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

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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.

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References

  • Bohra A, Jha UC, Adhimoolam P, Bisht D, Singh NP (2016) Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep 35:967–993

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • 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):18775–18780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):2341–2350

    Article  CAS  PubMed  Google Scholar 

  • Figueroa P, Browse J (2015) Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J 81(6):849–860

    Article  CAS  PubMed  Google Scholar 

  • 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):942–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):683–693

    Article  CAS  PubMed  Google Scholar 

  • 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):852–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266(1):383

    Article  CAS  PubMed  Google Scholar 

  • 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):1285–1292

    Article  CAS  PubMed  Google Scholar 

  • 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 42:1182–1187

    Article  Google Scholar 

  • 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):379–388

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Wan JM (2005) SSRHunter: development of a local searching software for SSR sites. Hereditas 27(5):808

    PubMed  Google Scholar 

  • Li S, Yang D, Zhu Y (2007) Characterization and use of male sterility in hybrid rice breeding. J Integr Plant Biol 49(6):791–804

    Article  CAS  Google Scholar 

  • 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):482–497

    Article  CAS  PubMed  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  CAS  PubMed  Google Scholar 

  • 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):136–146

    Article  CAS  PubMed  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16(suppl 1):S142–S153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):163–172

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • 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):1171–1184

    Article  CAS  PubMed  Google Scholar 

  • 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 639–656

    Chapter  Google Scholar 

  • 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):933–941

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):307–317

    Article  CAS  PubMed  Google Scholar 

  • 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):169–180

    Article  CAS  PubMed  Google Scholar 

  • Skibbe D, Schnable P (2005) Male sterility in maize. Maydica 50(3/4):367

    Google Scholar 

  • Sofi PA, Rather A, Wani SA (2007) Genetic and molecular basis of cytoplasmic male sterility in maize. Commun Biometry Crop Sci 2:49–60

    Google Scholar 

  • Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(1):S10.1–S10.12

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:455–465

    Article  CAS  PubMed  Google Scholar 

  • 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):1009–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):329–338

    Article  CAS  PubMed  Google Scholar 

  • 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 62:208–214

    Article  Google Scholar 

  • 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):1383–1394

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wise RP, Bronson CR, Schnable PS, Horner HT (1999) The genetics, pathology, and molecular biology of T-cytoplasm male sterility in maize. Adv Agron 65:79–130

    Article  CAS  Google Scholar 

  • 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):190–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1046–1054

    Article  CAS  PubMed  Google Scholar 

  • 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):280–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):3935–3950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):416–428

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):1–11

    Article  CAS  PubMed  Google Scholar 

  • 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):847–860

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):76–81

    Article  PubMed  Google Scholar 

  • 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 238:188–197

    Article  CAS  PubMed  Google Scholar 

  • 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):29–41

    Article  CAS  Google Scholar 

  • 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 

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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.

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Correspondence to Yilin Cai.

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Liu, C., Wang, G., Gao, J. et al. Characterization, fine mapping and candidate gene analysis of novel, dominant, nuclear male-sterile gene Ms53 in maize. Euphytica 214, 52 (2018). https://doi.org/10.1007/s10681-018-2132-4

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