Pollen viability as a potential trait for screening heat-tolerant wheat (Triticum aestivum L.)
Mamrutha Harohalli Masthigowda A * , Davinder Sharma A B , Rinki Khobra A , Gopalareddy Krishnappa A , Hanif Khan A , Sanjay Kumar Singh A , Gyanendra Singh A and Gyanendra Pratap Singh AA ICAR-Indian Institute of Wheat and Barley Research, Karnal, 132001 Haryana, India.
B The Institute for cereal crops improvement, Tel Aviv University, Tel Aviv 6997801, Israel.
Functional Plant Biology 49(7) 625-633 https://doi.org/10.1071/FP21096
Submitted: 31 March 2021 Accepted: 16 February 2022 Published: 11 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
High temperature during reproductive stage of winter crops causes sterility of pollen grains and reduced yield. It is essential to find the genotypes with higher pollen viability, as it is most sensitive to temperature extremes. A field study was conducted with wheat (Triticum aestivum L.) genotypes to understand the effect of high temperature on pollen viability and grain yield for 2 years under timely (TS) and late sown (LS) conditions. A strong correlation was observed between higher pollen viability and higher grain yield under heat stress condition. Genotypes like K7903, HD2932, WH730 and RAJ3765 showed higher pollen viability, whereas DBW17, HUW468, RAJ4014 and UP2425 had lower pollen viability under LS condition. Further, the quantification of antioxidant enzymes activity mainly, Super oxide dismutase (SOD), Catalase (CAT), Peroxidase (POD) and Glutathione peroxidase (GPX) has showed significant variation among study genotypes. Thus, the identified high pollen viability genotypes can serve as a potential source for trait based breeding under heat stress in wheat. The present study is a first of its kind to assess more number of wheat genotypes for pollen viability and antioxidants activity under field condition. It also confirms that pollen viability can be used as a potential trait to screen genotypes for heat stress tolerance in wheat.
Keywords: aniline blue, antioxidant enzymes, CAT activity, GPX activity, heat stress, pollen viability, SOD activity, wheat.
References
Akter N, Rafiqul Islam M (2017) Heat stress effects and management in wheat. A review. Agronomy for Sustainable Development 37, 37| Heat stress effects and management in wheat. A review.Crossref | GoogleScholarGoogle Scholar |
Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Current Science 82, 1227–1238.
Ba QS, Zhang GS, Wang JS, Che HX, Liu HZ, Niu N, Ma SC, Wang JW (2013) Relationship between metabolism of reactive oxygen species and chemically induced male sterility in wheat (Triticum aestivum L.). Canadian Journal of Plant Science 93, 675–681.
| Relationship between metabolism of reactive oxygen species and chemically induced male sterility in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiologia Plantarum 121, 231–238.
| Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit.Crossref | GoogleScholarGoogle Scholar | 15153190PubMed |
Bheemanahalli R, Sunoj VSJ, Saripalli G, Prasad PVV, Balyan HS, Gupta PK, Grant N, Gill KS, Jagadish SVK (2019) Quantifying the impact of heat stress on pollen germination, seed set, and grain filling in spring wheat. Crop Science 59, 684–696.
| Quantifying the impact of heat stress on pollen germination, seed set, and grain filling in spring wheat.Crossref | GoogleScholarGoogle Scholar |
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273
| Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar | 23914193PubMed |
Bokszczanin KL Bokszczanin KL Bokszczanin KL (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Frontiers in Plant Science 4, 315
| Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance.Crossref | GoogleScholarGoogle Scholar | 23986766PubMed |
Dancy BM, Sedensky MM, Morgan PG (2014) Effects of the mitochondrial respiratory chain on longevity in C. elegans. Experimental Gerontology 56, 245–255.
| Effects of the mitochondrial respiratory chain on longevity in C. elegans.Crossref | GoogleScholarGoogle Scholar | 24709342PubMed |
De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, Cell & Environment 37, 1–18.
| The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms.Crossref | GoogleScholarGoogle Scholar |
Ferris R, Ellis RH, Wheeler TR, Hadley P (1998) Effect of high temperature stress at anthesis on grain yield and biomass of field-grown crops of wheat. Annals of Botany 82, 631–639.
