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http://dx.doi.org/10.7235/hort.2015.15006

Application of the Molecular Marker in Linkage Disequilibrium with Ms, a Restorer-of-fertility Locus, for Improvement of Onion Breeding Efficiency  

Kim, Sujeong (Department of Plant Biotechnology, Biotechnology Research Institute, Chonnam National University)
Kim, Sunggil (Department of Plant Biotechnology, Biotechnology Research Institute, Chonnam National University)
Publication Information
Horticultural Science & Technology / v.33, no.4, 2015 , pp. 550-558 More about this Journal
Abstract
To analyze the linkage relationships among molecular markers recently reported to be linked to onion (Allium cepa L.) Ms, a restorer-of-fertility locus, in onion (Allium cepa L.), three single nucleotide polymorphism markers were converted into cleaved amplified polymorphic sequence (CAPS) markers based on onion transcriptome sequences and the rice genome database. Analysis of the recombinants selected from 4,273 segregating plants using CAPS and other linked markers demonstrated the jnurf13 and jnurf610 markers to perfectly co-segregate with the Ms locus. In contrast to jnurf13, the jnurf610 marker was not in perfect linkage disequilibrium with the Ms locus in diverse breeding lines. Thus, the jnurf13 marker and the marker for identification of cytoplasm types were utilized to enhance the efficiency of onion breeding through four applications. First, 89 maintainer lines containing the normal cytoplasm and homozygous recessive Ms genotypes were successfully identified from 100 breeding lines. Second, these two molecular markers were used to analyze the main sources of male-fertile contaminants frequently found in the male-sterile parental lines during F1 hybrid seed production. The majority of the contaminants contained heterozygous Ms genotypes, indicating that pollen grains harboring the dominant Ms genotype may have been introduced during propagation of the maintainer lines. Therefore, the genetic purity of the two maintainer lines was analyzed in the third application, and the results showed that both maintainer lines contained 13-21% off-types. Finally, the two markers were used to increase the seed yield potentials of two open-pollinated varieties containing sterile cytoplasms by removing the plants harboring homozygous recessive and heterozygous Ms genotypes.
Keywords
Allium cepa; cleaved amplified polymorphic sequence marker; cytoplasmic male-sterility; maintainer; marker-assisted selection; single nucleotide polymorphism;
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1 Brown, G.G., N. Formanova, H. Jin, R. Wargachuk, C. Dendy, P. Patil, M. Laforest, J. Zhang, W.Y. Cheung, and B.S. Landry. 2003. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35:262-272.   DOI
2 Budar, F., P. Touzet, and R. De Paepe. 2003. The nucleomitochondrial conflict in cytoplasmic male sterilities revised. Genetica 117:3-16.   DOI
3 Cho, Y., Y. Lee, B. Park, T. Han, and S. Kim. 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.). Theor. Appl. Genet. 125:467-477.   DOI
4 Cui, X., R.P. Wise, and P.S. Schnable. 1996. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334-1336.   DOI
5 Desloire, S., H. Gherbi, W. Laloui, S. Marhadour, V. Clouet, L. Cattolico, C. Falentin, S. Giancola, M. Renard, F. Budar, I. Small, M. Caboche, R. Delourme, and A. Bendahmane. 2003. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 4:588-594.   DOI
6 Doyle, J.J. and J.L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15.
7 Duangjit, J., B. Bohanec, A.P. Chan, C.D. Town, and M.J. Havey. 2013. Transcriptome sequencing to produce SNP-based genetic maps of onion. Theor. Appl. Genet. 126:3093-2101.
8 Engelke, T., D. Terefe, and T. Tatlioglu. 2003. A PCR-based marker system monitoring CMS-(S), CMS-(T) and (N)-cytoplasm in the onion (Allium cepa L.). Theor. Appl. Genet. 107:162-167.
9 Kim, S., E. Lee, C. Kim, and M. Yoon. 2009b. Distribution of three cytoplasm types in onion (Allium cepa L.) cultivars bred in Korea and Japan. Kor. J. Hort. Sci. Technol. 27:275-279.
