Euphytica

, 214:52 | Cite as

Characterization, fine mapping and candidate gene analysis of novel, dominant, nuclear male-sterile gene Ms53 in maize

  • Chaoxian Liu
  • Guoqiang Wang
  • Jie Gao
  • Chunyan Li
  • Ziru Zhang
  • Tingting Yu
  • Jiuguang Wang
  • Lian Zhou
  • Yilin Cai
Article
  • 128 Downloads

Abstract

To better understand the molecular mechanism of stamen formation in maize, we used chemical agent ethyl methanesulfonate (EMS) to treat B73 pollens and obtained a Ms53 mutant with no pollen shedding from maize anthers. Ms53 is a completely male-sterile mutant controlled by a single dominant gene; thus, it cannot propagate itself. Microscopic analysis suggested that mutant anthers are smaller in size and lack trichomes on the epidermis surface. Histological analyses revealed that mutant anther abortion occurs at the microspore development stage. Using 1864 individuals from a backcross population derived from Ms53× Mo17, we delimited Ms53 to an interval of approximately 350 kb containing seven annotated genes and flanked by simple repeat sequence (SSR) molecular markers AC196708-4 and AC233922-1. Sequencing analysis of candidate genes from Ms53 and B73 revealed that the 288th amino acid of a SBP-box transcription factor is substituted from glycine to serine and probably leads to the mutant phenotype. These studies will pave the way for elucidating the molecular mechanisms underlying anther development.

Keywords

Male-sterile mutant Ms53 Fine mapping SBP-box gene 

Notes

Acknowledgements

This study was supported by a China Postdoctoral Science Foundation funded project (2014M552303), Fundamental Research Funds for the Central Universities (XDJK2015B009), Technology Integration and Demonstration of Zhongkeyu 9699 and Xidabainuo No.1 (cstc2015jcsf-nycgzhA80006) and the China Scholarship Council.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest.

Supplementary material

10681_2018_2132_MOESM1_ESM.docx (45 kb)
Supplementary material 1 (DOCX 44 kb)
10681_2018_2132_MOESM2_ESM.docx (112 kb)
Supplementary material 2 (DOCX 111 kb)

