Skip to main content
Log in

Consequence of cyclic pollen selection for heat tolerance on the performance of different generations in maize (Zea mays L.)

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The reproductive stage in many crops, including maize, is very sensitive to heat stress and the genetic overlap between gametophytic and sporophytic phase gives an opportunity to select superior stress tolerant genotype at gametophytic stage. An attempt was made to evaluate the response of cyclic pollen selection in the F1 and F2 generations on the performance of F3 generation progenies for seed yield and yield contributing traits under natural heat stress conditions. In this direction three groups of F3 progenies, namely (i) pollen selection in F1 and F2 generations (GG), (ii) pollen selection only in F2 generation (CG), (iii) no pollen selection in F1 and F2 generations (CC) were screened for heat stress at Agricultural Research Station (ARS), Bheemarayanagudi. The GG progenies recorded significantly higher chlorophyll content, more number of pollen grains per anther and less pollen sterility compared to CG and CC group of progenies under heat stress. Further, the F4 progenies obtained through cyclic pollen selection (in F1, F2 and F3) were also tested for heat stress tolerance at seedling stage. The significant improvement for heat stress tolerance was recorded in F4 progenies derived through cyclic pollen selection as compared to control (no pollen selection for heat tolerance in any generation) F4 progenies. The results indicated that cyclic pollen selection in F1, F2 and F3 generations improved the heat stress tolerance of the progenies in the succeeding generations. To provide genetic evidence for the effect of pollen selection for heat tolerance, the control F2 (C) and selected F2 (G) populations were compared for the segregation of SSR markers. The selected F2 (G) population showed significant deviation from normal Mendelian ratio of 1:2:1 and showed skewness towards the alleles selected from male parent. The results provide strong evidence for an increase in the frequency of parental alleles in the progenies that impart heat stress tolerance.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  • Babu D. V., Sudhakar P. and Reddy Y. S. K. 2013 Screening of thermotolerant ragi genotypes at seedling stage using TIR technique. Bioscan 8, 1493–1495.

    Google Scholar 

  • Bajaj M., Cresti M. and Shivanna K. R. 1992 Effects of high temperature and humidity stresses on tobacco pollen and their progeny. In Angiosperm pollen and ovules (ed. E. Ottaviano, M. S. Gorla, D. L. Mulcahy and G. B. Mulcahy), pp. 349–354. Springer, New York.

    Chapter  Google Scholar 

  • Barnabás B., Jäger K. and Fehér A. 2008 The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Enviorn. 31, 11–38.

    Google Scholar 

  • Beaudry F. E., Rifkin J. L., Barrett S. C. and Wright S. I. 2020 Evolutionary genomics of plant gametophytic selection. Plant Commun. 1, 1–16.

    Article  Google Scholar 

  • Begcy K. and Dresselhaus T. 2018 Epigenetic responses to abiotic stresses during reproductive development in cereals. Plant Reprod. 31, 343–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bheemanahalli R., Sunoj V. S. J., Saripalli G., Prasad P. V. V., Balyan H. S., Gupta P. K. et al. 2019 Quantifying the impact of heat stress on pollen germination, seed set and grain filling in spring wheat. Crop Sci. 59, 1–13.

    Article  CAS  Google Scholar 

  • Cattivelli L., Rizza F., Badeck F. W., Mazzucotelli E., Mastrangelo A. M., Francia E. et al. 2008 Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res. 105, 1–14.

    Article  Google Scholar 

  • Chi H. S., Straath T. P., Löffler H. J. M. and Van Tuyl J. M. 1999 In vitro selection for heat tolerance in Lilies. In Anther and pollen (ed. C. Clément, E. Pacini and J. C. Audran), pp. 175–182. Springer, Berlin, Heidelberg.

    Chapter  Google Scholar 

  • Chikkodi S. B. and Ravikumar R. L. 2000 Influence of pollen selection for Alternaria helianthi resistance on the progeny performance against leaf blight in sunflower (Helianthus annuus L.). Sex. Plant Reprod. 12, 222–226.