10 Klein, R.R., P.E. Klein, J.E. Mullet, P. Minx, W.L. Rooney, and K.F. Schertz. 2005. Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the collinear region of rice chromosome 12. Theor. Appl. Genet. 111:994-1012.   DOI
11 Kmiec, B., M. Woloszynska, and H. Janska. 2006. Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr. Genet. 50:149-159.   DOI
12 Knoop, V. 2004. The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr. Genet. 46:123-139.
13 Koizuka, N., R. Imai, H. Fujimoto, T. Hayakawa, Y. Kimura, J. Kohno-Murase, T. Sakai, S. Kawasaki, and J. Imamura. 2003. Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 34:407-415.   DOI
14 Komori, T., S. Ohta, N. Murai, Y. Takakura, Y. Kuraya, S. Suzuki, Y. Hiei, H. Imaseki, and N. Nitta. 2004. Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J. 37:315-325.   DOI
15 Kubo, T. and K.J. Newton. 2008. Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5-14.   DOI
16 Laser, K.D. and N.R. Lersten. 1972. Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot. Rev. 38:425-454.   DOI
17 Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Window 95/98/NT. Nucl. Acids Symp. Ser. 41:95-98.
18 Fossen, T., O.M. Andersen, D.O. Ovstedal, A.T. Pedersen, and A. Raknes. 1996. Characteristic anthocyanin pattern from onions and other Allium spp. J. Food Sci. 61:703-706.   DOI
19 Gokce, A.F. and M.J. Havey. 2002. Linkage equilibrium among tightly linked RFLPs and the Ms locus in open-pollinated onion populations. J. Am. Soc. Hortic. Sci. 127:944-946.
20 Griffiths, G., L. Trueman, T. Crowther, B. Thomas, and B. Smith. 2002. Onions-A global benefit to health. Phytother. Res. 16:603-615.   DOI
21 Hamilton, J.P. and C.R. Buell. 2012. Advances in plant genome sequencing. Plant J. 70:177-190.   DOI
22 Hanson, M.R. 1991. Plant mitochondrial mutations and male sterility. Annu. Rev. Genet. 25:461-486.   DOI
23 Hanson, M.R. and S. Bentolila. 2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154-S169.   DOI
24 Havey, M.J. 1995. Identification of cytoplasms using the polymerase chain reaction to aid in the extraction of maintainer lines from open-pollinated populations of onion. Theor. Appl. Genet. 90:263-268.
25 Havey, M.J. 2013. Single nucleotide polymorphisms in linkage disequilibrium with the male-sterility restoration (Ms) locus in open-pollinated and inbred populations of onion. J. Am. Soc. Hortic. Sci. 138:306-309.
26 Hu, J., W. Huang, Q. Huang, X. Qin, C. Yu, L. Wang, S. Li, R. Zhu, and Y. Zhu. 2014. Mitochondria and cytoplasmic male sterility in plants. Mitochondrion 19:166-171.   DOI
27 Rhodes, M.J.C. and K.R. Price. 1996. Analytical problems in the study of flavonoid compounds in onions. Food Chem. 57:113-117.   DOI
28 Martin, W.J., J. McCallum, M. Shigyo, J. Jakse, J.C. Kuhl, N. Yamane, M. Pither-Joyce, A.F. Gokce, K.C. Sink, C.D. Town, and M.J. Havey. 2005. Genetic mapping of expressed sequences in onion and in silico comparisons with rice show scant colinearity. Mol. Gen. Genomics 274:197-204.   DOI
29 Mutz, K., A. Heilkenbrinker, M. Lonne, J. Walter, and F. Stahl. 2013. Transcriptome analysis using next-generation sequencing. Curr. Opin. Biotech. 24:22-30.   DOI
30 Park, J., H. Bang, D.Y. Cho, M. Yoon, B.S. Patil, and S. Kim. 2013. Construction of high-resolution linkage map of the Ms locus, a restorer-of-fertility gene in onion (Allium cepa L.). Euphytica 192:267-278.   DOI
31 Sato, Y. 1998. PCR amplification of CMS-specific mitochondrial nucleotide sequences to identify cytoplasmic genotypes of onion (Allium cepa L.). Theor. Appl. Genet. 96:367-370.   DOI
32 Schweisguth, B. 1973. etude d'un nouveau type de sterilite male chez l'oignon, Allium cepa L. Ann. Amelior. Plant 23:221-233.
