Theoretical and Applied Genetics

, Volume 131, Issue 1, pp 183–191 | Cite as

Fine mapping of the genic male-sterile ms 1 gene in Capsicum annuum L.

Original Article
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Abstract

Key message

The genomic region cosegregating with the genic male-sterile ms 1 gene of Capsicum annuum L. was delimited to a region of 869.9 kb on chromosome 5 through fine mapping analysis. A strong candidate gene, CA05g06780, a homolog of the Arabidopsis MALE STERILITY 1 gene that controls pollen development, was identified in this region.

Abstract

Genic male sterility caused by the ms 1 gene has been used for the economically efficient production of massive hybrid seeds in paprika (Capsicum annuum L.), a colored bell-type sweet pepper. Previously, a CAPS marker, PmsM1-CAPS, located about 2–3 cM from the ms 1 locus, was reported. In this study, we constructed a fine map near the ms 1 locus using high-resolution melting (HRM) markers in an F2 population consisting of 1118 individual plants, which segregated into 867 male-fertile and 251 male-sterile plants. A total of 12 HRM markers linked to the ms 1 locus were developed from 53 primer sets targeting intraspecific SNPs derived by comparing genome-wide sequences obtained by next-generation resequencing analysis. Using this approach, we narrowed down the region cosegregating with the ms 1 gene to 869.9 kb of sequence. Gene prediction analysis revealed 11 open reading frames in this region. A strong candidate gene, CA05g06780, was identified; this gene is a homolog of the Arabidopsis MALE STERILITY 1 (MS1) gene, which encodes a PHD-type transcription factor that regulates pollen and tapetum development. Sequence comparison analysis suggested that the CA05g06780 gene is the strongest candidate for the ms 1 gene of paprika. To summarize, we developed a cosegregated marker, 32187928-HRM, for marker-assisted selection and identified a strong candidate for the ms 1 gene.

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Notes

Acknowledgements

This research was supported by the “Cooperative Research Program for Agriculture Science & Technology Development” (Project no. PJ 01229801), Rural Development Administration, Republic of Korea. We are grateful to Soung-Woo Park for providing paprika F2 segregating seeds (NHSEED, South Korea).

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary material

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Supplementary material 1 (DOCX 1540 kb)

