Abstract
Key message
Mainly additive gene action governed inheritance of haploid male fertility, although epistatic effects were also significant. Recurrent selection for haploid male fertility resulted in substantial improvement in this trait.
Abstract
The doubled haploid (DH) technology offers several advantages in maize breeding compared to the traditional method of recurrent selfing. However, there is still great potential for improving the success rate of DH production. Currently, the majority of haploid plants are infertile after chromosome doubling treatment by antimitotic agents such as colchicine and cannot be selfed for production of DH lines. Improvement in haploid male fertility (HMF) by selection for a higher spontaneous chromosome doubling rate (SDR) has the potential to increase DH production efficiency. To investigate the gene action governing SDR in two breeding populations, we adapted the quantitative-genetic model of Eberhart and Gardner (in Biometrics 22:864–881. https://doi.org/10.2307/2528079, 1966) for the case of haploid progeny from ten DH lines and corresponding diallel crosses. Furthermore, we carried out three cycles of recurrent selection for SDR in two additional populations to evaluate the selection gain for this trait. Additive genetic effects predominated in both diallel crosses, but epistatic effects were also significant. Entry-mean heritability of SDR observed for haploid progeny of these populations exceeded 0.91, but the single-plant heritability relevant to selection was low, ranging from 0.11 to 0.19. Recurrent selection increased SDR from approximately 5–50%, which suggests the presence of few QTL with large effects. This improvement in HMF is greater than the effect of standard colchicine treatment, which yields at maximum 30% fertile haploids. Altogether, the results show the great potential of spontaneous chromosome doubling to streamline development DH lines and to enable new breeding schemes with more efficient allocation of resources.
Similar content being viewed by others
Abbreviations
- DH:
-
Doubled haploid
- SDR:
-
Spontaneous doubling rate
- HMF:
-
Haploid male fertility
- PS:
-
Pollen score
References
Abendroth LJ, Elmore RW, Boyer MJ, Marlay SK (2011) Corn growth and development. Iowa State University Extension, Ames, Iowa
Beyene Y, Mugo S, Oikeh SO et al (2017) Hybrids performance of doubled haploid lines derived from 10 tropical bi-parental maize populations evaluated in contrasting environments in Kenya. Afr J Biotech 16:371–379
Butler D, Cullis B, Gilmour A, Gogel, B (2009) ASReml-R reference manual. The State of Queensland, Department of Primary Industries and Fisheries, Brisbane
Chaikam V, Mahuku G (2012) Chromosome doubling of maternal haploids. In: Prasanna BM, Chaikam V, Mahuku G (eds) Doubled haploid technology in maize breeding. International Maize and Wheat Improvement Center, México, D.F., pp 24–29
Chaikam V, Martinez L, Melchinger AE et al (2016) Development and validation of red root marker-based haploid inducers in maize. Crop Sci 56:1678–1688
Chaikam V, Nair SK, Martinez L, et al (2018) Marker-assisted breeding of improved maternal haploid inducers in maize for the tropical/subtropical regions. Front Plant Sci https://doi.org/10.3389/fpls.2018.01527
Chalyk ST (1994) Properties of maternal haploid maize plants and potential application to maize breeding. Euphytica 79:13–18
Chase SS (1964) Monoploids and diploids of maize: a comparison of genotypic equivalents. Am J Bot 51:928–933
Duvick DN (1996) What is yield? In: Developing drought- and low N-tolerant maize. Proceedings of a symposium, March 25-29, 1996. CIMMYT, El Batan, Mexico, D.F., pp 332–335
Eberhart SA, Gardner CO (1966) A general model for genetic effects. Biometrics 22:864–881. https://doi.org/10.2307/2528079
Eder J, Chalyk S (2002) In vivo haploid induction in maize. Theor Appl Genet 104:703–708
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Addison Wesley Longman, Harlow
Ganal MW, Durstewitz G, Polley A, et al (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS ONE e28334–e28334. https://doi.org/10.1371/journal.pone.0028334
Hansen TF (2013) Why epistasis is important for selection and adaptation. Evolution 67:3501–3511. https://doi.org/10.1111/evo.12214
Isik F, Holland JB, Maltecca C (2017) Genetic data analysis for plant and animal breeding. Springer International Publishing
Johnson J (2017) Breaking Ground: Vijay Chaikam develops doubled haploid lines to accelerate maize breeding. CIMMYT. https://www.cimmyt.org/breaking-ground-vijay-chaikam-develops-doubled-haploid-lines-to-accelerate-maize-breeding/. Accessed 13 April 2018
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997
Kleiber D, Prigge V, Melchinger AE et al (2012) Haploid fertility in temperate and tropical maize germplasm. Crop Sci 52:623–630
Liu C, Li X, Meng D et al (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase a generates haploid induction in maize. Mol Plant 10:520–522
Longin CFH, Utz HF, Reif JC et al (2007) Hybrid maize breeding with doubled haploids: III. Efficiency of early testing prior to doubled haploid production in two-stage selection for testcross performance. Theor Appl Genet 115:519–527
