Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments
Viola Devasirvatham A B C D , Pooran M. Gaur B , Nalini Mallikarjuna B , Raju N. Tokachichu A , Richard M. Trethowan A and Daniel K. Y. Tan A CA Faculty of Agriculture and Environment, Plant Breeding Institute, University of Sydney, Cobbitty, NSW 2570, Australia.
B International Crops Research Institute for the Semiarid Tropics, Patancheru, Hyderabad, 502 324, AP, India.
C Suite 401, Biomedical Building, 1 Central Avenue, Australian Technology Park, Eveleigh, NSW 2015, Australia.
D Corresponding author. Email: viola.devasirvatham@sydney.edu.au
Functional Plant Biology 39(12) 1009-1018 https://doi.org/10.1071/FP12033
Submitted: 30 January 2012 Accepted: 14 August 2012 Published: 17 September 2012
Abstract
High temperature during the reproductive stage in chickpea (Cicer arietinum L.) is a major cause of yield loss. The objective of this research was to determine whether that variation can be explained by differences in anther and pollen development under heat stress: the effect of high temperature during the pre- and post-anthesis periods on pollen viability, pollen germination in a medium, pollen germination on the stigma, pollen tube growth and pod set in a heat-tolerant (ICCV 92944) and a heat-sensitive (ICC 5912) genotype was studied. The plants were evaluated under heat stress and non-heat stress conditions in controlled environments. High temperature stress (29/16°C to 40/25°C) was gradually applied at flowering to study pollen viability and stigma receptivity including flower production, pod set and seed number. This was compared with a non-stress treatment (27/16°C). The high temperatures reduced pod set by reducing pollen viability and pollen production per flower. The ICCV 92944 pollen was viable at 35/20°C (41% fertile) and at 40/25°C (13% fertile), whereas ICC 5912 pollen was completely sterile at 35/20°C with no in vitro germination and no germination on the stigma. However, the stigma of ICC 5912 remained receptive at 35/20°C and non-stressed pollen (27/16°C) germinated on it during reciprocal crossing. These data indicate that pollen grains were more sensitive to high temperature than the stigma in chickpea. High temperature also reduced pollen production per flower, % pollen germination, pod set and seed number.
Additional keywords: anther, high temperature, pollen viability, post-anthesis, pre-anthesis.
References
Ahmed FE, Hall AE, DeMason DA (1992) Heat injury during floral development in cowpea (Vigna unguiculata). American Journal of Botany 79, 784–791.| Heat injury during floral development in cowpea (Vigna unguiculata).Crossref | GoogleScholarGoogle Scholar |
Aist JR (1976) Papillae and related wound plugs of plant cells. Annual Review of Phytopathology 14, 145–163.
| Papillae and related wound plugs of plant cells.Crossref | GoogleScholarGoogle Scholar |
Alexander MP (1969) Differential staining of aborted and non-aborted pollen. Biotechnic & Histochemistry 44, 117–122.
| Differential staining of aborted and non-aborted pollen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M7ptlajug%3D%3D&md5=e11bf1c853360db93d265ceedcc2af18CAS |
Baker HG, Baker I (1979) Starch in angiosperm pollen grains and its evolutionary significance. American Journal of Botany 66, 591–600.
| Starch in angiosperm pollen grains and its evolutionary significance.Crossref | GoogleScholarGoogle Scholar |
Bassiri A, Ahmad F, Slinkard AE (1987) Pollen grain germination and pollen tube growth following in vivo and in vitro self and interspecific pollinations in annual Cicer species. Euphytica 36, 667–675.
| Pollen grain germination and pollen tube growth following in vivo and in vitro self and interspecific pollinations in annual Cicer species.Crossref | GoogleScholarGoogle Scholar |
Basu PS, Ali M, Chaturvedi SK (2009) Terminal heat stress adversely affects chickpea productivity in Northern India – strategies to improve thermotolerance in the crop under climate change. In ‘ISPRS archives XXXVIII-8/W3 workshop proceedings: impact of climate change on agriculture’. (Eds S Panigrahy, SR Shankar, JS Parihar) pp. 189–193. (International Society for Photogrammetry and Remote Sensing: New Delhi, India)
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. American Journal of Botany 50, 859–865.
