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Euphytica

, 215:109 | Cite as

Mitochondrial orf463 causing male sterility in radish is possessed by cultivars belonging to the ‘Niger’ group

  • H. YamagishiEmail author
  • Y. Tanaka
  • S. Shiiba
  • A. Hashimoto
  • A. Fukunaga
  • T. Terachi
Original Article
  • 59 Downloads

Abstract

In addition to Ogura cytoplasmic male sterility (CMS), which is used worldwide in radish and Brassica crops, another type of CMS was found and named DCGMS. A mitochondrial candidate gene (orf463) of DCGMS was identified, but the distribution of this gene in radish species has not been clarified to date. We found that orf463 is distributed specifically in black radish cultivars belonging to the ‘Niger’ group and a line of wild species, Raphanus raphanistrum. The progeny tests using the cultivars having orf463 as a female parent demonstrated that the cytoplasm induces male sterility in radishes. Although the DNA sequences of orf463 possessed by the ‘Niger’ group cultivars are identical to those of DCGMS, the orf463 sequence of the wild radish line contained nine nucleotide substitutions, seven of which were nonsynonymous. All radishes with orf463 had both DCGMS-type and ‘Black radish’- type mitochondrial structures according to multiplex PCR. Based on these results, the mechanism of rearrangement between the two mitochondrial types was studied.

Keywords

Black radish Cytoplasmic male sterility DCGMS Mitochondrial genome Orf463 

Notes

References

  1. Brown GG, Formanová N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhan J, Cheung WY, Landry BS (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J 35:262–272CrossRefGoogle Scholar
  2. Cho Y, Lee YP, Park BS, Han TH, Kim S (2012) Construction of a high-resolution linkage map of Rfd1, a restorer-of-fertility locus for cytoplasmic male sterility conferred by DCGMS cytoplasm in radish (Raphanus sativus L.) using synteny between radish and Arabidopsis genomes. Theor Appl Genet 125:467–477CrossRefGoogle Scholar
  3. Davila J, Arrieta-Montiel M, Wamboldt Y, Cao J, Hagmann J, Shedge V, Xu YZ, Weigel D, Mackenzie S (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9:64CrossRefGoogle Scholar
  4. Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V, Cattolico L, Falentin C, Giancola S, Renard M, Budar F, Small I, Caboche M, Delourme R, Bendahmane A (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 4:588–594CrossRefGoogle Scholar
  5. Fujii S, Kazama T, Yamada M, Toriyama K (2010) Discovery of global genomic re-organization based on comparison of two newly sequenced rice mitochondrial genomes with cytoplasmic male sterility-related genes. BMC Genom 11:209CrossRefGoogle Scholar
  6. Kaneko Y, Matsuzawa Y (1993) Radish. In: Kalloo G, Bergh BO (eds) Genetic improvement of vegetable crops. Pergamon Press, London, pp 487–510CrossRefGoogle Scholar
  7. Kim K, Lee YP, Lim H, Han T, Sung SK, Kim S (2010) Identification of Rfd1, a novel restorer-of-fertility locus for cytoplasmic male-sterility caused by DCGMS cytoplasm and development of simple PCR markers linked to the Rfd1 locus in radish (Raphanus sativus L.). Euphytica 175:79–90CrossRefGoogle Scholar
  8. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34:407–415CrossRefGoogle Scholar
  9. Lee YP, Park S, Lim C, Kim H, Ahn Y, Sung SK, Yoon MK, Kim S (2008) Discovery of a novel cytoplasmic male-sterility and its restorer lines in radish (Raphanus sativus L.). Theor Appl Genet 117:905–913CrossRefGoogle Scholar
  10. Lee YP, Kim S, Lim H, Ahn Y, Sung SK (2009) Identification of mitochondrial genome rearrangements unique to novel cytoplasmic male sterility in radish (Raphanus sativus L.). Theor Appl Genet 118:719–728CrossRefGoogle Scholar
  11. Lü N, Yamane K, Ohnishi O (2008) Genetic diversity of cultivated and wild radish and phylogenetic relationships among Raphanus and Brassica species revealed by the analysis of trnK/matK sequence. Breed Sci 58:15–22CrossRefGoogle Scholar
  12. Ogura H (1968) Studies on the new male-sterility in Japanese radish, with special reference to the utilization of this sterility towards the practical raising of hybrid seeds. Mem Fac Agric Kagoshima Univ 6:39–78Google Scholar
  13. Palmer JD, Herbon LA (1987) Tricircular mitochondrial genomes of Brassica and Raphanus: reversal of repeat configurations by inversion. Nucl Acids Res 14:9755–9764CrossRefGoogle Scholar
  14. Park JY, Lee YP, Lee J, Choi BS, Kim S, Yang TJ (2013) Complete mitochondrial genome sequence and identification of a candidate gene responsible for cytoplasmic male sterility in radish (Raphanus sativus L.) containing DCGMS cytoplasm. Theor Appl Genet 126:1763–1774CrossRefGoogle Scholar
  15. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012a) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001214CrossRefGoogle Scholar
  16. Sloan DB, Müller K, McCauley DE, Taylor DR, Štorchová H (2012b) Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol 196:1228–1239CrossRefGoogle Scholar
  17. Tanaka Y, Tsuda M, Yasumoto K, Yamagishi H, Terachi T (2012) A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.). BMC Genom 13:352CrossRefGoogle Scholar
  18. Yamagishi H (1998) Distribution and allelism of restorer genes for Ogura cytoplasmic male sterility in wild and cultivated radishes. Genes Genet Syst 73:79–83CrossRefGoogle Scholar
  19. Yamagishi H (2017) Speciation and diversification of radish. In: Nishio T, Kitashiba H (eds) The Radish Genome. Springer, Dordrecht, pp 11–30CrossRefGoogle Scholar
  20. Yamagishi H, Terachi T (2001) Intra- and inter-specific variations in the mitochondrial gene orf138 of Ogura-type male-sterile cytoplasm from Raphanus sativus and Raphanus raphanistrum. Theor Appl Genet 103:725–732CrossRefGoogle Scholar
  21. Yamagishi H, Terachi T (2017) Cytoplasmic male sterility and mitochondrial genome variations in radish. Nishio T, Kitashiba H(eds) The Radish Genome. Springer, Dordrecht, pp 93–108CrossRefGoogle Scholar
  22. Yasumoto K, Terachi T, Yamagishi H (2009) A novel Rf gene controlling fertility restoration of Ogura male sterility by RNA processing of orf138 found in Japanese wild radish and its STS markers. Genome 52:495–504CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • H. Yamagishi
    • 1
    Email author
  • Y. Tanaka
    • 2
  • S. Shiiba
    • 1
  • A. Hashimoto
    • 3
  • A. Fukunaga
    • 1
  • T. Terachi
    • 1
  1. 1.Faculty of Life SciencesKyoto Sangyo UniversityKyotoJapan
  2. 2.Graduate School of Environmental and Life ScienceOkayama UniversityOkayamaJapan
  3. 3.Plant Organelle Genome Research CenterKyoto Sangyo UniversityKyotoJapan

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