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Identification of a male sterile gene Ms in Brassica rapa L.

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Abstract

Male sterile lines are important for hybrid seed production in Brassica rapa. In our previous study, we obtained a multiple-allele inherited male sterile line of Chinese cabbage. To identify the male sterile gene Ms in B. rapa, we used B. rapa L. var. chinensis (‘AB03’; MsMs) and B. rapa var. purpuraria (‘AB04’; MsfMsf) as parents to construct an F2 segregating population, and mapped the Ms gene on chromosome A07 between single sequence repeat (SSR) markers SSRY17 and SSRY22, which flank the gene at genetic distances of 0.11 cM and 0.31 cM, respectively. The interval between the two markers was 231.3 kb and comprised 21 genes. Whole-genome resequencing and sequence comparison revealed that only one gene, Bra015018, harbored an insertion–deletion (InDel) in an exon in the mapped interval. This InDel led to premature termination of translation due to generation of the stop codon TGA. Bra015018 was homologous to AT1G34355, which encoded a forkhead-associated (FHA) domain-containing protein that was related to plant growth and floral development. Genotyping revealed that male sterility was fully co-segregated with the InDel. qRT-PCR analysis showed that Bra015018 was specifically expressed in the stamen. Consequently, we predicted that Bra015018 was a candidate gene of Ms.

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References

  • Ahn ER, Cho HK, Pai HS (2013) The forkhead-associated domain 2 (FHA2) in Arabidopsis plays a role in plant fertility by regulating stamen development. Planta 237(4):1015–1023

  • Barrero JM, Piqueras P, Gonza’lez-Guzma’n M, Serrano R, Rodrı’guez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56:2071–2083

    Article  CAS  PubMed  Google Scholar 

  • Bino RJ (1985) Histological aspects of microsporogenesis in fertile, cytoplasmic male sterile and restored fertile Petunia hybrida. Theor Appl Genet 69:423–428

    Article  CAS  PubMed  Google Scholar 

  • Brogna S, Wen J (2009) Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 16:107–113

    Article  CAS  PubMed  Google Scholar 

  • Chang YF, Imam JS, Wilkinson MF (2007) The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76:51–74

    Article  CAS  PubMed  Google Scholar 

  • Chaudhury AM (1993) Nuclear genes controlling male fertility. Plant Cell 5(10):1277–1283

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng Q, Wang P, Liu J, Wu L, Zhang Z, Li T, Gao W, Yang W, Sun L, Shen H (2018) Identification of candidate genes underlying genic male-sterile msc-1 locus via genome resequencing in Capsicum annuum L. Theor Appl Genet 131(9):1861–1872

    Article  CAS  PubMed  Google Scholar 

  • Choi H, Jin JY, Choi S, Hwang JU, Kim YY, Suh MC, Lee Y (2011) An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J 65(2):181–193

    Article  CAS  PubMed  Google Scholar 

  • Doma MK, Parker R (2007) RNA quality control in eukaryotes. Cell 131(4):660–668

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42(3):315–328

    Article  CAS  PubMed  Google Scholar 

  • Dun X, Zhou Z, Xia S, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T (2011) BnaC.Tic40, a plastid inner membrane translocon originating from Brassica oleracea, is essential for tapetal function and microspore development in Brassica napus. Plant J 68(3):532–545

    Article  CAS  PubMed  Google Scholar 

  • Fang Z, Sun P, Liu Y, Yang L, Wang X, Hou A, Bian C (1997) A male sterile line with dominant gene (Ms) in cabbage (Brassica oleracea var. capitata) and its utilization for hybrid seed production. Euphytica. 97(3):265–268

    Article  Google Scholar 

  • Feng H, Wei YT, Zhang SN (1995) Inheritance of and utilization model for genic male sterility in Chinese cabbage (Brassica pekinensis Rupr.). Acta Hortic 402:133–140

    Google Scholar 

  • Feng H, Wei YT, Ji SJ, Jin G, Jin JS, Dong WJ (1996) Multiple allele model for genic male sterility in Chinese cabbage. Acta Hortic 467:133–142