33 Slimestad, R., T. Fossen, and I.M. Vagen. 2007. Onions: a source of unique dietary flavonoids. J. Agric. Food Chem. 55:10067-10080.   DOI
34 Small, I., R. Suffolk, and C.J. Leaver. 1989. Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69-76.   DOI
35 Vitte, C., M.C. Estep, J. Leebens-Mack, and J.L. Bennetzen. 2013. Young, intact and nested retrotransposons are abundant in the onion and asparagus genomes. Ann. Bot. 112:881-889.   DOI
36 Berninger, E. 1965. Contribution a l'etude de la sterilite male de l'oignon (Allium cepa L.). Ann Amelior. Plant 15:183-199.
37 Wolf, J.B.W. 2013. Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol. Ecol. Resour. 13:559-572.   DOI
38 Arumuganathan, K. and E.D. Earle. 1991. Nuclear DNA content of some important plant species. Plant Mol. Rep. 9:208-218.   DOI
39 Bang, H., S. Kim, S.O. Park, K. Yoo, and B.S. Patil. 2013. Development of a codominant CAPS marker linked to the Ms locus controlling fertility restoration in onion (Allium cepa L.). Sci. Hortic. 153:42-49.   DOI
40 Bentolila, S., A.A. Alfonso, and M.R. Hanson. 2002. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99:10887-10892.   DOI
41 Brewster, J.L. 2008. Onions and other vegetable alliums, 2nd edn. CAB International: Wallingford, UK.
42 Jones, H.A. and S.L. Emsweller. 1936. A male-sterile onion. Proc. Am. Soc. Hortic. Sci. 34:582-585.
43 Jakse, J., J.D.F. Meyer, G. Suzuki, J. McCallum, F. Cheung, C.D. Town, and M.J. Havey. 2008. Pilot sequencing of onion genomic DNA reveals fragments of transposable elements, low gene densities, and significant gene enrichment after methyl filtration. Mol. Genet. Genomics 280:287-292.   DOI
44 Jakse, J., A. Telgmann, C. Jung, A. Khar, S. Melgar, F. Cheung, C.D. Town, and M.J. Havey. 2006. Comparative sequence and genetic analyses of asparagus BACs reveal no microsynteny with onion or rice. Theor. Appl. Genet. 114:31-39.   DOI
45 Jones, H.A. and A. Clarke. 1943. Inheritance of male sterility in the onion and the production of hybrid seed. Proc. Am. Soc. Hortic. Sci. 43:189-194.
46 Kawahara, Y., M. de la Bastide, J.P. Hamilton, H. Kanamori, W.R. McCombie, S. Ouyang, D.C. Schwartz, T. Tanaka, J. Wu, S. Zhou, K.L. Childs, R.M. Davidson, H. Lin, L. Quesada-Ocampo, B. Vaillancourt, H. Sakai, S.S. Lee, J. Kim, H. Numa, T. Itoh, C.R. Buell, and T. Matsumoto T. 2013. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4.   DOI   ScienceOn
47 Kim, S. 2014. A codominant molecular marker in linkage disequilibrium with a restorer-of-fertility gene (Ms) and its application in reevaluation of inheritance of fertility restoration in onions. Mol. Breed. 34:769-778.   DOI
48 Kim, S., E. Lee, D.Y. Cho, T. Han, H. Bang, B.S. Patil, Y.K. Ahn, and M. Yoon. 2009a. Identification of a novel chimeric gene, orf725, and its use in development of a molecular marker for distinguishing three cytoplasm types in onion (Allium cepa L.). Theor. Appl. Genet. 118:433-441.   DOI