| Effect of high temperature stress at anthesis on grain yield and biomass of field-grown crops of wheat.Crossref | GoogleScholarGoogle Scholar |
Impe D, Reitz J, Köpnick C, Rolletschek H, Börner A, Senula A, Nagel M (2020) Assessment of pollen viability for wheat. Frontiers in Plant Science 10, 1588
| Assessment of pollen viability for wheat.Crossref | GoogleScholarGoogle Scholar | 32038666PubMed |
IPCC (2018) ‘Global warming of 1.5°C. An IPCC special report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty.’ (IPCC-World Meteorological Organization: Geneva)
Katar M, Ozugurlu AF, Ozyurt H, Benli I (2014) Evaluation of glutathione peroxidase and superoxide dismutase enzyme polymorphisms in celiac disease patients. Genetics and Molecular Research 13, 1030–1037.
| Evaluation of glutathione peroxidase and superoxide dismutase enzyme polymorphisms in celiac disease patients.Crossref | GoogleScholarGoogle Scholar | 24634124PubMed |
Kaushal N, Bhandari K, Siddique KHM, Nayyar H (2016) Food crops face rising temperatures: an overview of responses, adaptive mechanisms, and approaches to improve heat tolerance. Cogent Food & Agriculture 2, 1
| Food crops face rising temperatures: an overview of responses, adaptive mechanisms, and approaches to improve heat tolerance.Crossref | GoogleScholarGoogle Scholar |
Kearns CA, Inouye DW (1993) ‘Techniques for pollination biologists.’ (University Press of Colorado)
Liu Z, Shi X, Li S, Zhang L, Song X (2018) Oxidative stress and aberrant programmed cell death are associated with pollen abortion in isonuclear alloplasmic male-sterile wheat. Frontiers in Plant Science 9, 595
| Oxidative stress and aberrant programmed cell death are associated with pollen abortion in isonuclear alloplasmic male-sterile wheat.Crossref | GoogleScholarGoogle Scholar | 29780399PubMed |
Mamrutha HM, Rinki K, Venkatesh K, Gopalareddy K, Khan H, Mishra CN, Kumar S, Kumar Y, Singh G, Singh GP (2020) Impact of high night temperature stress on different growth stages of wheat. Plant Physiology Reports 25, 707–715.
| Impact of high night temperature stress on different growth stages of wheat.Crossref | GoogleScholarGoogle Scholar |
Mascarenhas JP, Crone DE (1996) Pollen and the heat shock response. Sexual Plant Reproduction 9, 370–374.
| Pollen and the heat shock response.Crossref | GoogleScholarGoogle Scholar |
Møller IM (2001) PLANT MITOCHONDRIA AND OXIDATIVE STRESS: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology 52, 561–591.
| PLANT MITOCHONDRIA AND OXIDATIVE STRESS: electron transport, NADPH turnover, and metabolism of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 11337409PubMed |
Müller F, Rieu I (2016) Acclimation to high temperature during pollen development. Plant Reproduction 29, 107–118.
| Acclimation to high temperature during pollen development.Crossref | GoogleScholarGoogle Scholar | 27067439PubMed |
Muthukumar K, Rajakumar S, Sarkar MN, Nachiappan V (2011) Glutathione peroxidase3 of Saccharomyces cerevisiae protects phospholipids during cadmium-induced oxidative stress. Antonie van Leeuwenhoek 99, 761–771.
| Glutathione peroxidase3 of Saccharomyces cerevisiae protects phospholipids during cadmium-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar | 21229313PubMed |
Narayanan S, Tamura PJ, Roth MR, Prasad PVV, Welti R (2016) Wheat leaf lipids during heat stress: I. High day and night temperatures result in major lipid alterations: wheat leaf lipid composition during heat stress. Plant, Cell & Environment 39, 787–803.
| Wheat leaf lipids during heat stress: I. High day and night temperatures result in major lipid alterations: wheat leaf lipid composition during heat stress.Crossref | GoogleScholarGoogle Scholar |
Nasehzadeh M, Ellis RH (2017) Wheat seed weight and quality differ temporally in sensitivity to warm or cool conditions during seed development and maturation. Annals of Botany 120, 479–493.
| Wheat seed weight and quality differ temporally in sensitivity to warm or cool conditions during seed development and maturation.Crossref | GoogleScholarGoogle Scholar | 28637252PubMed |
Pandey GC, Mamrutha HM, Tiwari R, Sareen S, Bhatia S, Siwach P, Tiwari V, Sharma I (2015) Physiological traits associated with heat tolerance in bread wheat (Triticum aestivum L.). Physiology and Molecular Biology of Plants 21, 93–99.
