Use of morpho-physiological and biochemical traits to identify sources of drought and heat tolerance in chickpea (Cicer arietinum)
Shayla Bindra A , Inderjit Singh A , Satinder Singh A , Ashutosh Kushwah A , B. S. Gill A , Sonia Salaria A , Karan Kapoor A , Satvir Kaur Grewal
B , C. Bharadwaj C , Harsh Nayyar D and Sarvjeet Singh A E
+ Author Affiliations
- Author Affiliations
A Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana, Punjab 141 004, India.
B Department of Biochemistry, Punjab Agricultural University, Ludhiana, Punjab 141 004, India.
C ICAR – Indian Agricultural Research Institute, New Delhi, 110 011, India.
D Department of Botany, Panjab University, Chandigarh, Punjab 160 014, India.
E Corresponding author. Email: sarvjeet62@pau.edu
Crop and Pasture Science 72(10) 801-814 https://doi.org/10.1071/CP21189
Submitted: 16 March 2021 Accepted: 21 May 2021 Published: 18 September 2021
Abstract
Productivity of chickpea (Cicer arietinum) under current climatic conditions is severely limited by water deficit and high temperatures, either alone or in combination. Breeding for improved tolerance, and increasing understanding of the physiological and biochemical mechanisms underlying tolerance, are imperative for achieving yield stabilisation. We evaluated 36 chickpea genotypes including 21 interspecific derivatives (from the cross C. arietinum ICCV96030 × C. pinnatifidum IC525200), their parents, 10 elite genotypes, and three checks (drought tolerant, heat tolerant, drought and heat susceptible) under three environments: timely sowing with irrigation, timely sowing with drought stress, and late sowing leading to heat stress. Four parameters were considered: seed yield, proline content, membrane permeability index, and relative leaf water content. Although the average seed yield plummeted under both stresses, the impact of high temperature was more pronounced. Mean leaf water content declined, whereas membrane permeability index and proline content increased, under both stresses. Leaf water content showed a significant positive correlation with seed yield under all environments, and thus can be employed as an early-stage screening strategy in breeding programs for developing stress tolerant genotypes. Based on estimated stress susceptibility indices for seed yield, derivative line GLW605 was identified as a promising donor for both drought and heat tolerance. Additionally, three derivative lines (GLW607, GLW649, GLW677) were found tolerant to drought, and one derivative line (GLW669) showed tolerance to heat alone. Yield levels of the identified lines were statistically on par with respective tolerant checks. Results suggest that tolerance to drought and heat was successfully introgressed from the wild species, C. pinnatifidum, into the cultivated background. The promising derivative lines can be employed for developing multi-stress tolerant cultivars.
Keywords: abiotic stress, heat tolerance, interspecific derivative, drought resistance, plant–water relations, membrane permeability, proline accumulation, stress tolerance.
References
Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. Journal of Agronomy & Crop Science 197, 177–185.| Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange.Crossref | GoogleScholarGoogle Scholar |
Awasthi R, Gaur P, Turner NC, Vadez V, Siddique KHM, Nayyar H (2017) Effects of individual and combined heat and drought stress during seed filling on the oxidative metabolism and yield of chickpea (Cicer arietinum) genotypes in heat and drought tolerance. Crop & Pasture Science 68, 823–841.
| Effects of individual and combined heat and drought stress during seed filling on the oxidative metabolism and yield of chickpea (Cicer arietinum) genotypes in heat and drought tolerance.Crossref | GoogleScholarGoogle Scholar |
Barnabás B, Jager K, Feher A (2007) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell & Environment 31, 11–38.
| The effect of drought and heat stress on reproductive processes in cereals.Crossref | GoogleScholarGoogle Scholar |
Bates LS, Waldren R, Pand-Teare ID (1973) Rapid determination of free proline for moisture stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for moisture stress studies.Crossref | GoogleScholarGoogle Scholar |
Bayoumi TY, Eid M, Metwali EM (2008) Application of physiological and biochemical indices as a screening technique for drought tolerance in wheat genotypes. African Journal of Biotechnology 7, 2341–2352.