References

  1. Bohra A, Jha UC, Adhimoolam P, Bisht D, Singh NP (2016) Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep 35:967–993CrossRefPubMedGoogle Scholar
  2. 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):778–788PubMedGoogle Scholar
  3. Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefPubMedGoogle Scholar
  4. Chuck GS, Brown PJ, Meeley R, Hake S (2014) Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc Natl Acad Sci 111(52):18775–18780CrossRefPubMedPubMedCentralGoogle Scholar
  5. Feng Y, Zheng Q, Song H, Wang Y, Wang H, Jiang L, Yan J, Zheng Y, Yue B (2015) Multiple loci not only Rf3 involved in the restoration ability of pollen fertility, anther exsertion and pollen shedding to S type cytoplasmic male sterile in maize. Theoretical and Applied Genetics 128(11):2341–2350CrossRefPubMedGoogle Scholar
  6. Figueroa P, Browse J (2015) Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J 81(6):849–860CrossRefPubMedGoogle Scholar
  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(8):942–952CrossRefPubMedPubMedCentralGoogle Scholar
  8. Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49(4):683–693CrossRefPubMedGoogle Scholar
  9. Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147(2):852–863CrossRefPubMedPubMedCentralGoogle Scholar
  10. Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266(1):383CrossRefPubMedGoogle Scholar
  11. Ito T, Shinozaki K (2002) The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a phd-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43(11):1285–1292CrossRefPubMedGoogle Scholar
  12. Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucl Acids Res 42:1182–1187CrossRefGoogle Scholar
  13. Kheyr-Pour A, Gracen V, Everett H (1981) Genetics of fertility restoration in the C-group of cytoplasmic male sterility in maize. Genetics 98(2):379–388PubMedPubMedCentralGoogle Scholar
  14. Li Q, Wan JM (2005) SSRHunter: development of a local searching software for SSR sites. Hereditas 27(5):808PubMedGoogle Scholar
  15. Li S, Yang D, Zhu Y (2007) Characterization and use of male sterility in hybrid rice breeding. J Integr Plant Biol 49(6):791–804CrossRefGoogle Scholar
  16. Li J, Yu M, Geng LL, Zhao J (2010) The fasciclin-like arabinogalactan protein gene, FLA3, is involved in microspore development of Arabidopsis. Plant J 64(3):482–497CrossRefPubMedGoogle Scholar
  17. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434CrossRefPubMedGoogle Scholar
  18. Ma J, Yan B, Qu Y, Qin F, Yang Y, Hao X, Yu J, Zhao Q, Zhu D, Ao G (2008) Zm401, a short-open reading-frame mRNA or noncoding RNA, is essential for tapetum and microspore development and can regulate the floret formation in maize. J Cell Biochem 105(1):136–146CrossRefPubMedGoogle Scholar
  19. McCormick S (2004) Control of male gametophyte development. Plant Cell 16(suppl 1):S142–S153CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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):592–602CrossRefPubMedPubMedCentralGoogle Scholar
  21. Nan G, Zhai J, Arikit S, Morrow D, Fernandes J, Mai L, Nguyen N, Meyers B, Walbot V (2017) MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development 144(1):163–172CrossRefPubMedGoogle Scholar
  22. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425PubMedGoogle Scholar
  23. Salinas M, Xing S, Höhmann S, Berndtgen R, Huijser P (2012) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 235(6):1171–1184CrossRefPubMedGoogle Scholar
  24. Saxena KB, Hingane AJ (2015) Male sterility systems in major field crops and their potential role in crop improvement. In: Bahadur B, Venkat Rajam M, Sahijram L, Krishnamurthy KV (eds) Plant biology and biotechnology, vol I. Plant diversity, organization function and improvement. Springer, New Delhi, pp 639–656CrossRefGoogle Scholar
  25. Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153(2):933–941PubMedPubMedCentralGoogle Scholar
  26. Shukla P, Singh NK, Kumar D, Vijayan S, Ahmed I, Kirti PB (2014) Expression of a pathogen-induced cysteine protease (AdCP) in tapetum results in male sterility in transgenic tobacco. Funct Integr Genomics 14(2):307–317CrossRefPubMedGoogle Scholar
  27. Sinha R, Rajam MV (2013) RNAi silencing of three homologues of S-adenosylmethionine decarboxylase gene in tapetal tissue of tomato results in male sterility. Plant Mol Biol 82(1–2):169–180CrossRefPubMedGoogle Scholar
  28. Skibbe D, Schnable P (2005) Male sterility in maize. Maydica 50(3/4):367Google Scholar
  29. Sofi PA, Rather A, Wani SA (2007) Genetic and molecular basis of cytoplasmic male sterility in maize. Commun Biometry Crop Sci 2:49–60Google Scholar
  30. Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(1):S10.1–S10.12CrossRefPubMedPubMedCentralGoogle Scholar
  31. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725CrossRefPubMedPubMedCentralGoogle Scholar
  32. Unger E, Cigan AM, Trimnell M, R-j Xu, Kendall T, Roth B, Albertsen M (2002) A chimeric ecdysone receptor facilitates methoxyfenozide-dependent restoration of male fertility in ms45 maize. Transgenic Res 11:455–465CrossRefPubMedGoogle Scholar
  33. Unte US, Sorensen A-M, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15(4):1009–1019CrossRefPubMedPubMedCentralGoogle Scholar
  34. Wang D, Skibbe DS, Walbot V (2013) Maize Male sterile 8 (Ms8), a putative β-1, 3-galactosyltransferase, modulates cell division, expansion, and differentiation during early maize anther development. Plant Reprod 26(4):329–338CrossRefPubMedGoogle Scholar
  35. Wang Y, Gu R, Chen H, Shi H, Yu X, Zhang H, Zhao C, Sun Q, Ke Y (2015) Characterization and genetic mapping of a novel recessive genic male sterile gene ms305 in maize (Zea mays L.). Israel J Plant Sci 62:208–214CrossRefGoogle Scholar
  36. Wise RP, Dill CL, Schnable PS (1996) Mutator-induced mutations of the rf1 nuclear fertility restorer of t-cytoplasm maize alter the accumulation of t-urfl3 mitochondrial transcripts. Genetics 143(3):1383–1394PubMedPubMedCentralGoogle Scholar
  37. Wise RP, Bronson CR, Schnable PS, Horner HT (1999) The genetics, pathology, and molecular biology of T-cytoplasm male sterility in maize. Adv Agron 65:79–130CrossRefGoogle Scholar
  38. Woo MO, Ham TH, Ji HS, Choi MS, Jiang W, Chu SH, Piao R, Chin JH, Kim JA, Park BS (2008) Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J 54(2):190–204CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wu Y, Fox TW, Trimnell MR, Wang L, Rj Xu, 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):1046–1054CrossRefPubMedGoogle Scholar
  40. Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142(1):280–293CrossRefPubMedPubMedCentralGoogle Scholar
  41. Xing S, Salinas M, Höhmann S, Berndtgen R, Huijser P (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22(12):3935–3950CrossRefPubMedPubMedCentralGoogle Scholar
  42. Xing S, Quodt V, Chandler J, Höhmann S, Berndtgen R, Huijser P (2013) SPL8 acts together with the brassinosteroid-signaling component BIM1 in controlling Arabidopsis thaliana male fertility. Plants 2(3):416–428CrossRefPubMedPubMedCentralGoogle Scholar
  43. Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407(1):1–11CrossRefPubMedGoogle Scholar
  44. Zabala G, Gabay-Laughnan S, Laughnan JR (1997) The nuclear gene Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male sterility in maize. Genetics 147(2):847–860PubMedPubMedCentralGoogle Scholar
  45. Zhang H, Xu C, He Y, Zong J, Yang X, Si H, Sun Z, Hu J, Liang W, Zhang D (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci 110(1):76–81CrossRefPubMedGoogle Scholar
  46. Zhang L, Mao D, Xing F, Bai X, Zhao H, Yao W, Li G, Xie W, Xing Y (2015) Loss of function of OsMADS3 via the insertion of a novel retrotransposon leads to recessive male sterility in rice (Oryza sativa). Plant Sci 238:188–197CrossRefPubMedGoogle Scholar
  47. Zhang W, Bei L, Bin Y (2016) Genome-wide identification, phylogeny and expression analysis of the SBP-box gene family in maize (Zea mays). J Integr Agric 15(1):29–41CrossRefGoogle Scholar
  48. Zhang D, Wu S, An X, Xie K, Dong Z, Zhou Y, Xu L, Fang W, Liu S, Liu S, Zhu T, Li J, Rao L, Zhao J, Wan X (2017) Construction of a multicontrol 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.  https://doi.org/10.1111/pbi.12786 Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Chaoxian Liu
    • 1
  • Guoqiang Wang
    • 1
  • Jie Gao
    • 2
  • Chunyan Li
    • 1
  • Ziru Zhang
    • 1
  • Tingting Yu
    • 1
  • Jiuguang Wang
    • 1
  • Lian Zhou
    • 1
  • Yilin Cai
    • 1
  1. 1.Maize Research InstituteSouthwest UniversityChongqingChina
  2. 2.National Maize Improvement Center of ChinaChina Agricultural UniversityBeijingChina

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