Abstract
A novel male-sterile maize mutant male sterility 39 (ms39) was obtained from offspring of the commercial hybrid Chuandan No. 9 that had been carried into outer space. A previous study demonstrated that ms39 is controlled by a single recessive nuclear gene, located on the long arm of chromosome 3. Here, we used 1073 mutant individuals derived from the (ms39 × Mo17) F2 population and sequentially developed new primers to identify markers supporting the fine mapping of ms39. A 365-kb region on chromosome 3 flanked by markers L8 and M30 at a genetic distance of 0.18 and 0.47 cM, respectively, was identified. According to the reference sequence of ZmB73_Ref-Gen_v4, 12 candidate genes were identified within the 365-kb mapping region. Based on cloning and sequence BLAST analysis of the 12 candidate genes, a four-base-pair deletion was found within the exon of Zm00001d043909, which encoded callose synthase12. This four-base-pair deletion resulted in a frameshift mutation in ms39, leading to the earlier termination of the coding protein, and ultimately caused abnormal performance of the callose synthase. Additionally, cytological observation was conducted on a sister cross population (ms39/ms39 × ms39/Ms39). These observations showed that the tapetum cells of the ms39 mutant appeared abnormal from the dyad stage, and aborted microspores were observed during pollen development. These results lay the foundation for the cloning of ms39 and exploration of the molecular mechanism underlying aborted pollen development in ms39 maize.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albertsen MC, Fox T, Trimnell M, Wu Y, Lowe K, Li B, Faller M (2011) Msca1 nucleotide sequences impacting plant male fertility and method of using same. Google Patents
Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460
Barratt DHP, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose synthase GSL7 is necessary for Normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol 155(1):328–341. https://doi.org/10.1104/pp.110.166330
Cao MJ, Rong TZ, Pan GT (2003) Genetic analysis about maize male sterile mutant obtained by space flight. J Genet Genomics (Chinese) 30(9):817–822
Cao MJ, Huang WC, Pan GT, Rong TZ, Zhu YG (2004) Analysis of plant height between male sterile plants obtained by space flight and male fertile plants in maize. J Nucl Agric Sci (Chinese) 18(4):261–264
Chaubal R, Anderson JR, Trimnell MR, Fox TW, Albertsen MC, Bedinger P (2003) The transformation of anthers in the msca1 mutant of maize. Planta 216(5):778–788. https://doi.org/10.1007/s00425-002-0929-8
Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606. https://doi.org/10.1146/annurev-arplant-050213-040119
Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100(5):959–966. https://doi.org/10.1093/aob/mcm121
Cigan AM, Unger E, Xu RJ, Kendall T, Fox TW (2001) Phenotypic complementation of ms45 maize requires tapetal expression of MS45. Sex Plant Reprod 14(3):135–142. https://doi.org/10.1007/s004970100099
Djukanovic V, Smith J, Lowe K, Yang M, Gao H, Jones S, Nicholson MG, West A, Lape J, Bidney D, Carl Falco S, Jantz D, Alexander Lyznik L (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J 76(5):888–899. https://doi.org/10.1111/tpj.12335
Dong XY, Hong ZL, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42(3):315–328. https://doi.org/10.1111/j.1365-313X.2005.02379.x
Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58(3):333–349. https://doi.org/10.1007/s11103-005-4526-7
Fox T, DeBruin J, Haug Collet K, Trimnell M, Clapp J, Leonard A, Li B, Scolaro E, Collinson S, Glassman K, Miller M, Schussler J, Dolan D, Liu L, Gho C, Albertsen M, Loussaert D, Shen B (2017) A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnol J 15:942–952. https://doi.org/10.1111/pbi.12689
Gomez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57(11):876–891. https://doi.org/10.1111/jipb.12425
Huang L, Chen XY, Rim Y, Han X, Cho WK, Kim SW, Kim JY (2009) Arabidopsis glucan synthase-like 10 functions in male gametogenesis. J Plant Physiol 166(4):344–352. https://doi.org/10.1016/j.jplph.2008.06.010
Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15(11):2503–2513. https://doi.org/10.1105/tpc.016097
Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, Campbell MS, Stein JC, Wei X, Chin CS, Guill K, Regulski M, Kumari S, Olson A, Gent J, Schneider KL, Wolfgruber TK, May MR, Springer NM, Antoniou E, McCombie WR, Presting GG, McMullen M, Ross-Ibarra J, Dawe RK, Hastie A, Rank DR, Ware D (2017) Improved maize reference genome with single-molecule technologies. Nature 546(7659):524–527. https://doi.org/10.1038/nature22971
Li Q, Wan J-M (2005) SSRHunter: development of a local searching software for SSR sites. Yi Chuan 27(5):808–810
Li SZ, Cao MJ, Rong TZ, Pan GT, Zhu YG (2007) Cytological observation on pollen abortion of genetic male sterile mutant induced by space flight in maize. J Mol Cell Biol (Chinese) 40(5):359–364
Liu FX, Cao MJ, Rong TZ, Pan GT (2005) Locating maize male sterility gene induced by space flight using microsatellite markers. J Genet Genomics (Chinese) 32(7):753–757
Liu J, Qu J, Yang C, Tang D, Li J, Lan H, Rong T (2015) Development of genome-wide insertion and deletion markers for maize, based on next-generation sequencing data. BMC Genomics 16:601. https://doi.org/10.1186/s12864-015-1797-5
Longin CF, Muhleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125(6):1087–1096. https://doi.org/10.1007/s00122-012-1967-7
Lu P, Chai M, Yang J, Ning G, Wang G, Ma H (2014) The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol 164(4):1893–1904. https://doi.org/10.1104/pp.113.233387
Moon J, Skibbe D, Timofejeva L, Wang CJR, Kelliher T, Kremling K, Walbot V, Cande WZ (2013) Regulation of cell divisions and differentiation by MALE STERILITY32 is required for anther development in maize. Plant J 76(4):592–602. https://doi.org/10.1111/tpj.12318
Nan G-L, Zhai J, Arikit S, Morrow D, Fernandes J, Mai L, Nguyen N, Meyers BC, Walbot V (2016) MS23, a master basic helix-loop-helix factor, regulates the specification and development of tapetum in maize. Development. https://doi.org/10.1242/dev.140673
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl):S46–S60. https://doi.org/10.1105/tpc.017012
Sekhon RS, Lin HN, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66(4):553–563. https://doi.org/10.1111/j.1365-313X.2011.04527.x
Shi X, Sun XH, Zhang ZG, Feng D, Zhang Q, Han LD, Wu JX, Lu TG (2015) Glucan synthase-like 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant Cell Physiol 56(3):497–509. https://doi.org/10.1093/pcp/pcu193
Skibbe DS, Schnable PS (2005) Male sterility in maize. Maydica 50(3–4):367–376
Somaratne Y, Tian Y, Zhang H, Wang M, Huo Y, Cao F, Zhao L, Chen H (2017) Abnormal pollen vacuolation1 (APV1) is required for male fertility by contributing to anther cuticle and pollen exine formation in maize. Plant J
Unger E, Cigan AM, Trimnell M, Xu RJ, Kendall T, Roth B, Albertsen M (2002) A chimeric ecdysone receptor facilitates methoxyfenozide-dependent restoration of male fertility in ms45 maize. Transgenic Res 11(5):455–465. https://doi.org/10.1023/A:1020350208095
Walbot V, Egger RL (2016) Pre-meiotic anther development: cell fate specification and differentiation. Annu Rev Plant Biol 67:365–395. https://doi.org/10.1146/annurev-arplant-043015-111804
Wang D, Oses-Prieto JA, Li KH, Fernandes JF, Burlingame AL, Walbot V (2010) The male sterile 8 mutation of maize disrupts the temporal progression of the transcriptome and results in the mis-regulation of metabolic functions. Plant J 63(6):939–951. https://doi.org/10.1111/j.1365-313X.2010.04294.x
Wang CJR, Nan GL, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN, Harper L, Egger R, Walbot V, Cande WZ (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139(14):2594–2603. https://doi.org/10.1242/dev.077891
Wang DX, Skibbe D, Walbot V (2013) Maize male sterile 8 (Ms8), a putative beta-1,3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod 26(4):329–338. https://doi.org/10.1007/s00497-013-0230-y
Willing RP, Bashe D, Mascarenhas JP (1988) An analysis of the quantity and diversity of messenger-RNAs from pollen and shoots of Zea mays. Theor Appl Genet 75(5):751–753
Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60(5):1479–1492. https://doi.org/10.1093/jxb/erp095
Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male-sterility in transgenic tobacco. Plant Cell 4(7):759–771. https://doi.org/10.1105/Tpc.4.7.759
