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Journal of Integrative Agriculture  2022, Vol. 21 Issue (11): 3158-3168    DOI: 10.1016/j.jia.2022.07.055
Special Issue: 玉米遗传育种合辑Maize Genetics · Breeding · Germplasm Resources
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Cytological study on haploid male fertility in maize
YANG Ji-wei1, 2*, LIU Zong-hua1*, QU Yan-zhi1, ZHANG Ya-zhou1, LI Hao-chuan1
1 College of Agronomy, Henan Agricultural University/State Key Laboratory of Wheat and Maize Crop Science/Henan Grain Crop Collaborative Innovation Center, Zhengzhou 450046, P.R.China
2 Institute of Cereal Crops, Henan Academy of Agricultural Sciences, Zhengzhou 450002, P.R.China
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摘要  

玉米单倍体育种技术主要取决于单倍体基因组加倍,并已广泛应用于商业育种之中。单倍体基因组自然加倍(SHGD)是一种简单、快捷的方法,并在育种者中越来越受欢迎。但目前SHGD的细胞学机制仍不清楚。为此,我们利用诱导系YHI-1与两个极端SHGD能力的重组自交系RL36RL7进行杂交,得到单倍体籽粒。对单倍体植物中花药减数分裂过程中花粉母细胞(PMC)与对应的二倍体花粉母细胞进行了比较。结果表明:早期加倍、第一次减数分裂中期染色体偏分离及第二次减数分裂异常三个主要的途径与SHGD有关。此外,对单倍体和二倍体植株的叶片及PMC利用流式细胞仪进行倍性分析,结果表明:单倍体植株体细胞染色体加倍和生殖细胞染色体加倍是相对独立的过程。这些结果为进一步研究SHGD的可能机制提供了基础,将有助于单倍体育种技术在玉米育种实践中应用。



Abstract  Doubled haploid (DH) breeding technology, which relies on haploid genome doubling, is widely used in commercial maize breeding.  Spontaneous haploid genome doubling (SHGD), a more simplified and straightforward method, is gaining popularity among maize breeders.  However, the cytological mechanism of SHGD remains unclear.  This study crossed inbred lines RL36 and RL7, which have differing SHGD abilities, with inducer line YHI-1 to obtain haploid kernels.  The meiotic processes of pollen mother cells (PMCs) in the haploid plants were compared with diploid controls.  The results suggested that three main pathways, the early doubling of haploid PMCs, the first meiotic metaphase chromosomal segregation distortion, and anomaly of the second meiosis, are responsible for SHGD.  Furthermore, flow cytometry analysis of ploidy levels in leaves and PMCs from haploids and diploid controls revealed that somatic cell chromosome doubling and germ cell chromosome doubling are independent processes.  These findings provide a foundation for further studies on the underlying mechanism of SHGD, aiding the application of DH technology in maize breeding practices.  
Keywords:  maize       haploid         male fertility        spontaneous genome doubling        meiosis  
Received: 31 March 2021   Accepted: 07 June 2021
Fund: This work was supported by the Agricultural Seed Joint Research Project of Henan Province, China (2022010202), the Science and Technology Project of Henan Province, China (222102110276) and the China Postdoctoral Science Foundation (2020M682031).
About author:  YANG Ji-wei, E-mail: yangjiwei2009@126.com; LIU Zong-hua, E-mail: zhliu100@163.com; Correspondence LI Hao-chuan, Tel: +86-371-56990188, E-mail: lihaochuan1220@163.com * These authors contributed equally to this study.

Cite this article: 

YANG Ji-wei, LIU Zong-hua, QU Yan-zhi, ZHANG Ya-zhou, LI Hao-chuan. 2022. Cytological study on haploid male fertility in maize. Journal of Integrative Agriculture, 21(11): 3158-3168.