Chakherchaman , Mostafaei H, Yari A, Hassanzadeh M, Jamaati-e-Somarin , Easazadeh R (2009) Study of relationships of leaf relative water content, cell membrane stability and duration of growth period with grain yield of lentil under rainfed and irrigated conditions. Research Journal of Biological Sciences 4, 842–847.
Deshmukh DV, Mhase LB, Jamadagni BM (2004) Evaluation of chickpea genotypes for drought tolerance. Indian Journal of Pulses Research 17, 47–49.
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2017) Drought stress in grain legumes during reproduction and grain filling. Journal of Agronomy & Crop Science 203, 81–102.
| Drought stress in grain legumes during reproduction and grain filling.Crossref | GoogleScholarGoogle Scholar |
Fischer RA, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield response. Australian Journal of Agricultural Research 29, 897–907.
| Drought resistance in spring wheat cultivars. I. Grain yield response.Crossref | GoogleScholarGoogle Scholar |
Gaur PM, Krishnamurthy L, Kashiwagi J (2008) Improving drought-avoidance root traits in chickpea (Cicer arietinum L.): current status of research at ICRISAT. Plant Production Science 11, 3–11.
| Improving drought-avoidance root traits in chickpea (Cicer arietinum L.): current status of research at ICRISAT.Crossref | GoogleScholarGoogle Scholar |
Gaur PM, Jukanti AK, Srinivasan S, Chaturvedi SK, Basu PS, Babbar A, Jayalakshmi AV, Nayyar H, Devasirvatham V, Mallikarjuna N, Krishnamurthy L, Gowda CLL (2013) Climate change and heat stress tolerance in chickpea. In ‘Climate change and plant abiotic stress tolerance’. (Eds N Tuteja, SS Gill) pp. 837–856. (Wiley: New York)
Gaur PM, Samineni S, Thudi M, Tripathi S, Sajja SB, Jayalakshmi V, Mannur DM, Vijaykumar AG, Ganaga Rao NVPR, Ojiewo C, Fikre A, Kimurto P, Kielo RO, Girma N, Chaurvedi SK, Varshney RK, Dixit GP (2019) Integrated breeding approaches for improving drought and heat adaptation in chickpea (Cicer arietinum L.). Plant Breeding 138, 389–400.
| Integrated breeding approaches for improving drought and heat adaptation in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |
Gunes A, Pilbeam DJ, Inal A, Coban S (2008) Influence of silicon on sunflower cultivars under drought stress, I: Growth, antioxidant mechanisms, and lipid peroxidation. Communications in Soil Science and Plant Analysis 39, 1885–1903.
| Influence of silicon on sunflower cultivars under drought stress, I: Growth, antioxidant mechanisms, and lipid peroxidation.Crossref | GoogleScholarGoogle Scholar |
Hamwieh A, Imtiaz M (2015) Identifying water-responsive and drought-tolerant chickpea genotypes. Crop & Pasture Science 66, 1003–1011.
| Identifying water-responsive and drought-tolerant chickpea genotypes.Crossref | GoogleScholarGoogle Scholar |
Ismail AM, Hall AE (1999) Reproductive-stage heat tolerance, leaf membrane thermo stability and plant morphology in cowpea. Crop Science 39, 1762–1768.
| Reproductive-stage heat tolerance, leaf membrane thermo stability and plant morphology in cowpea.Crossref | GoogleScholarGoogle Scholar |
Jaleel CA, Gopi R, Sankar B, Gomathinayagam M, Panneerselvam R (2008) Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress. Comptes Rendus Biologies 331, 42–47.
| Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress.Crossref | GoogleScholarGoogle Scholar | 18187121PubMed |
Jukanti AK, Gaur PM, Gowda CIL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. British Journal of Nutrition 108, S11–S26.
| Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review.Crossref | GoogleScholarGoogle Scholar |
Kalra N, Chakraborty D, Sharma A, Rai HK, Jolly M, Chander S, Kumar PR, Bhadraray , Barman D, Mittal RB, Lal M, Sehgal M (2008) Effect of increasing temperature on yield of some winter crops in northwest India. Current Science 94, 82–88.
Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Gaur PM (2008) Rapid screening technique for canopy temperature status and its relevance to drought tolerance improvement in chickpea. Journal of SAT Agricultural Research 6, 1–4.