    Google Scholar 

  • Feng H, Xu W, Wang YG (2007) Directive transfer of the genetic male sterile line of milk Chinese cabbage AI023. Acta Hortic Sin 34:659–664

    CAS  Google Scholar 

  • Feng H, Wei P, Piao ZY, Liu ZY, Li CY, Wang YG, Ji RQ, Ji SJ, Zou T, Choi SR, Lim YP (2009) SSR and SCAR mapping of a multiple-allele male-sterile gene in Chinese cabbage (Brassica rapa L.). Theor Appl Genet 119:333–339

    Article  CAS  PubMed  Google Scholar 

  • Fletcher JC (2002) Shoot and floral meristem maintenance in Arabidopsis. Annu Rev Plant Biol 53:45–66

    Article  CAS  PubMed  Google Scholar 

  • He J, Ke L, Hong D, Xie Y, Wang G, Liu P, Yang G (2008) Fine mapping of a recessive genic male sterility gene (Bnms3) in rapeseed - (Brassica napus) with AFLP- and Arabidopsis-derived PCR markers. Theor Appl Genet 117:11–18

    Article  CAS  PubMed  Google Scholar 

  • He, J., Zhao, X., Laroche, A., Lu, Z. X., Liu, H., and Li, Z. (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5

  • Hua Y, Zhang D, Zhou T, He M, Ding G, Shi L, Xu F (2016) Transcriptomics-assisted quantitative trait locus fine mapping for the rapid identification of a nodulin 26-like intrinsic protein gene regulating boron efficiency in allotetraploid rapeseed. Plant Cell Environ 39:1601–1618

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Cao J, Zhang A, Ye Y, Zhang Y, Liu T (2009) The polygalacturonase gene BcMF2 from Brassica campestris is associated with intine development. J Exp Bot 60(1):301–313

    Article  CAS  PubMed  Google Scholar 

  • Ji JL, Yang LM, Fang ZY, Zhuang M, Zhang YY, Lv HH, Liu YM, Li ZS (2017) Recessive male sterility in cabbage (Brassica oleracea var. capitata) caused by loss of function of BoCYP704B1 due to the insertion of a LTR-retrotransposon. Theor Appl Genet 130:1441–1451

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Yu Y, Dong H, Yao L, Zhang Z, Cao J (2014) BcMF21 is important for pollen development and germination in Brassica campestris ssp. chinensis. Mol Biol Rep 41(1):537–544

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugenics 12:172–175

    Article  Google Scholar 

  • Lei S, Yao X, Yi B, Chen W, Ma C, Tu J, Fu T (2007) Towards map-based cloning: fne mapping of a recessive genic male-sterile gene (BnMs2) in Brassica napus L. and syntenic region identification based on the Arabidopsis thaliana genome sequences. Theor Appl Genet 115:643–651

    Article  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Smith GP, Walker JC (1999) Kinase interaction domain of kinase-associated protein phosphatase, a phosphoprotein-binding domain. Proc Natl Acad Sci U S A 96:7821–7826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Hong D, He J, Ma L, Wan L, Liu P, Yang G (2012) Map-based cloning of a recessive genic male sterility locus in Brassica napus L. and development of its functional marker. Theor Appl Genet 125:223–234

    Article  CAS  PubMed  Google Scholar 

  • Liang Q, Wen D, Xie J, Liu L, Wei Y, Wang Y, Shi S (2014) A rapid and effective method for silver staining of PCR products separate in polyacrylamide gels. Electrophoresis 35(17):2520–2523

    Article  CAS  PubMed  Google Scholar 

  • Liang JL, Ma Y, Wu J, Cheng F, Liu B, Wang XW (2017) Map-based cloning of the dominant genic male sterile Ms-cd1 gene in cabbage (Brassica oleracea). Theor Appl Genet 130(1):71–79

    Article  CAS  PubMed  Google Scholar 

  • Lin S, Dong H, Zhang F, Qiu L, Wang F, Cao J, Huang L (2014) BcMF8, a putative arabinogalactan protein-encoding gene, contributes to pollen wall development, aperture formation and pollen tube growth in Brassica campestris. Ann Bot 113(5):777–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin S, Huang L, Yu XL, Xiong XP, Yue XY, Liu TT, Liang Y, Lv ML, Cao JS (2017) Characterization of BcMF23a and BcMF23b, two putative pectin methylesterase genes related to pollen development in Brassica campestris ssp. chinensis. Mol Biol Rep 44(1):139–148