| Physiological traits associated with heat tolerance in bread wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 25648644PubMed |
Prasad PVV, Djanaguiraman M (2014) Response of floret fertility and individual grain weight of wheat to high temperature stress: sensitive stages and thresholds for temperature and duration. Functional Plant Biology 41, 1261
| Response of floret fertility and individual grain weight of wheat to high temperature stress: sensitive stages and thresholds for temperature and duration.Crossref | GoogleScholarGoogle Scholar | 32481075PubMed |
Prasad PVV, Boote KJ, Allen LH, Sheehy JE, Thomas JMG (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research 95, 398–411.
| Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress.Crossref | GoogleScholarGoogle Scholar |
Rathod V, Behera TK, Munshi AD, Durgesh K, Jat GS, Boopala Krishnan G, Sharma N (2018) Pollen viability and in vitro pollen germination studies in Momordica species and their intra and interspecific hybrids. International Journal of Chemical Studies 6, 32–40.
Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G (2012) Achieving yield gains in wheat: achieving yield gains in wheat. Plant, Cell & Environment 35, 1799–1823.
| Achieving yield gains in wheat: achieving yield gains in wheat.Crossref | GoogleScholarGoogle Scholar |
Saini HS, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Annals of Botany 49, 835–846.
| Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature.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
| Development anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid.Crossref | GoogleScholarGoogle Scholar |
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.
Scheibye-Knudsen M, Fang EF, Croteau DL, Wilson DM, Bohr VA (2015) Protecting the mitochondrial powerhouse. Trends in Cell Biology 25, 158–170.
| Protecting the mitochondrial powerhouse.Crossref | GoogleScholarGoogle Scholar | 25499735PubMed |
Sharma D, Singh R, Rane J, Gupta VK, Mamrutha HM, Tiwari R (2016) Mapping quantitative trait loci associated with grain filling duration and grain number under terminal heat stress in bread wheat (Triticum aestivum L. Plant Breeding 135, 538–545.
| Mapping quantitative trait loci associated with grain filling duration and grain number under terminal heat stress in bread wheat (Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar |
Sharma D, Chandra Pandey G, Mamrutha HM, Singh R, Singh NK, Singh GP, Rane J, Tiwari R (2019) Genotype–phenotype relationships for high temperature tolerance: an integrated method for minimizing phenotyping constraints in wheat. Crop Science 59, 1973–1982.
| Genotype–phenotype relationships for high temperature tolerance: an integrated method for minimizing phenotyping constraints in wheat.Crossref | GoogleScholarGoogle Scholar |
Sheoran S, Thakur V, Narwal S, Turan R, Mamrutha HM, Singh V, Tiwari V, Sharma I (2015) Differential activity and expression profile of antioxidant enzymes and physiological changes in wheat (Triticum aestivum L.) under drought. Applied Biochemistry and Biotechnology 177, 1282–1298.
| Differential activity and expression profile of antioxidant enzymes and physiological changes in wheat (Triticum aestivum L.) under drought.Crossref | GoogleScholarGoogle Scholar | 26319568PubMed |
Wan C, Li S, Wen L, Kong J, Wang K, Zhu Y (2007) Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice. Plant Cell Reports 26, 373–382.
| Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice.Crossref | GoogleScholarGoogle Scholar | 17053903PubMed |
West AP, Khoury-Hanold W, Staron M, Tal MC, Pineda CM, Lang SM, Bestwick M, Duguay BA, Raimundo N, MacDuff DA, Kaech SM, Smiley JR, Means RE, Iwasaki A, Shadel GS (2015) Mitochondrial DNA stress primes the antiviral innate immune response. Nature 520, 553–557.
| Mitochondrial DNA stress primes the antiviral innate immune response.Crossref | GoogleScholarGoogle Scholar | 25642965PubMed |
Zafra A, Castro AJ, de Dios Alché J (2018) Identification of novel superoxide dismutase isoenzymes in the olive (Olea europaea L.) pollen. BMC Plant Biology 18, 114
| Identification of novel superoxide dismutase isoenzymes in the olive (Olea europaea L.) pollen.Crossref | GoogleScholarGoogle Scholar | 29884131PubMed |
Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959–1968.
| Temperature stress and plant sexual reproduction: uncovering the weakest links.Crossref | GoogleScholarGoogle Scholar | 20351019PubMed |