Kaur D, Grewal SK, Kaur J, Singh I, Singh S (2016) Water deficit stress tolerance in chickpea is mediated by the contribution of integrative defence systems in different tissues of the plant. Functional Plant Biology 43, 903–918.
| Water deficit stress tolerance in chickpea is mediated by the contribution of integrative defence systems in different tissues of the plant.Crossref | GoogleScholarGoogle Scholar | 32480514PubMed |
Kaur D, Grewal SK, Kaur J, Singh S (2017) Differential proline metabolism in vegetative and reproductive tissues determines drought tolerance in chickpea. Biologia Plantarum 61, 359–366.
| Differential proline metabolism in vegetative and reproductive tissues determines drought tolerance in chickpea.Crossref | GoogleScholarGoogle Scholar |
Kaushal N, Awasthi R, Gupta K, Gaur PM, Siddique KHM, Nayyar H (2013) Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Functional Plant Biology 40, 1334–1349.
| Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers.Crossref | GoogleScholarGoogle Scholar | 32481199PubMed |
Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semi arid environments. Advances in Agronomy 72, 107–138.
| Genetics of flowering time in chickpea and its bearing on productivity in semi arid environments.Crossref | GoogleScholarGoogle Scholar |
Kumar N, Nandwal AS, Yadav R, Bhasker P, Kumar S, Devi S, Singh S, Lather VS (2012) Assessment of chickpea genotypes for high temperature tolerance. Indian Journal of Plant Physiology 17, 225–232.
Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Frontiers in Chemistry 6, 26–30.
| Heat and drought stresses in crops and approaches for their mitigation.Crossref | GoogleScholarGoogle Scholar | 29520357PubMed |
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment 25, 275–294.
| Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.Crossref | GoogleScholarGoogle Scholar |
Li Y, Ruperao P, Batley J, Edwards D, Khan T, Colmer TD, Pang J, Siddique KHM, Sutton T (2018) Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Frontiers in Plant Science 9, 190
| Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data.Crossref | GoogleScholarGoogle Scholar | 29515606PubMed |
Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiology 156, 1921–1933.
| Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress.Crossref | GoogleScholarGoogle Scholar | 21670222PubMed |
Nayyar H, Gupta D (2006) Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants. Environmental and Experimental Botany 58, 106–113.
| Differential sensitivity of C3 and C4 plants to water deficit stress: association with oxidative stress and antioxidants.Crossref | GoogleScholarGoogle Scholar |
Nayyar H, Walia DP (2004) Genotypic variation in wheat in response to water stress and abscisic acid induced accumulation of osmolytes in developing grains. Journal of Agronomy & Crop Science 190, 39–45.
| Genotypic variation in wheat in response to water stress and abscisic acid induced accumulation of osmolytes in developing grains.Crossref | GoogleScholarGoogle Scholar |
Nayyar H, Kaur S, Kumar SS, Singh KJ, Dhir KK (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max) to water deficit stress. Botanical Bulletin of Academia Sinica 46, 333–338.
Nayyar H, Singh S, Kaur S, Kumar S, Upadhyaya HD (2006) Differential sensitivity of macrocarpa and microcarpa types of chickpea (Cicer arietinum L.) to water stress: association of contrasting stress response with oxidative injury. Journal of Integrative Plant Biology 48, 1318–1329.
| Differential sensitivity of macrocarpa and microcarpa types of chickpea (Cicer arietinum L.) to water stress: association of contrasting stress response with oxidative injury.Crossref | GoogleScholarGoogle Scholar |
Patel PK, Hemantaranjan A, Sarma BK, Singh R (2011) Growth and antioxidant system under drought stress in chickpea (Cicer arietinum L.) as sustained by salicylic acid. Journal of Stress Physiology & Biochemistry 7, 130–144.