    Article  CAS  PubMed  Google Scholar 

  • Liu XD, Huang J, Parameswaran S, Ito T, Seubert B, Auer M, Rymaszewski A, Jia GX, Owen HA, Zhao DZ (2009) The SPOROCYTELESS/NOZZLE gene is involved in controlling stamen identity in Arabidopsis. Plant Physiol 151:1401–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu ZY, Feng H, Li CY, Wei P, Wang LL (2010) SCAR markers linked to Ms, a genetic male sterile gene in Chinese cabbage. Acta Hortic Sin 37:757–762

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△Ct method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Lyu ML, Yu YJ, Jiang JJ, Song LM, Liang Y, Ma ZM, Xiong XP, Cao JS (2015) BcMF26a and BcMF26b are duplicated polygalacturonase genes with divergent expression patterns and functions in pollen development and pollen tube formation in Brassica campestris. PLoS One 10(7):e0131173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore MJ (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309:1514–1518

    Article  CAS  PubMed  Google Scholar 

  • Morris ER, Chevalier D, Walker JC (2006) DAWDLE, a forkhead-associated domain gene, regulates multiple aspects of plant development. Plant Physiol 141(3):932–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prunet N, Morel P, Negrutiu I, Trehin C (2009) Time to stop: flower meristem termination. Plant Physiol 150:1764–1772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. P Natl Acad Sci USA 96:11664–11669

    Article  CAS  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl):S46–S60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319

    Article  CAS  PubMed  Google Scholar 

  • Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  CAS  PubMed  Google Scholar 

  • Stone JM, Trotochaud AE, Walker JC, Clark SE (1998) Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol 117:1217–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan C, Liu ZY, Huang SN, Feng H (2018) Mapping of the male sterile mutant gene ftms in Brassica rapa L. ssp. pekinensis via BSR-Seq combined with whole-genome resequencing. Theor. Appl. Genet 132(2):355–370

    Google Scholar 

  • Van Ooijen J (2006) Joinmap 4.0 software for the calculation of genetic linkage maps in experimental populations. Wageningen, Kyazma BV

  • Vandermeer QP (1987) Chromosomal monogenic dominant male-sterility in Chinese-cabbage (Brassica-Rapa Subsp Pekinensis (Lour) Hanelt). Euphytica 36:927–931

    Article  Google Scholar 

  • Wang XW, Fang ZY, Huang SW, Sun PT, Liu YM, Yang LM, Zhuang M, Qu DY (2000a) An extended random primer amplified region (ERPAR) marker linked to a dominant male sterility gene in cabbage (Brassica oleracea var. capitata). Euphytica 112:267–273

    Article  CAS  Google Scholar 

  • Wang XW, Fang ZY, Sun PT, Liu YM, Yang LM, Zhuang M (2000b) A SCAR marker applicable in marker assisted selection of a dominant male sterility gene in cabbage. Acta Hortic Sin 27(2):143–144

    Google Scholar 

  • Wang YG, Feng H, Lin GR, Xu SF, Yang KY, Zhang NJ (2005) The transfer of genetic male sterile lines in Brassica campestris L. ssp. chinensis Makino. Acta Hortic Sin 32:628–631

    Google Scholar 

  • Wang LL, Wei P, Liu ZY, Li CY, Wang YG, Ji RQ, Feng H (2010) SSR mapping of the Msf, a multiple-allele male-fertility restorer gene in Chinese cabbage (Brassica campestris L. ssp. pekinensis). Acta Hortic Sin 37:923–930

    CAS  Google Scholar 

  • Wang N, Liu ZY, Zhang Y, Li CY, Feng H (2017) Identifcation and fine mapping of a stay-green gene (Brnye1) in pakchoi (Brassicacampestris L. ssp. chinensis). Theor Appl Genet 131(3):673–684