| The essential role of calcium ion in pollen germination and pollen tube growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2cXhvVajtA%3D%3D&md5=92cbf93f9f1d2cabdcbb1c458fe0458fCAS |
Clarke HJ, Khan TN, Siddique KHM (2004) Pollen selection for chilling tolerance at hybridisation leads to improved chickpea cultivars. Euphytica 139, 65–74.
| Pollen selection for chilling tolerance at hybridisation leads to improved chickpea cultivars.Crossref | GoogleScholarGoogle Scholar |
De Beer JF (1963) Influences of temperature on Arachis hypogaea L. with special reference to its pollen viability. PhD thesis, The State Agricultural University, Wageningen, The Netherlands.
Devasirvatham V, Tan DKY, Trethowan RM, Gaur PM, Mallikarjuna N (2010) Impact of high temperature on the reproductive stage of chickpea. In ‘Food security from sustainable agriculture. Proceedings of the 15th Australian Society of Agronomy Conference’. (Eds H Dove, RA Culvenor) (Australian Society of Agronomy: Lincoln, New Zealand)
Dumas C, Knox RB (1983) Callose and determination of pistil viability and incompatibility. Theoretical and Applied Genetics 67, 1–10.
| Callose and determination of pistil viability and incompatibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkvVGjtQ%3D%3D&md5=1218b8e0142d87842bd7581c3f6530caCAS |
Duthion C, Pigeaire A (1991) Seed lengths corresponding to the final stage in seed abortion of three grain legumes. Crop Science 31, 1579–1583.
| Seed lengths corresponding to the final stage in seed abortion of three grain legumes.Crossref | GoogleScholarGoogle Scholar |
Gaur PM, Chaturvedi SK, Tripathi S, Gowda CLL, Krishnamurthy L, Vadez V, Mallikarjuna N, Varshney RK (2010) Improving heat tolerance in chickpea to increase its resilience to climate change. In ‘Proceeding of the 5th International food legumes research conference and 7th European conference on grain legume’. pp. 26–30. (European Association for the Grain Legume Research: Antalya, Turkey)
Goldberg RB, Beals TP, Sanders TM (1993) Anther development: principles and practical applications. The Plant Cell 5, 1217–1229.
Gross Y, Kigel J (1994) Differential sensitivity to high temperature of stages in the reproductive development in common bean (Phaseolus vulgaris L.). Field Crops Research 36, 201–212.
| Differential sensitivity to high temperature of stages in the reproductive development in common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar |
Halterlein AJ, Clayberg CD, Teare ID (1980) Influence of high temperature on pollen grain viability and pollen tube growth in the styles of Phaseolus vulgaris L. Journal of the American Society for Horticultural Science 105, 12–14.
Hoekstra FA (1979) Mitochondrial development and activity of binucleate and trinucleate pollen during germination in vitro. Planta 145, 25–36.
| Mitochondrial development and activity of binucleate and trinucleate pollen during germination in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlslWktb4%3D&md5=7e7ff620e2bc8267532b512143fa056cCAS |
Hoekstra FA (1983) Physiological evolution in angiosperm pollen: possible role of pollen vigour. In ‘Pollen – biology and implications for plant breeding’. (Eds DL Mulcahy, E Ottaviano) pp. 35–41. (Elsevier: New York)
Hoekstra FA, Bruinsma J (1979) Protein synthesis of binucleate and trinucleate pollen and its relationship to tube emergence and growth. Planta 146, 559–566.
| Protein synthesis of binucleate and trinucleate pollen and its relationship to tube emergence and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtVOmurw%3D&md5=14437fb190bbeb72472d09e1c1b77e14CAS |
Iwanami Y, Sasakuma T, Yamada Y (1988) Physiology of pollen. In ‘Pollen: illustrations and scanning electronmicrographs’. pp. 141–150. (Springer-Verlag: Berlin)
Kalra N, Chakraborty D, Sharma A, Rai HK, Jolly M, Chander S, Kumar PR, Bhadraray S, 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.
