS  Google Scholar 

  • Shuster L, Gifford RH (1962) Assay of amylases. Arch Biochem Biophys 194:534–540

    Article  Google Scholar 

  • Smirnoff N (1995) Antioxidant systems and plant response to the environment. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific Publishers, Oxford, UK, pp 217–243

  • Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235

    PubMed  CAS  Google Scholar 

  • Srinivasan A, Johansen C, Saxena NP (1998) Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): characterization of stress and genetic variation in pod set. Field Crops Res 57:179–191

    Article  Google Scholar 

  • Sumner JB (1935) A more specific reagent for determination of sugar in urine. J Biol Chem 69:393–396

    Google Scholar 

  • Teranishi Y, Tanaka A, Osumi M, Fukui S (1974) Catalase activities of hydrocarbon-utilizing Candida yeasts. Agric Biol Chem 38:1213–1220

    CAS  Google Scholar 

  • Thiaw S, Hall AE (2004) Comparison of selection for either leaf electrolyte-leakage or pod set in enhancing heat tolerance and grain yield of cowpea. Field Crops Res 86:239–253

    Article  Google Scholar 

  • Wang WB, Kim YH, Lee HS, Deng XP, Kwak SS (2009) Differential antioxidation activities in two alfalfa cultivars under chilling stress. Plant Biotech Rep 3:301–307

    Article  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    PubMed  CAS  Google Scholar 

  • Ying J, Lee EA, Tollenaar M (2000) Response of maize leaf photosynthesis to low temperature during the grain-filling period. Field Crops Res 68:87–96

    Article  Google Scholar 

  • Yu JQ, Zhou YH, Huang LF, Allen DJ (2002) Chill-induced inhibition of photosynthesis: genotypic variation within Cucumis sativus. Plant Cell Physiol 43:1182–1188

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Dai JY, Su ZS, Xu SC, Cheng J (1995) The injurious effect of low temperature at booting stage on female inflorescence of maize. Acta Agron Sin 21:235–239

    Google Scholar 

Download references

Acknowledgments

The authors are thankful to DBT (India), DST (India), ICRISAT and DEST (Australia) for funding this work.

Author information

Authors and Affiliations

  1. Department of Botany, Panjab University, Chandigarh, India

    Sanjeev Kumar, Jahid Malik, Prince Thakur, Suchi Kaistha & Harsh Nayyar

  2. Biotechnology Centre, H.P.K.V., Palampur, India

    Kamal Dev Sharma

  3. ICRISAT, Hyderabad, India

    H. D. Upadhyaya

  4. CSIRO Plant Industry, Perth, Australia

    J. D. Berger

Authors
  1. Sanjeev Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jahid Malik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Prince Thakur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Suchi Kaistha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kamal Dev Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. D. Upadhyaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. D. Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Harsh Nayyar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harsh Nayyar.

Additional information

Communicated by P. Sowinski.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kumar, S., Malik, J., Thakur, P. et al. Growth and metabolic responses of contrasting chickpea (Cicer arietinum L.) genotypes to chilling stress at reproductive phase. Acta Physiol Plant 33, 779–787 (2011). https://doi.org/10.1007/s11738-010-0602-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-010-0602-y

Keywords

Search

Navigation