    Article  PubMed  CAS  Google Scholar 

  • Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492

    Article  CAS  PubMed  Google Scholar 

  • Xin Q, Shen Y, Li X, Lu W, Wang X, Han X, Dong FM, Wan LL, Yang GS, Hong DF, Cheng ZK (2016) MS5 mediates early meiotic progression and its natural variants may have applications for hybrid production in Brassica napus. Plant Cell 28(6):1263–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang H, Tao Y, Zheng Z, Li C, Sweetingham MW, Howieson JG (2012) Application of next-generation sequencing for rapid marker development in molecular plant breeding: a case study on anthracnose disease resistance in Lupinus angustifolius L. BMC Genomics 13:318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi B, Chen Y, Lei S, Tu J, Fu T (2006) Fine mapping of the recessive genic male-sterile gene (Bnms1) in Brassica napus L. Theor Appl Genet 113:643–650

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52:528–538

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    Article  CAS  PubMed  Google Scholar 

  • Zhou Z, Dun X, Xia S, Shi D, Qin M, Yi B, Wen J, Shen J, Ma C, Tu J, Fu T (2012) BnMs3 is required for tapetal differentiation and degradation, microspore separation, and pollen-wall biosynthesis in Brassica napus. J Exp Bot 63(5):2041–2058

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by grants from the National Natural Science Foundation of China (No. 31730082).

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Authors and Affiliations

  1. Department of Horticulture, Shenyang Agricultural University, 120 Dongling Road, Shenhe District, Shenyang, 110866, China

    Fengyan Shi, Zhiyong Liu, Nan Wang, Ying Zhao, Shiyao Dong, Jiaqi Zou & Hui Feng

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  1. Fengyan Shi
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  2. Zhiyong Liu
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Contributions

Fengyan Shi conducted the experiments, performed data analysis, and wrote the manuscript. Hui Feng and Zhiyong Liu directed the whole study including experimental design and manuscript revision. Nan Wang, Ying Zhao, Shiyao Dong, and Jiaqi Zou participated in the creation of materials. All authors have read and approved the final manuscript.

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Correspondence to Hui Feng.

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ESM 1

Genetic model of multiple-allele male sterility in a Chinese cabbage AB line (PNG 4072 kb)

High Resolution Image (TIF 10 mb)

ESM 2

Markers tightly linked to the Ms. gene. a, Recombinants with SSRY17 in the mapping population; b, Recombinants with SSRY22 in the mapping population. P1: AB04-F; P2: AB03-S. The asterisks represent recombinants. AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 1718 kb)

High Resolution Image (TIF 23.6 mb)

ESM 3

Promoter, full-length DNA, and coding sequence (CDS) amplification of Bra015018. a, Promoter amplicon; b, Full-length DNA amplicon; c, CDS amplicon. Markers are 2000, 1000, 750, 500, 250, and 100 bp from top to bottom. F: AB04-F; S: AB03-S; M: Marker (DNA ladder). AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 575 kb)

High Resolution Image (TIF 18.6 mb)

ESM 4

Alignment of the promoter sequences of Bra015018 in AB03-S and AB04-F. F: AB04-F; S: AB03-S. AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 35224 kb)

High Resolution Image (TIF 21 mb)

ESM 5

Sequence alignment of the Bra015018 gene in AB03-S and AB04-F. F: AB04-F; S: AB03-S. AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 367 kb)

High Resolution Image (TIF 24.6 mb)

ESM 6

Alignment of the CDS of Bra015018 in AB03-S and AB04-F. F: AB04-F; S: AB03-S. AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 4329 kb)

High Resolution Image (TIF 22 mb)

ESM 7

Bra015018 gene structure and protein sequence alignment. a, Bra015018 gene structure with the AB03-S mutant site; b, Alignment of amino acid sequences of Bra015018 in AB03-S and AB04-F. F: AB04-F; S: AB03-S. AB03-S and AB04-F are male sterile and male fertile lines, respectively, of Brassica rapa (PNG 4695 kb)

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Shi, F., Liu, Z., Wang, N. et al. Identification of a male sterile gene Ms in Brassica rapa L.. Mol Breeding 40, 61 (2020). https://doi.org/10.1007/s11032-020-01141-9

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