    Google Scholar 

  • Clarke H. J., Khan T. N. and Siddique K. H. M. 2004 Pollen selection for chilling tolerance at hybridisation leads to improved chickpea cultivars. Euphytica 139, 65–74.

    Article  Google Scholar 

  • Dar Z. A., Sheshsayee M. S., Ajaz A., Pratibha M. D., Khan J. A., Biradar J. et al. 2016 Thermal induction response (TIR) in temperate maize Inbred lines. Ecol. Enviorn. Conserv. 22, 387–393.

    Google Scholar 

  • De Storme N. and Geelen D. 2014 The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Enviorn. 37, 1–18.

    Article  CAS  Google Scholar 

  • Devi K. R., Sudhakar P. and Sivasankar A. 2013 Screening of paddy genotypes for high water use efficiency and yield components. Bioinfolet-A Quart. J. Life Sci. 10, 214–224.

    Google Scholar 

  • Djanaguiraman M., Perumal R., Ciampitti I. A., Gupta S. K. and Prasad P. V. V. 2018 Quantifying pearl millet response to high temperature stress: thresholds, sensitive stages, genetic variability and relative sensitivity of pollen and pistil. Plant Cell Enviorn. 41, 993–1007.

    Article  CAS  Google Scholar 

  • Domínguez E., Cuartero J. and Fernández-Muñoz R. 2005 Breeding tomato for pollen tolerance to low temperatures by gametophytic selection. Euphytica 142, 253–263.

    Article  Google Scholar 

  • Doyle J. J. and Doyle J. L. 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11–15.

    Google Scholar 

  • Frascaroli E. and Songstad D. D. 2001 Pollen genotype selection for a simply inherited qualitative factor determining resistance to chlorsulfuron in maize. Theor. Appl. Genet. 102, 342–346.

    Article  CAS  Google Scholar 

  • Frova C., Portaluppi P., Villa M. and Goria M. S. 1995 Sporophytic and gametophytic components of thermotolerance affected by pollen selection. J. Hered. 86, 50–54.

    Article  Google Scholar 

  • Greenway C. A. and Harder L. D. 2007 Variation in ovule and seed size and associated size number trade-offs in angiosperms. Am. J. Bot. 94, 840–846.

    Article  PubMed  Google Scholar 

  • Herrero M. P. and Johnson R. R. 1980 High temperature stress and pollen viability of maize. Crop Sci. 20, 796–800.

    Article  Google Scholar 

  • Honys D. and Twell D. 2004 Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Boil. 5, 1–13.

    Google Scholar 

  • Kakani V. G., Reddy K. R., Koti S., Wallace T. P., Prasad P. V. V., Reddy V. R. et al. 2005 Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Ann. Bot. 96, 59–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovács G. and Barnabás B. 1992 Production of highly cold tolerant maize inbred lines by repeated gametophytic selection. In Angiosperm pollen and ovules (ed. E. Ottaviano, M. S. Gorla, D. L. Mulcahy and G. B. Mulcahy), pp. 359–363. Springer, New York.

    Chapter  Google Scholar 

  • Landi P., Frascaroli E., Tuberosa R. and Conti S. 1989 Comparison between responses to gametophytic and sporophytic recurrent selection in maize (Zea mays L.). Theor. Appl. Genet. 77, 761–767.

    Article  CAS  PubMed  Google Scholar 

  • Lizaso J. I., Ruiz-Ramosa M., Rodrigueza L., Gabaldon-Lealb C., Oliveirac J. A., Loriteb I. J. et al. 2018 Impact of high temperatures in maize: phenology and yield components. Field Crops Res. 216, 129–140.

    Article  Google Scholar 

  • Mohapatra U., Singh A. and Ravikumar R. L. 2020 Effect of gamete selection in improving of heat tolerance as demonstrated by shift in allele frequency in maize (Zea mays L.). Euphytica 216, 76.

    Article  CAS  Google Scholar 

  • Nieto-Sotelo J., Martínez L. M., Ponce G., Cassab G. I., Alagón A. and Meeley R. B. 2002 Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell 14, 1621–1633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ottaviano E., Sidoti P. and Villa M. 1986 Pollen competitive ability in maize selection and single gene analysis. In Biotechnology and ecology of pollen (ed. D. L. Mulcahy, G. B. Mulcahy and E. Ottaviano), pp. 21–26. Springer, New York.