Premachandra GS, Saneoka H, Ogata S (1990) Cell membrane stability, an indicator of drought tolerance as affected by applied nitrogen in soybean. The Journal of Agricultural Science 115, 63–66.
| Cell membrane stability, an indicator of drought tolerance as affected by applied nitrogen in soybean.Crossref | GoogleScholarGoogle Scholar |
Pushpavalli R, Krishnamurthy L, Thudi M, Gaur PM, Rao MV, Siddique KHM, Colmer TD, Turner NC, Varshney RK, Vadez V (2015) Two key genomic regions harbour QTLs for salinity tolerance in ICCV 2 × JG 11 derived chickpea (Cicer arietinum L.) recombinant inbred lines. BMC Plant Biology 15, 124
| Two key genomic regions harbour QTLs for salinity tolerance in ICCV 2 × JG 11 derived chickpea (Cicer arietinum L.) recombinant inbred lines.Crossref | GoogleScholarGoogle Scholar | 25994494PubMed |
Rahbarian R, Khavari-Nejad R, Ali G, Bagheri A, Najafi F (2011) Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietinum L.) genotypes. Acta Biologica Cracoviensia. Series; Botanica 53, 47–56.
| Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietinum L.) genotypes.Crossref | GoogleScholarGoogle Scholar |
Rani A, Devi P, Jha UC, Sharma KD, Siddique KHM, Nayyar H (2020) Developing climate-resilient chickpea involving physiological and molecular approaches with a focus on temperature and drought stresses. Frontiers in Plant Science 10, 1759
| Developing climate-resilient chickpea involving physiological and molecular approaches with a focus on temperature and drought stresses.Crossref | GoogleScholarGoogle Scholar | 32161601PubMed |
Rosales-Serna R, Kohashi-Shibata J, Acosta-Gallegos JA, Trejo-López C, Ortiz-Cereceres J, Castillo GFY, Kelly JD (2000) Rendimiento de grano y tolerancia a la sequía del frijol comúnencondiciones de campo. Agrociencia 34, 153–165.
Sabaghpour SH, Mahmodi AA, Saeed A, Kamel M, Malhotra RS (2006) Study on chickpea drought tolerance lines under dryland condition of Iran. Indian Journal of Crop Science 1, 70–73.
Sairam RK, Srivastava GC (2001) Water stress tolerance of wheat (Triticum aestivum L.): variations in hydrogen peroxide accumulation and antioxidant activity in tolerant and susceptible genotypes. Journal of Agronomy & Crop Science 186, 63–70.
| Water stress tolerance of wheat (Triticum aestivum L.): variations in hydrogen peroxide accumulation and antioxidant activity in tolerant and susceptible genotypes.Crossref | GoogleScholarGoogle Scholar |
Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Science 163, 1037–1046.
| Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration.Crossref | GoogleScholarGoogle Scholar |
Salehpour M, Ebadi A, Izadi M, Jamaati-e-Somarin S (2009) Evaluation of water stress and nitrogen fertilizer effects on relative water content, membrane stability index, chlorophyll and some other traits of lentils (Lens culinaris L.) under hydroponics conditions. Research Journal of Environmental Sciences 3, 103–109.
| Evaluation of water stress and nitrogen fertilizer effects on relative water content, membrane stability index, chlorophyll and some other traits of lentils (Lens culinaris L.) under hydroponics conditions.Crossref | GoogleScholarGoogle Scholar |
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10, 296–302.
| Regulatory metabolic networks in drought stress responses.Crossref | GoogleScholarGoogle Scholar | 17468040PubMed |
Shaban M, Lak M, Hamid Y, Nabaty E, Khodaei F, Yarahmadi M, Azimi SM, Rahmat MG, Shaban M, Motlagh ZR (2012) Response of chickpea (Cicer arietinum L.) cultivars to integrated application of zinc nutrient with water stress. International Journal of Agriculture and Crop Sciences 4, 1074–1082.