Ma H, Li G, Würschum T, et al (2018) Genome-wide association study of haploid male fertility in maize (Zea Mays L.). Front Plant Sci 9:974. https://doi.org/10.3389/fpls.2018.00974
Marulanda JJ, Mi X, Melchinger AE et al (2016) Optimum breeding strategies using genomic selection for hybrid breeding in wheat, maize, rye, barley, rice and triticale. Theor Appl Genet 129:1901–1913
Melchinger AE, Schipprack W, Würschum T, et al (2013) Rapid and accurate identification of in vivo-induced haploid seeds based on oil content in maize. Sci Rep 3. https://doi.org/10.1038/srep02129
Melchinger AE, Brauner PC, Böhm J, Schipprack W (2016a) In vivo haploid induction in maize: Comparison of different testing regimes for measuring haploid induction rates. Crop Sci 56:1127–1135
Melchinger AE, Molenaar WS, Mirdita V, Schipprack W (2016b) Colchicine alternatives for chromosome doubling in maize haploids for doubled- haploid production. Crop Sci 56:559–569
Melchinger AE, Böhm J, Utz HF et al (2017a) High-throughput precision phenotyping of the oil content of single seeds of various oilseed crops. Crop Sci 58:670
Melchinger AE, Schopp P, Müller D et al (2017b) Safeguarding our genetic resources with libraries of doubled-haploid lines. Genetics 206:1611. https://doi.org/10.1534/genetics.115.186205
Möhring J, Piepho H-P (2009) Comparison of weighting in two-stage analysis of plant breeding trials. Crop Sci 49:1977–1988
Molenaar WS, Melchinger AE (2019) Production of doubled haploid lines for hybrid breeding in maize. In: Ordon F, Friedt W (eds) Advances in breeding techniques for cereal crops. Burleigh Dodds Science Publishing, Cambridge. (in print)
Molenaar WS, Schipprack W, Melchinger AE (2018) Nitrous oxide induced chromosome doubling of maize haploids. Crop Sci 58:650–659
NPGS (2018) U.S. National Plant Germplasm System. https://npgsweb.ars-grin.gov/gringlobal/taxonomybrowse.aspx. Accessed 7 Nov 2018
Piepho H-P (2012) A SAS macro for generating letter displays of pairwise mean comparisons. Communications in Biometry and Crop Science 7:4–13
Portwood JL, Woodhouse MR, Cannon EK, Gardiner JM, Harper LC et al (2019) MaizeGDB 2018: the maize multi-genome genetics and genomics database. Nucleic Acids Res 47(D1):D1146–D1154. https://doi.org/10.1093/nar/gky1046
Prigge V, Melchinger AE (2012) Production of haploids and doubled haploids in maize. Methods Mol Biol Clifton NJ 877:161–172. https://doi.org/10.1007/978-1-61779-818-4_13
Prigge V, Schipprack W, Mahuku G et al (2012) Development of in vivo haploid inducers for tropical maize breeding programs. Euphytica 185:481–490
R Core Team (2018) R: A language and environment for statistical computing. Version 3.5.1. R Foundation for Statistical Computing, Vienna
Ren J, Wu P, Tian X et al (2017) QTL mapping for haploid male fertility by a segregation distortion method and fine mapping of a key QTL qhmf4 in maize. Theor Appl Genet 130:1349–1359
SAS Institute (2013) The SAS system for windows. 9.4 SAS institute, Cary
Uribelarrea M, Cárcova J, Otegui ME, Westgate ME (2002) Pollen production, pollination dynamics, and kernel set in maize. Crop Sci 42:1910–1918
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423
Wang H, Liu J, Xu X et al (2016) Fully-automated high-throughput NMR system for screening of haploid kernels of maize (corn) by measurement of oil content. PLoS ONE 11:e0159444. https://doi.org/10.1371/journal.pone.0159444
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Wu P, Ren J, Tian X et al (2017) New insights into the genetics of haploid male fertility in maize. Crop Sci 57:637–647
Yang J, Qu Y, Chen Q, Tang J, Lübberstedt T et al (2019) Genetic dissection of haploid male fertility in maize (Zea mays L.). Plant Breeding. https://doi.org/10.1111/pbr.12688
Acknowledgements
We are grateful to the technical staff of the maize breeding program at the University of Hohenheim, J. Jesse, F. Mauch, H. Pöschel, and R. Volkhausen for their dedicated work in the greenhouse and field trials. We are also thankful for advice on the statistical analysis from Prof. H. F. Utz and Prof. H.-P. Piepho.
Author contribution statement
AEM, WS and WSM designed the experiments. WS, WSM and AEM coordinated the field trials and phenotyping. WSM carried out the phenotyping with assistance from technical staff. WSM and PCB analyzed the data. WSM and AEM wrote the manuscript. AEM and WS edited the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest
Data availability statement
Data will be made available upon request by the authors.
Ethical standards
The authors declare that the experiments comply with the laws of Germany
Additional information
Communicated by Laurence Moreau.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Molenaar, W.S., Schipprack, W., Brauner, P.C. et al. Haploid male fertility and spontaneous chromosome doubling evaluated in a diallel and recurrent selection experiment in maize. Theor Appl Genet 132, 2273–2284 (2019). https://doi.org/10.1007/s00122-019-03353-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03353-w