Beaumont V H, Widholm J M. 1993. Ploidy variation of pronamide-treated maize calli during long term culture. Plant Cell Reports, 12, 648–651.
Bielig L M, Mariani A, Berding N. 2003. Cytological studies of 2n male gamete formation in sugarcane, Saccharum L. Euphytica, 133, 117–124.
Chaikam V, Mahuku G. 2012. Chromosome doubling of maternal haploids. In: Prasanna B M, Chaikam V, Mahuku G, eds., Doubled Haploid Technology in Maize Breeding: Theory and Practice. International Maize and Wheat Improvement Center, Mexico, DF. pp. 24–29.
Chalyk S T. 1994. Properties of maternal haploid maize plants and potential application to maize breeding. Euphytica, 79, 13–18. 
Dwivedi S L, Britt A B, Tripathi L, Sharma S, Upadhyaya H D, Ortiz R. 2015. Haploids: Constraints and opportunities in plant breeding. Biotechnology Advances, 33, 812–829. 
Gallo P H, Micheletti P L, Boldrini K R, Risso-Pascotto C, Pagliarini M S, Valle C B D. 2007. 2n gamete formation in the genus Brachiaria (Poaceae: Paniceae). Euphytica, 154, 255–260.
Geiger H H, Braun M D, Gordillo G A, Koch S, Jesse J, Krutzfeld B A E. 2006. Variation for female fertility among haploid maize lines. Maize Genetics Newsletter, 80, 28–29.
Geiger H H, Schönleben M. 2011. Incidence of male fertility in haploid elite dent maize germplasm. Maize Genetics Newsletter, 85, 22–32.
Germanà M A. 2011. Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Reports, 30, 839–857.
Hallauer A R, Carena M J, Miranda J B. 2010. Quantitative Genetics in Maize Breeding. Springer Science & Business Media, LLC, New York, NY.
Häntzschel K R, Weber G. 2010. Blockage of mitosis in maize root tips using colchicine-alternatives. Protoplasma, 241, 99–104.
Heyn F W. 1977. Analysis of unreduced gametes in the Brassicaceae by crosses between species and ploidy levels. Zeitschrift fur Pflanzenzuchtung, 78, 13–30.
Kato A, Geiger H H. 2002. Chromosome doubling of haploid maize seedlings using nitrous oxide gas at the flower primordial stage. Plant Breeding, 121, 370–377. 
Kelliher T, Walbot V. 2011. Emergence and patterning of the five cell types of the Zea mays anther locule. Developmental Biology, 350, 32–49. 
Kelliher T, Walbot V. 2014. Maize germinal cell initials accommodate hypoxia and precociously express meiotic genes. The Plant Journal, 77, 639–652. 
Kleiber D, Prigge V, Melchinger A E, Burkard F, San Vicente F, Palomino G, Gordillo G A. 2012. Haploid fertility in temperate and tropical maize germplasm. Biological Science, 52, 623–630. 
Lam S L. 1974. Origin and formation of unreduced gametes in the potato. Heredity, 65, 175–178. 
Ma H L, Li G L, Tobias W, Zhang Y, Zheng D B, Yang X H, Li J S, Liu W X, Yan J B, Chen S J. 2018. Genome-wide association study of haploid male fertility in maize (Zea mays L.). Frontiers in Plant Science, 9, 974.
Mashkina O S. 1979. Ways of formation of unreduced microspores in sweet cherries. Tsitolo Genetika, 13, 343–346.
Melchinger A E, Molenaar W S, Mirdita V, Schipprack W. 2016. Colchicine alternatives for chromosome doubling in maize haploids for doubled haploid production. Crop Science, 56, 1–11.
Molenaar W S, Schipprack W, Melchinger A E. 2018. Nitrous oxide induced chromosome doubling of maize haploids. Crop Science, 58, 650–659. 
Nanda D K, Chase S S. 1966. An embryo marker for detecting monoploids of maize (Zea mays L.). Crop Science, 6, 131–138. 
Nelms B, Walbot V. 2019. Defining the developmental program leading to meiosis in maize. Science, 364, 52–56.
Pagliarini M S, Takayama S Y, Freitas P M D, Carraro L R, Adamowski E V, Silva N. 1999. Failure of cytokinesis and 2n gamete formation in Brazilian accessions of Paspalum. Euphytica, 108, 129–135. 
