Abstract
Key message
Using map-based cloning, we delimited the Ms - cd1 gene responsible for the male sterile phenotype in B. oleracea to an approximately 39-kb fragment. Expression analysis suggests that a new predicted gene, a homolog of the Arabidopsis SIED1 gene, is a potential candidate gene.
Abstract
A dominant genic male sterile (DGMS) mutant 79-399-3 in Brassica oleracea (B. oleracea) is controlled by a single gene named Ms-cd1, which was genetically mapped on chromosome C09. The derived DGMS lines of 79-399-3 have been successfully applied in hybrid cabbage breeding and commercial hybrid seed production of several B. oleracea cultivars in China. However, the Ms-cd1 gene responsible for the DGMS has not been identified, and the molecular basis of the DGMS is unclear, which then limits its widespread application in hybrid cabbage seed production. In the present study, a large BC9 population with 12,269 individuals was developed for map-based cloning of the Ms-cd1 gene, and Ms-cd1 was mapped to a 39.4-kb DNA fragment between two InDel markers, InDel14 and InDel24. Four genes were identified in this region, including two annotated genes based on the available B. oleracea annotation database and two new predicted open reading frames (ORFs). Finally, a newly predicted ORF designated Bol357N3 was identified as the candidate of the Ms-cd1 gene. These results will be useful to reveal the molecular mechanism of the DGMS and develop more practical DGMS lines with stable male sterility for hybrid seed production in cabbage.
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Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178
Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83
Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B (2008) Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ 31:1592–1605
Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. Comptes Rendus de l’Académie des Sciences–Series III—Sciences de la Vie 324:543–550
Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial–nuclear interactions. Trends Genet 23:81–90
Chen L, Liu Y-G (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606
Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136
Cheng F, Wu J, Fang L, Wang X (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198
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 97:265–268
Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2008) Global analysis of gene expression in flower buds of Ms-cd1 Brassica oleracea conferring male sterility by using an Arabidopsis microarray. Plant Mol Biol 66:177–192
Lee J, Koh H-J (2013) Gene identification using rice genome sequences. Genes Genom 35:415–424
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Hu Z, Zhuang M, Huang J, Shi J, Mei D, Liu J, Lee TH, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Lou P, Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2007) Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119
Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:1–18
Peng J, Li Z, Wen X, Li W, Shi H, Yang L, Zhu H, Guo H (2014) Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet 10:e1004664
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183
Wang XW, Fang ZY, Sun PT, Liu YM, Yang LM (1998) Identification of a RAPD marker linked to a dominant male sterile gene in cabbage. Acta Hortic Sin 25(2):197–198
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
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
Wang XW, Lou P, Bonnema G, Yang BJ, He HJ, Zhang YG, Fang ZY (2005) Linkage mapping of a dominant male sterility gene Ms-cd1 in Brassica oleracea. Genome 48:848–854
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Yu J, Meng J, Min J, Poulain J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Z, Li Z, Xiong Z, Zhang Z (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039
Wang X, Wu J, Liang J, Cheng F, Wang X (2015) Brassica database (BRAD) version 2.0: integrating and mining Brassicaceae species genomic resources. Database 2015: bav093
Yang Y-W, Lai K-N, Tai P-Y, Li W-H (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J Mol Evol 48:597–604
Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant cell 19:3530–3548
Yang ZT, Wang MJ, Sun L, Lu SJ, Bi DL, Song ZT, Zhang SS, Zhou SF, Liu JX (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10:e1004243
Zhang X, Wu J, Zhang H, Ma Y, Guo A, Wang X (2011) Fine mapping of a male sterility gene MS-cd1 in Brassica oleracea. Theor Appl Genet 123:231–238
Zheng SJ, van Dijk JP, Bruinsma M, Dicke M (2007) Sensitivity and speed of induced defense of cabbage (Brassica oleracea L.): dynamics of BoLOX expression patterns during insect and pathogen attack. Mol Plant Microbe Interact 20:1332–1345
Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P, Lu S, Li F, Zhu L, Liu Z, Chen L, Liu YG, Zhuang C (2012) Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res 22:649–660
Zhou H, Zhou M, Yang Y, Li J, Zhu L, Jiang D, Dong J, Liu Q, Gu L, Zhou L, Feng M, Qin P, Hu X, Song C, Shi J, Song X, Ni E, Wu X, Deng Q, Liu Z, Chen M, Liu YG, Cao X, Zhuang C (2014) RNase Z (S1) processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884
Acknowledgments
This work was supported by funding from the National Program Fund for Key Basic Research Projects (the 973 Program: 2013CB127000), the National Natural Science Foundation of China (NSFC: 31301784), and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences. This research work was conducted at the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, China.
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Communicated by M. J. Havey.
J. Liang and Y. Ma have equally contributed to the study.
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122_2016_2792_MOESM1_ESM.pdf
Supplementary Fig. S1 The PCR products amplified by 9 two-marker combinations in parental lines and some BC9 individuals. P1: M20 + InDel28, P2: M20 + InDelN31, P3: M20L + InDel28, P4: M20L + InDelN31, P5: InDelN1 + InDelN31, P6: InDelN3 + InDelN31, P7: IndelN4 + IndelN31, P8: IndelN6 + IndelN31, P9: sf32-SSR6 + IndelN31. M: Marker, ck: recurrent parent, S: BC9 sterile individuals, F: BC9 fertile individuals (PDF 64 kb)
122_2016_2792_MOESM2_ESM.pdf
Supplementary Fig. S2 Five putative ORFs of the 39.4 kb (B. oleracea) region identified by Softberry website (PDF 76 kb)
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Liang, J., Ma, Y., Wu, J. et al. Map-based cloning of the dominant genic male sterile Ms-cd1 gene in cabbage (Brassica oleracea). Theor Appl Genet 130, 71–79 (2017). https://doi.org/10.1007/s00122-016-2792-1
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DOI: https://doi.org/10.1007/s00122-016-2792-1