Wu YZ, Fox TW, Trimnell MR, Wang LJ, Xu RJ, Cigan AM, Huffman GA, Garnaat CW, Hershey H, Albertsen MC (2016) Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J 14(3):1046–1054. https://doi.org/10.1111/pbi.12477
Wych RD (1988) Production of hybrid seed corn. Corn and corn improvement (cornandcornimpr), pp 565–607
Zhang D, Wu S, An X, Xie K, Zhou Y, Xu L, Fang W, Liu S, Liu S, Zhu T (2017) Construction of a multi-control sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnol J
Zhao X, de Palma J, Oane R, Gamuyao R, Luo M, Chaudhury A, Herve P, Xue Q, Bennett J (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54(3):375–387. https://doi.org/10.1111/j.1365-313X.2008.03426.x
Funding
This work was supported by the National Natural Science Foundation of China (31771876), the National Key Research and Development Program of China (2016YFD0102104), and the Platform for Mutation Breeding by Radiation in Sichuan (2016NZ0106).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Electronic supplementary material
Fig. S1
Flow chart of the development of three populations. The (ms39 × Mo17) F2 population was developed for fine mapping, (ms39 × Mo17) BC1F2 and the (ms39 × B73) F2 populations was developed for verifying the fine mapping results. A sister cross population was developed for cytological observations. F1 and backcross F1 were planted in winter in Xishuangbanna, Yunnan Province; F2 and backcross F2 were grown in the summer in Chengdu, Sichuan Province; sister cross population was planted in the summer in Sichuan and in the winter in Yunnan over the course one year. (PDF 172 kb)
Fig. S2
Comparison of agronomic traits between the ms39 mutant and wild-type. (a) Plant height. (b) Ear height. (c) Tassel length. (d) Branch number. * Represents significance at 0.05 level. (PDF 94 kb)
Fig. S3
Schematic representation of ZmCals12 and ZmNAC82 gene structure. (a) The exon (solid black box) and untranslated region (UTR; empty box) of ZmCals12; four nucleotides in the first exon was deleted in ms39. (b) The exon (solid black box), intron (black lines) and untranslated region (UTR; empty box) of ZmNAC82; three nucleotides in the first exon and six nucleotides in the third exon were deleted in ms39. (PDF 317 kb)
Fig. S4
Application of the InDel-cals marker for analysis of the 321 mutants from (ms39 × Mo17) BC4F2 population. Mo17, inbred line; S, ms39 mutant; A, male-sterile genotype; B, male-fertile genotype. (PDF 188 kb)
Fig. S5
Expression pattern of candidate genes in different developmental stages of tissues. Colors indicate the individual genes. (PDF 253 kb)
Fig. S6
Phylogenetic analysis of Zmcals12 and its homologous proteins. The evolutionary analyses were conducted in MEGA7. Group A includes eight proteins from monocots, and group B contains four proteins from dicots. (PDF 195 kb)
Fig. S7
Predicted protein structure of callose synthase. (a), (b), (c), (d) are the Zmcals12 from ms39, ZmCals12 from the fertile group, and Cals11 and Cals12 from Arabidopsis, respectively. (PDF 494 kb)
Table S1
All populations used in this study. (DOCX 14 kb)
Table S2
Information of all primers used for mapping in this experiment. (XLSX 28 kb)
Table S3
Information of polymorphic markers used for fine mapping between the ms39 mutant and male-fertile plants. (DOCX 14 kb)
Table S4
Fertility segregation patterns of the F2 and sister cross populations. (DOCX 14 kb)
Table S5
The (ms39 × B73) F2 population was detected by L7, L8, M30, L30, L33 markers. A, male sterile genotype; B, male fertile genotype; H, Heterozygous genotype. χ2 value of the genotype of the (ms39 × B73) F2 population is for χ2 1:2:1, the value is smaller than 5.99; χ2 value of the (ms39 × B73) F2 population is for χ2 3:1, the value is smaller than 3.84. (DOCX 17 kb)
Table S6
Recombination in the (ms39 × Mo17) BC1F2 population by using L7, L8, M30, L30, L33 markers. A, male-sterile genotype; B, male-fertile genotype; H, Heterozygous genotype (DOCX 14 kb)
Rights and permissions
About this article
Cite this article
Zhu, Y., Shi, Z., Li, S. et al. Fine mapping of the novel male-sterile mutant gene ms39 in maize originated from outer space flight. Mol Breeding 38, 125 (2018). https://doi.org/10.1007/s11032-018-0878-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-018-0878-y