    Chapter  Google Scholar 

  • Ottaviano E., Gorla M. S. and Pe E. 1982 Male gametophytic selection in maize. Theor. Appl. Genet. 63, 249–254.

    Article  CAS  PubMed  Google Scholar 

  • Ottaviano E., Sari-Gorla M. and Villa M. 1988 Pollen competitive ability in maize: within population variability and response to selection. Theor. Appl. Genet. 76, 601–608.

    Article  CAS  PubMed  Google Scholar 

  • Patil B. S., Ravikumar R. L. and Salimath P. M. 2006 Effect of pollen selection for moisture stress tolerance on progeny performance in Sorghum. J. Food Agric. Environ. 4, 201–204.

    Google Scholar 

  • Paupière M. J., van Haperen P., Rieu I., Visser R. G., Tikunov Y. M. and Bovy A. G. 2017 Screening for pollen tolerance to high temperatures in tomato. Euphytica 213, 1–8.

    Article  CAS  Google Scholar 

  • Payero J. O., Melvin S. R., Irmak S. and Tarkalson D. 2006 Yield response of corn to deficit irrigation in a semiarid climate. Agric. Water. Manag. 84, 101–112.

    Article  Google Scholar 

  • Peters M. A. and Weis A. E. 2018 Selection for pollen competitive ability in mixed-mating systems. Evolution 72, 2513–2536.

    Article  PubMed  Google Scholar 

  • Petolino J. F., Cowen N. M., Thompson S. A. and Mitchell J. C. 1990 Gamete selection for heat-stress tolerance in maize. J. Plant Physiol. 136, 219–224.

    Article  Google Scholar 

  • Prasad P. V., Bheemanahalli R. and Jagadish S. K. 2017 Field crops and the fear of heat stress—opportunities, challenges and future directions. Field Crops Res. 200, 114–121.

    Article  Google Scholar 

  • Quesada M., Winsor J. A. and Stephenson A. G. 1996 Effects of pollen competition on the reproductive performance in cucurbit hybrids (Cucurbitaceae): F1 and back cross generations. Can. J. Bot. 74, 1113–1118.

    Article  Google Scholar 

  • Rajesh P., Ramesh T., Farzana J., Keshavulu K. and Prakash B. 2011 Identification of thermotolerant single cross hybrids based on temperature induction response (TIR) technique in maize (Zea mays L.). J. Res. ANGRAU. 39, 66–69.

    Google Scholar 

  • Ravikumar R. L., Patil B. S., Soregaon C. D. and Hegde S. G. 2007 Genetic evidence for gametophytic selection of wilt resistant alleles in chickpea. Theor. Appl. Genet. 114, 619–625.

    Article  CAS  PubMed  Google Scholar 

  • Ravikumar R. L., Chaitra G. N., Choukimath A. M. and Soregaon C. D. 2013 Gametophytic selection for wilt resistance and its impact on the segregation of wilt resistance alleles in chickpea (Cicer arietinum L.). Euphytica 189, 173–181.

    Article  CAS  Google Scholar 

  • Rieu I., Twell D. and Firon N. 2017 Pollen development at high temperature: from acclimation to collapse. Plant Physiol. 173, 1967–1976.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shobha R. T. and Ravikumar R. L. 2006 Sporophytic and gametophytic recurrent selection for improvement of partial resistance to Alternaria leaf blight in sunflower (Helianthus annuus L.). Euphytica 147, 421–431.

    Article  Google Scholar 

  • Singh A., Kuchanur P. H. and Ravikumar R. L. 2017 Identification of heat tolerant inbred lines using TIR technique and its association with field tolerance. Bioscan 12, 2053–2058.

    CAS  Google Scholar 

  • Singh A., Ravikumar R. L. and Jingade P. 2016 Genetic variability for gametophytic heat tolerance in maize inbred lines. SABRAO J. Breed. Genet. 48, 41–49.