Siddique KHM, Loss SP, Regan KL, Jettner RL (1999) Adaptation and seed yield of cool season grain legumes in Mediterranean environments of south-western Australia. Australian Journal of Agricultural Research 50, 375–387.
| Adaptation and seed yield of cool season grain legumes in Mediterranean environments of south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Sohrabi Y, Heidari G, Weisany W, Ghasemi Golezani K, Mohammadi K (2012) Some physiological responses of chickpea cultivars to arbuscular mycorrhiza under drought stress. Russian Journal of Plant Physiology 59, 708–716.
| Some physiological responses of chickpea cultivars to arbuscular mycorrhiza under drought stress.Crossref | GoogleScholarGoogle Scholar |
Thudi M, Upadhyaya HD, Rathore A, Gaur PM, Krishnamurthy L, Roorkiwal M, Nayak SN, Chaturvedi SK, Basu PS, Ganagarao NVPR, Fikre A, Kimurto P, Sharma PC, Sheshashayee MS, Tobita S, Kashiwagi J, Ito O, Killian A, Varshney RK (2014) Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene-based association mapping approaches. PLoS One 9, e96758
| Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene-based association mapping approaches.Crossref | GoogleScholarGoogle Scholar | 24801366PubMed |
Toker C, Cagirgan M (1998) Assessment of response to drought stress of chickpea (Cicer arietinum L.) lines under rainfed conditions. Turkish Journal of Agriculture and Forestry 22, 615–621.
Türkan I, Bor M, Ozdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science 168, 223–231.
| Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress.Crossref | GoogleScholarGoogle Scholar |
Upadhyaya HD, Dronavalli N, Gowda CLL, Singh S (2011) Identification and evaluation of chickpea germplasm for tolerance to heat stress. Crop Science 51, 2079–2094.
| Identification and evaluation of chickpea germplasm for tolerance to heat stress.Crossref | GoogleScholarGoogle Scholar |
Varshney RK, Thudi M, May GD, Jackson SA (2010) Legume genomics and breeding. Plant Breeding Reviews 33, 257–304.
Varshney RK, Thudi M, Nayak SN, Gaur PM, Kashiwagi J, Krishnamurthy L, Jaganathan D, Koppolu J, Bohra A, Tripathi S, Rathore A, Jukanti AK, Jayalakshi V, Vemula A, Singh SJ, Yasin M, Sheshshayee MS, Viswanatha KP (2014) Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.). Theoretical and Applied Genetics 127, 445–462.
| Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar | 24326458PubMed |
von Wettberg EJB, Chang PL, Basdemir F, Carrasquila-Garcia N, Korbu LB, Moenga SM, Bedada G, Greenlon A, Moriuchi KS, Singh V, Cordeiro MA, Mnoujdina NV, Dinegde KN, Shah Sani SGA, Getahum T, Vance L, Bergmann E, Lindsay D, Mamo BE, Warchefsky EJ, Dacosta-Calheiros E, Marques E, Yilmaz MA, Cakmak A, Rose J, Migneault A, Kreig CP, Saylak S, Temel H, Friesen ML, Siler E, Akhmeov Z, Ozcelik H, Kholova J, Can C, Gaur P, Yildirim M, Sharma H, Vadez V, Tesfaye K, Woldemedhin AF, Tar’an B, Aydogan A, Bukun B, Penmetsa RV, Berger JJ, Kahraman A, Nuzhdin SV, Cook DR (2018) Ecology and genomics of an important crop wild relative as a prelude to agricultural innovation. Nature Communications 9, 649
| Ecology and genomics of an important crop wild relative as a prelude to agricultural innovation.Crossref | GoogleScholarGoogle Scholar | 29440741PubMed |
Wahid A, Shabbir A (2005) Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycine betaine. Plant Growth Regulation 46, 133–141.
| Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycine betaine.Crossref | GoogleScholarGoogle Scholar |
Weatherley PE (1950) Studies in the water relations of the cotton plant. I. The field measurement of water deficits in leaves. New Phytologist 49, 81–97.
| Studies in the water relations of the cotton plant. I. The field measurement of water deficits in leaves.Crossref | GoogleScholarGoogle Scholar |
Woldeamanuel ME, Ahmad M, Abu-Awwad , Haddad NI (2006) Response of chickpea (Cicer arietinum L.) to soil moisture levels in a semi-arid environment. Dirasat Journal of Agricultural Sciences 33, 200
Zhang X, Ervin EH, Evanylo GK, Haering KC (2009) Impact of biosolids on hormone metabolism in drought-stressed tall fescue. Crop Science 49, 1893–1901.
| Impact of biosolids on hormone metabolism in drought-stressed tall fescue.Crossref | GoogleScholarGoogle Scholar |