Keijzer CJ (1983) Hydration changes during anther development. In ‘Pollen – biology and implications for plant breeding’ (Eds DL Mulcahy, E Ottaviano) pp. 197–201. (Elsevier: New York)
Koti S, Reddy KR, Reddy VR, Kakani VG, Zhao D (2005) Interactive effects of carbon dioxide, temperature, and ultraviolet-B radiation on soybean (Glycine max L.) flower and pollen morphology, pollen production, germination, and tube lengths. Journal of Experimental Botany 56, 725–736.
| Interactive effects of carbon dioxide, temperature, and ultraviolet-B radiation on soybean (Glycine max L.) flower and pollen morphology, pollen production, germination, and tube lengths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2rur0%3D&md5=6932a8655c9ce4575dc7429e65525913CAS |
Krishnamurthy L, Gaur PM, Basu PS, Chaturvedi SK, Tripathi S, Vadez V, Rathore A, Varshney RK, Gowda CLL (2011) Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm. Plant Genetic Resources 9, 59–69.
| Large genetic variation for heat tolerance in the reference collection of chickpea (Cicer arietinum L.) germplasm.Crossref | GoogleScholarGoogle Scholar |
Mallikarjuna N, Mcgrew S, Reinerson S, Rajesh PN, Coyne C, Muehlbauer FJ (2007) Pollen as a means of international transfer of germplasm. Journal of SAT Agricultural Research 3, 1–3.
Nakano H, Momonoki T, Miyashige T, Otsuka H, Hanada T, Sugimoto A, Nakagawa H, Matsuoka M, Terauchi T, Kobayashi M, Oshiro M, Yasuda K, Vanichwattanarumruk N, Chotechuen S, Boonmalison D (1997) ‘Haibushi’, a new variety of snap bean tolerant to heat stress. Japan International Research Center for Agriculture Science Journal 5, 1–12.
Nakano H, Kobayashi M, Terauchi T (1998) Sensitive stages to heat stress in pod setting of common bean (Phaseolus vulgaris L.). Japanese Journal of Tropical Agriculture 42, 78–84.
Nayyar H, Bains T, Kumar S (2005) Low temperature induced floral abortion in chickpea: relationship to abscisic acid and cryoprotectants in reproductive organs. Environmental and Experimental Botany 53, 39–47.
| Low temperature induced floral abortion in chickpea: relationship to abscisic acid and cryoprotectants in reproductive organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksVOr&md5=e701922995969edac2960c62448b789fCAS |
Ormrod DP, Woolley CJ, Eaton GW, Stobbe EH (1967) Effect of temperature on embryo sac development in Phaseolus vulgaris L. Botany 45, 948–950.
| Effect of temperature on embryo sac development in Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar |
Ozalkan C, Sepetoglu H, Daur I, Sen OF (2010) Relationship between some growth parameters and grain yield of chickpea (Cicer arietinum L.) during different growth stages. Turkish Journal of Field Crops 15, 79–83.
Palmer RG, Albertsen MC, Heer H (1978) Pollen production in soybean with respect to genotype, environment, and stamen position. Euphytica 27, 427–433.
| Pollen production in soybean with respect to genotype, environment, and stamen position.Crossref | GoogleScholarGoogle Scholar |
Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male fertile and male sterile tomatoes. Plant, Cell & Environment 21, 225–231.
| Comparing heat stress effects on male fertile and male sterile tomatoes.Crossref | GoogleScholarGoogle Scholar |
Porch TG, Jahn M (2001) Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant, Cell & Environment 24, 723–731.
| Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar |
Prasad PVV, Craufurd PQ, Summerfield RJ (1999a) Sensitivity of peanut to timing of heat stress during reproductive development. Crop Science 39, 1352–1359.
| Sensitivity of peanut to timing of heat stress during reproductive development.Crossref | GoogleScholarGoogle Scholar |
Prasad PVV, Craufurd PQ, Summerfield RJ (1999b) Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress. Annals of Botany 84, 381–386.
| Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress.Crossref | GoogleScholarGoogle Scholar |
Prasad PVV, Craufurd PQ, Summerfield RJ, Wheeler TR (2000) Effects of short episode to heat stress on flower production and fruit-set of groundnut (Arachis hypogaea L.). Journal of Experimental Botany 51, 777–784.
| Effects of short episode to heat stress on flower production and fruit-set of groundnut (Arachis hypogaea L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsL0%3D&md5=4312706482c97137992856634e6d25c4CAS |
Prasad PVV, Craufurd PQ, Kakani VG, Wheeler TR, Boote KJ (2001) Influence of high temperature during pre- and post-anthesis stages of floral development on fruit set and pollen germination in peanut. Functional Plant Biology 28, 233–240.
| Influence of high temperature during pre- and post-anthesis stages of floral development on fruit set and pollen germination in peanut.Crossref | GoogleScholarGoogle Scholar |
Saini HS, Sedgley M, Aspinall D (1984) Development anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Functional Plant Biology 11, 243–253.
Sakata T, Higashitani A (2008) Male sterility accompanied with abnormal anther development in plants – genes and environmental stresses with special reference to high temperature injury. International Journal of Plant Developmental Biology 2, 42–51.
Shivanna KR (2003) ‘Pollen biology and biotechnology.’ (Scientific Publishers: Enfield, NH)
Singh F, Diwakar B (1995) Chickpea botany and production practices. Skill development series no. 16. (International Crops Research Institute for the Semi-Arid Tropics, Patancheru, India.
Srinivasan A, Saxena NP, Johansen C (1999) Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): genetic variation in gamete development and function. Field Crops Research 60, 209–222.
| Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): genetic variation in gamete development and function.Crossref | GoogleScholarGoogle Scholar |
Stanley RG, Linskens HF (1974) Carbohydrates and cell walls. In ‘Pollen – biology, biochemistry management’. pp. 133–135. (Springer: New York)
Summerfield RJ, Wien HC (1980) Effects of photoperiod and air temperature on growth and yield of economic legumes. In ‘Advances in legumes sciences. Proceedings of the International Legumes Conference. Vol. 1’. (Eds RJ Summerfield, AH Bunting) pp. 17–36. (Royal Botanic Gardens: Kew, UK)
Summerfield RJ, Virmani SM, Roberts EH, Ellis RH (1990) Adaption of chickpea to agroclimatic constraints. In ‘Chickpea in the nineties. Proceedings of the 2nd International workshop on chickpea improvement’. (Eds HA van Rheenen, MC Saxena) pp. 50–61. (ICRISAT Center: Hyderabad, India)
Suzuki K, Takeda H, Tsukaguchi T, Egawa Y (2001) Ultra structural study of degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat-stress. Sexual Plant Reproduction 13, 293–299.
| Ultra structural study of degeneration of tapetum in anther of snap bean (Phaseolus vulgaris L.) under heat-stress.Crossref | GoogleScholarGoogle Scholar |
Talwar HS, Yanagihara S (1999) Physiological basis of heat tolerance during flowering and pod setting stages in groundnut (Arachis hypogaea L.). In ‘JIRCAS Workshop report no. 14’. pp. 47–65 (JIRCAS: Tsubuka, Japan)
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 |
Wang J, Gan YT, Clarke F, McDonald CL (2006) Response of chickpea yield to high temperature stress during reproductive development. Crop Science 46, 2171–2178.
| Response of chickpea yield to high temperature stress during reproductive development.Crossref | GoogleScholarGoogle Scholar |
Warrag MOA, Hall AE (1984) Reproductive responses of cowpea (Vigna unguiculata L. Walp.) to heat stress – II Responses to night air temperature. Field Crops Research 8, 17–33.
| Reproductive responses of cowpea (Vigna unguiculata L. Walp.) to heat stress – II Responses to night air temperature.Crossref | GoogleScholarGoogle Scholar |