    Google Scholar 

  • Singh A., Antre S. H., Ravikumar R. L., Kuchanur P. H. and Lohithaswa H. C. 2020a Genetic evidence of pollen selection mediated phenotypic changes in maize conferring transgenerational heat stress tolerance. Crop Sci. 60, 1907–1924.

    Article  CAS  Google Scholar 

  • Singh A., Ravikumar R. L. and Antre S. H. 2020b Comparison of methods of pollen selection for heat tolerance and their effect in segregating population of maize (Zea mays L.). Agri. Res. 10, 15–20.

    Article  CAS  Google Scholar 

  • Song G., Wang M., Zeng B., Zhang J., Jiang C., Hu Q. et al. 2015 Anther response to high-temperature stress during development and pollen thermotolerance heterosis as revealed by pollen tube growth and in vitro pollen vigor analysis in upland cotton. Planta. 241, 1271–1285.

    Article  CAS  PubMed  Google Scholar 

  • Sunoj V. S. J., Somayanda I. M., Chiluwal A., Perumal R., Prasad P. V. V. and Jagadish S. V. K. 2017 Resilience of pollen and post-flowering response in diverse sorghum genotypes exposed to heat stress under field conditions. Crop Sci. 57, 1658–1669.

    Article  CAS  Google Scholar 

  • Tang X., Zhang Z. Y., Zhang W. J., Zhao X. M., Li X., Zhang D. et al. 2010 Global gene profiling of laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis. Plant Physiol. 154, 1855–1870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur P., Kumar S., Malik J. A., Berger J. D. and Nayyar H. 2010 Cold stress effects on reproductive development in grain crops: an overview. Environ. Exp. Bot. 67, 429–443.

    Article  CAS  Google Scholar 

  • Touraev A., Fink C. S., Stöger E. and Heberle-Bors E. 1995 Pollen selection: a transgenic reconstruction approach. Proc. Natl. Acad. Sci. USA 92, 12165–12169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y., Tao H., Tian B., Sheng D., Xu C., Zhou H. et al. 2019 Flowering dynamics, pollen, and pistil contribution to grain yield in response to high temperature during maize flowering. Environ. Exp. Bot. 158, 80–88.

    Article  Google Scholar 

  • Warman C., Panda K., Vejlupkova Z., Hokin S., Unger-Wallace E. et al. 2020 High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements. PLoS Genet. 16, 1–32.

    Article  CAS  Google Scholar 

  • Westgate M. E., Lizaso J. and Batchelor W. 2003 Quantitative relationships between pollen shed density and grain yield in maize. Crop Sci. 43, 934–942.

    Article  Google Scholar 

  • Winsor J. A., Davis L. E. and Stefenson A. G. 1987 The relationship between pollen load and fruit maturation and the effect of pollen load on offspring vigor in Cucurbita pepo. Am. Nat. 129, 643–656.

    Article  Google Scholar 

  • Zamir D., Tanksley S. D. and Jones R. A. 1981 Low temperature effect on selective fertilization by pollen mixtures of wild and cultivated tomato species. Theor. Appl. Genet. 59, 235–238.

    Article  CAS  PubMed  Google Scholar 

  • Zhao C., Liu B., Piao S., Wang X., Lobell D. B. and Huang Y. 2017 Temperature increase reduces global yields of major crops in four independent estimates. PNAS 114, 9326–9331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors acknowledge the DBT-FIST funded Department of Plant Biotechnology, UAS, GKVK Campus, Bengaluru, and Agriculture Research Station Bheemarayanagudi, UAS, Raichur for extending necessary facilities to carry out the research work.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ashutosh Singh or R. L. Ravikumar.

Additional information

Corresponding editor: Durgadas P. Kasbekar

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, A., Ravikumar, R.L., Antre, S.H. et al. Consequence of cyclic pollen selection for heat tolerance on the performance of different generations in maize (Zea mays L.). J Genet 101, 33 (2022). https://doi.org/10.1007/s12041-022-01373-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12041-022-01373-y

Keywords

Navigation