Palomino G, Hernández L T, Torres E D. 2008. Nuclear genome size and chromosome analysis in Chenopodium quinoa and C. berlandieri subsp. nuttaliae. Euphytica, 164, 221–230. 
Prasanna B M, Chaikam V, Mahuku G. 2012. Doubled Haploid Technology in Maize Breeding: Theory and Practice. International Maize and Wheat Improvement Center, Mexico.
Ramanna M S. 1979. A re-examination of the mechanisms of 2n gamete formation in potato and its implications for breeding. Euphytica, 28, 537–561. 
Ren J J, Boerman N, Liu R X, Wu P H, Trampe B, Vanous K, Frei U K, Chen S J, Lübberstedt T. 2020. Mapping of QTL and identification of candidate genes conferring spontaneous haploid genome doubling in maize (Zea mays L.). Plant Science, 293, 110337. 
Ren J J, Wu P H, Tian X L, Lübberstedt T, Chen S J. 2017. QTL mapping for haploid male fertility by a segregation distortion method and fine mapping of a key QTL qhmf4 in maize. Theoretical and Applied Genetics, 130, 1349–1359. 
Ross K J, Fransz P, Jones G H. 1996. A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Research, 4, 507–516. 
Rouiss H, Cuenca J, Navarro L, Ollitrault P, Aleza P. 2017. Unreduced megagametophyte production in lemon occurs via three meiotic mechanisms, predominantly second-division restitution. Frontiers in Plant Science, 8, 1211. 
Shamina N V, Shatskaia O A. 2011. Two novel meiotic restitution mechanisms in haploid maize (Zea mays L.). Russian Journal of Genetics, 47, 438–445. 
De Storme N, Geelen D. 2013. Sexual polyploidization in plants cytological mechanisms and molecular regulation. New Phytologist, 198, 670–684. 
Sugihara N, Higashigawa T, Aramoto D, Kato A. 2013. Haploid plants carrying a sodium azide-induced mutation (fdr1) produce fertile pollen grains due to first division restitution (FDR) in maize (Zea mays L.). Theoretical and Applied Genetics, 126, 2931–2941. 
Trampe B, Santos I G D, Frei U K, Ren J J, Chen S J, Lübberstedt T. 2020. QTL mapping of spontaneous haploid genome doubling using genotyping-by-sequencing in maize (Zea mays L.). Theoretical and Applied Genetics, 133, 2131–2140.
Wan Y, Duncan D R, Rayburn A L, Petolino J F, Widholm J M. 1991. The use of antimicrotubule herbicides for the production of doubled haploid plants from anther-derived maize callus. Theoretical and Applied Genetics, 81, 205–211. 
Weber D F. 2014. Today’s use of haploids in corn plant breeding. Advances in Agronomy, 123, 123–144. 
Wu P H, Ren J J, Li L, Chen S J. 2014. Early spontaneous diploidization of maternal maize haploids generated by in vivo haploid induction. Euphytica, 200, 127–138. 
Wu P H, Ren J J, Tian X L, Lübberstedt T, Li W, Li G L, Li X L, Chen S J. 2017. New insights into the genetics of haploid male fertility in maize. Crop Science, 57, 637–647. 
Yamashita, K, Nakazaw, Y, Namai K, Amagai M, Tsukazaki H, Wako T, Kojima A. 2012. Modes of inheritance of two apomixis components, diplospory and parthenogenesis, in Chinese chive (Allium ramosum) revealed by analysis of the segregating population generated by back-crossing between amphimictic and apomictic diploids. Breed Science, 62, 160–169. 
Yang J W, Qu Y Z, Chen Q, Tang J H, Lübberstedt T, Li H C, Liu Z H. 2019. Genetic dissection of haploid male fertility in maize (Zea mays L.). Plant Breeding, 138, 259–265. 
Zabirova E R, Shatskaya O A, Shcherbak V S. 1993. Line 613/2 as a source of a high frequency of spontaneous diploidization in corn. Maize Genetics Cooperation Newsletter, 67, 67.

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