References

  1. Akter S, Huq MA, Jung YJ, Cho YG, Kang KK (2016) Application of single nucleotide polymorphism markers for selection of male sterility in crop plants. Plant Breed Biotech 4:379–386CrossRefGoogle Scholar
  2. Aulakh PS, Dhaliwal MS, Jindal SK, Schafleitner R, Singh K (2016) Mapping of male sterility gene ms10 in chilli pepper (Capsicum annuum L.). Plant Breed 135:531–535CrossRefGoogle Scholar
  3. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefPubMedGoogle Scholar
  4. Bartoszewski G, Waszczak C, Gawroński P, Stępień I, Bolibok-Brągoszewska H, Palloix A, Lefebvre V, Korzeniewska A, Niemirowicz-Szczytt K (2012) Mapping of the ms8 male sterility gene in sweet pepper (Capsicum annuum L.) on the chromosome P4 using PCR-based markers useful for breeding programmes. Euphytica 186:453–461CrossRefGoogle Scholar
  5. Bienz M (2006) The PHD finger, a nuclear protein-interaction domain. Trends Biochem Sci 31:35–40CrossRefPubMedGoogle Scholar
  6. 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
  7. Chen C, Chen G, Hao X, Cao B, Chen Q, Liu S, Lei J (2011) CaMF2, an anther-specific lipid transfer protein (LTP) gene, affects pollen development in Capsicum annuum L. Plant Sci 181:439–448CrossRefPubMedGoogle Scholar
  8. Chen CM, Hao XF, Chen GJ, Cao BH, Chen QH, Liu SQ, Lei JJ (2012) Characterization of a new male sterility-related gene Camf1 in Capsicum annuum L. Mol Biol Rep 39:737–744CrossRefPubMedGoogle Scholar
  9. Chen C, Chen G, Cao B, Lei J (2015) Transcriptional profiling analysis of genic male sterile-fertile Capsicum annuum reveal candidate genes for pollen development and maturation by RNA-Seq technology. Plant Cell Tiss Organ Cult 122:465–476CrossRefGoogle Scholar
  10. deSilva D, Blackett J (2007) Assay: high-resolution melting & unlabeled probes. Genetic Engineering & Biotechnology News. http://www.genengnews.com/gen-articles/assay-high-resolution-melting-unlabeled-probes/1986. Accessed 20 Sept 2017
  11. Dhaliwal MS, Jindal SK (2014) Induction and exploitation of nuclear and cytoplasmic male sterility in pepper (Capsicum spp.): a review. J Hortic Sci Biotechnol 89:471–479CrossRefGoogle Scholar
  12. Eun MH, Han JH, Yoon JB, Lee JD (2016) QTL mapping of resistance to the Cucumber mosaic virus P1 strain in pepper using a genotyping-by-sequencing analysis. Hortic Environ Biotechnol 57:589–597CrossRefGoogle Scholar
  13. Fu D, Xiao M, Hayward A, Fu Y, Liu G, Jiang G, Zhang H (2014) Utilization of crop heterosis: a review. Euphytica 197:161–173CrossRefGoogle Scholar
  14. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principle and practical applications. Plant Cell 5:1217–1229CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 117:11–18CrossRefPubMedGoogle Scholar
  16. Huang Z, Chen Y, Yi B, Xiao L, Ma C, Tu J, Fu T (2007) Fine mapping of the recessive genic male sterility gene (Bnms3) in Brassica napus L. Theor Appl Genet 115:113–118CrossRefPubMedGoogle Scholar
  17. 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 43:1285–1292CrossRefPubMedGoogle Scholar
  18. Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K (2007) Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19:3549–3562CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kim S, Park M, Yeom SI, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270CrossRefPubMedGoogle Scholar
  20. Kim JS, An CG, Park JS, Lim YP, Kim S (2016) Carotenoid profiling from 27 types of paprika (Capsicum annuum L.) with different colors, shapes, and cultivation methods. Food Chem 201:64–71CrossRefPubMedGoogle Scholar
  21. Kosambi DD (1944) The estimation of map distance from recombination value. Ann Eugen 12:172–175CrossRefGoogle Scholar
  22. Lee DS, Chen LJ, Suh HS (2005) Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile gene tms6 in rice (Oryza sativa L.). Theor Appl Genet 111:1271–1277CrossRefPubMedGoogle Scholar
  23. Lee J, Yoon JB, Park HG (2008) A CAPS marker associated with the partial restoration of cytoplasmic male sterility in chili pepper (Capsicum annuum L.). Mol Breed 21:95–104CrossRefGoogle Scholar
  24. Lee J, Han JH, An CG, Lee WP, Yoon JB (2010a) A CAPS marker linked to a genic male-sterile gene in the colored sweet pepper, ‘Paprika’ (Capsicum annuum L.). Breed Sci 60:93–98CrossRefGoogle Scholar
  25. Lee J, Lee WP, Han JH, Yoon JB (2010b) Development of molecular marker linked to a genic male-sterile gene, ms k in chili pepper. Korean J Hortic Sci Technol 28:270–274Google Scholar
  26. Lee J, Yoon JB, Han JH, Lee WP, Kim SH, Park HG (2010c) Three AFLP markers tightly linked to the genic male sterility ms 3 gene in chili pepper (Capsicum annuum L.) and conversion to a CAPS marker. Euphytica 173:55–61CrossRefGoogle Scholar
  27. Lee J, Do JW, Han JH, An CG, Kweon OY, Kim YK, Yoon JB (2011) Allelism and molecular marker tests for genic male sterility in paprika cultivars. Korean J Hortic Sci Technol 29:130–134Google Scholar
  28. Lee HR, An HJ, Yang DC, Choi SH, Kim HJ (2012) Development of a high resolution melting (HRM) marker linked to genic male sterility in Capsicum annuum L. Plant Breeding 131:444–448CrossRefGoogle Scholar
  29. Lei S, Yao X, Yi B, Chen W, Ma C, Tu J, Fu T (2007) Towards map-based cloning: fine 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 115:643–651CrossRefPubMedGoogle Scholar
  30. 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 125:223–234CrossRefPubMedGoogle Scholar
  31. Liang J, Ma Y, Wu J, Cheng F, Liu B, Wang X (2017) Map-based cloning of the dominant genic male sterile Ms-cd1 gene in cabbage (Brassica oleracea). Theor Appl Genet 130:71–79CrossRefPubMedGoogle Scholar
  32. Liu DF (1992) The theoretical studies on the restoration for dominant genic male sterility in plants. Heriditas 14:31–36Google Scholar
  33. Peng HF, Chen XH, Lu YP, Peng YF, Wan BH, Chen ND, Wu B, Xin SP, Zhang GQ (2010) Fine mapping of a gene for non-pollen type thermosensitive genic male sterility in rice (Oryza sativa L.). Theor Appl Genet 120:1013–1020CrossRefPubMedGoogle Scholar
  34. Poland JA, Rife TW (2012) Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102CrossRefGoogle Scholar
  35. Qi Y, Liu Q, Zhang L, Mao B, Yan D, Jin Q, He Z (2014) Fine mapping and candidate gene analysis of the novel thermo-sensitive genic male sterility tms9-1 gene in rice. Theor Appl Genet 127:1173–1182CrossRefPubMedGoogle Scholar
  36. Shifriss C (1997) Male sterility in pepper (Capsicum annuum L.). Euphytica 93:83–88CrossRefGoogle Scholar
  37. Simko I (2016) High-resolution DNA melting analysis in plant research. Trends Plant Sci 21:528–537CrossRefPubMedGoogle Scholar
  38. Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(Suppl I):S10CrossRefPubMedPubMedCentralGoogle Scholar
  39. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  40. Wang D, Bosland PW (2006) The genes of Capsicum. HortSci 41:1169–1187Google Scholar
  41. Wang YG, Xing QH, Deng QY, Liang FS, Yuan LP, Weng ML, Wang B (2003) Fine mapping of the rice thermo-sensitive genic male-sterile gene tms5. Theor Appl Genet 107:917–921CrossRefPubMedGoogle Scholar
  42. Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY 1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39CrossRefPubMedGoogle Scholar
  43. Xu J, Wang B, Wu Y, Du P, Wang J, Wang M, Yi C, Gu M, Liang G (2011) Fine mapping and candidate gene analysis of ptgms2-1, the photoperiod-thermo-sensitive genic male sterile gene in rice (Oryza sativa L.). Theor Appl Genet 122:365–372CrossRefPubMedGoogle Scholar
  44. Yang Q, Liang C, Zhuang W, Li J, Deng H, Deng Q, Wang B (2007) Characterization and identification of the candidate gene of rice thermo-sensitive genic male sterile gene tms5 by mapping. Planta 225:321–330CrossRefPubMedGoogle Scholar
  45. 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 113:643–650CrossRefPubMedGoogle Scholar
  46. 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 22:649–660CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of HorticultureChonbuk National UniversityJeonjuSouth Korea
  2. 2.Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life SciencesSeoul National UniversitySeoulSouth Korea

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