Development of simple PCR-based markers linked to the Ms locus, a restorer-of-fertility gene in onion (Allium cepa L.)

Euphytica

Volumn 179, Issue 3, 2011, Pages 439-449

  Bang, Haejeen ^a   Cho, Dong Youn ^b   Yoo, Kil Sun ^a   Yoon, Moo Kyoung ^c   Patil, Bhimanagouda S ^a   Kim, Sunggil ^d  

^a TEXAS A AND M UNIVERSITY   (United States)

^b ONBREETECH Corp   (South Korea)

^c Rural Development Administration   (South Korea)

^d Chonnam National University   (South Korea)

Author keywords

Cytoplasmic male sterility; Marker assisted selection; Molecular markers; Onion (Allium cepa L.); Restorer of fertility genes

Indexed keywords

ALLIUM CEPA;

EID: 79955683754     PISSN: 00142336     EISSN: 15735060     Source Type: Journal    
DOI: 10.1007/s10681-010-0342-5     Document Type: Article

References (66)

1. Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci 100: 5968-5973.
2. Abdelnoor RV, Christensen AC, Mohammed S, Munoz-Castillo B, Moriyama H, Mackenzie SA (2006) Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue. J Mol Evol 63: 165-173.
3. Albert B, Godelle B, Gouyon PH (1998) Evolution of the plant mitochondrial genome: dynamics of duplication and deletion of sequences. J Mol Evol 46: 155-158.
4. Andersen JR, Lübberstedt T (2003) Functional markers in plants. Trends Plant Sci 8: 554-560.
5. Arrieta-Montiel M, Lyznik A, Woloszynska M, Janska H, Tohme J, Mackenzie S (2001) Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics 158: 851-864.
6. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580.
7. Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci 99: 10887-10892.
8. Berninger E (1965) Contribution à l'étude de la sterilité mâle de l'oignon (Allium cepa L.). Ann Amélior Plant 15: 183-199.
9. Bilgen M, Karaca M, Onus AN, Ince AG (2004) A software program combining sequence motif searches with keywords for finding repeats containing DNA sequences. Bioinformatics 20: 3379-3386.
10. Bois PRJ (2003) Hypermutable minisatellites, a human affair? Genomics 81: 349-355.
11. Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang 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: 262-272.
12. Budar F, Touzet P, De Paepe R (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revised. Genetica 117: 3-16.
13. Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, Gouzy J, Wang X, Mudge J, Vasdewani J, Schiex T, Spannagl M, Monaghan E, Nicholson C, Humphray SJ, Schoof H, Mayer KFX, Rogers J, Quétierk F, Oldroyd GE, Debellé F, Cook DR, Retzel EF, Roe BA, Town CD, Tabata S, van de Peer Y, Young ND (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicas genomes. Proc Natl Acad Sci 103: 14959-14964.
14. Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272: 1334-1336.
15. de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CarthaGene: multipopulation intergrated genetic and radiated hybrid mapping. Bioinformatics 21: 1703-1704.
16. 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: 588-594.
17. Engelke T, Terefe D, Tatlioglu T (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.
18. Fauron CMR, Havlik M, Brettell RIS (1990) The mitochondrial genome organization of a maize fertile cmsT revertant line is generated through recombination between two sets of repeats. Genetics 124: 423-428.
19. Fuji S, Toriyama K (2009) Suppressed expression of RETROGRADE-REGULATED MALE STERILITY restores pollen fertility in cytoplasmic male sterile rice plants. Proc Natl Acad Sci 106: 9513-9518.
20. Gillman JD, Bentolila S, Hanson MR (2007) The petunia restorer of fertility protein is part of a large mitochondrial complex that interacts with transcripts of the CMS-associated locus. Plant J 49: 217-227.
21. Gökçe AF, Havey MJ (2002) Linkage equilibrium among tightly linked RFLPs and the Ms locus in open-pollinated onion populations. J Am Soc Hort Sci 127: 944-946.
22. Gökçe AF, McCallum J, Sato Y, Havey MJ (2002) Molecular tagging of the Ms locus in onion. J Am Soc Hort Sci 127: 576-582.
23. Gothandam KM, Kim E, Cho H, Chung Y (2005) OsPPR1, a pentatricopeptide repeat protein of rice is essential for the chloroplast biogenesis. Plant Mol Biol 58: 421-433.
24. Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25: 461-486.
25. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16: S154-S169.
26. Havey MJ (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.
27. Havey MJ (2000) Diversity among male-sterility-inducing and male-fertile cytoplasms of onion. Theor Appl Genet 101: 778-782.
28. Hawkins JS, Grover CE, Wendel JF (2008) Repeated big bangs and the expanding universe: directionality in plant genome size evolution. Plant Sci 174: 557-562.
29. 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.
30. Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10: 1163-1180.
31. Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable 'minisatellite' regions in human DNA. Nature 314: 67-73.
32. Jones HA, Clarke A (1943) Inheritance of male sterility in the onion and the production of hybrid seed. Proc Am Soc Hort Sci 43: 189-194.
33. Jones HA, Emsweller SL (1936) A male-sterile onion. Proc Am Soc Hort Sci 34: 582-585.
34. Kanazawa A, Tsutsumi N, Hirai A (1994) Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138: 865-870.
35. Kazama T, Nakamura T, Watanabe M, Sugita M, Toriyama K (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J 55: 619-628.
36. Kim S, Yoon M (2010) Comparison of mitochondrial and chloroplast genome segments from three onion (Allium cepa L.) cytoplasm types and identification of trans-splicing intron of cox2. Curr Genet, in press, doi: 10. 1007/s00294-010-0290-6.
37. Kim S, Binzel ML, Yoo KS, Park S, Pike LM (2004) Pink (P), a new locus responsible for a pink trait in onions (Allium cepa) resulting from natural mutations of anthocyanidin synthase. Mol Genet Genomics 272: 1827.
38. Kim S, Lee E, Cho DY, Han T, Bang H, Patil BS, Ahn YK, Yoon M (2009) 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.
39. Klein RR, Klein PE, Mullet JE, Minx P, Rooney WL, Schertz KF (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.
40. Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46: 123-139.
41. 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: 407-415.
42. Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37: 315-325.
43. Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12: 172-175.
44. Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniete M, Mireau H, Peeters N, Renou J, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
45. Mackenzie SA, Chase CD (1990) Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2: 905-912.
46. Martin WJ, McCallum J, Shigyo M, Jakse J, Kuhl JC, Yamane N, Pither-Joyce M, Gokce AF, Sink KC, Town CD, Havey MJ (2005) Genetic mapping of expressed sequences in onion and in silico comparisons with rice show scant colinearity. Mol Gen Genomics 274: 197-204.
47. Murray MG, Thompson WF (1980) Rapid isolation of high-molecular-weight plant DNA. Nucleic Acids Res 8: 4321-4326.
48. Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BCY, Septiningsih EM, Vergara G, Sanchez D, Xu K, Ismail AM, Mackill DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115: 767-776.
49. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomènech P, Pitrat M, Caboche M, Dogimont C, Garcia-Mas J, Aranda MA, Bendahmane A (2006) An elF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J 48: 452-462.
50. Palmer JD (1988) Intraspecific variation and multicircularity in Brassica mitochondrial DNAs. Genetics 118: 341-351.
51. Palmer JD, Herbon LA (1987) Unicircular structure of the Brassica hirta mitochondrial genome. Curr Genet 11: 565-570.
52. Ramu P, Kassahun B, Senthilvel S, Kumar CA, Jayashree B, Folkertsma RT, Reddy LA, Kuruvinashetti MS, Haussmann BIG, Hash CT (2009) Exploiting rice-sorghum synteny for targeted development of EST-SSRs to enrich the sorghum genetic linkage map. Theor Appl Genet 119: 1193-1204.
53. Sandhu AS, Abdelnoor RV, Mackenzie SA (2007) Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants. Proc Natl Acad Sci 104: 1766-1770.
54. 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.
55. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13: 663-670.
56. Schweisguth B (1973) Étude d'un nouveau type de stérilité male chez l'oignon, Allium cepa L. Ann Amélior Plant 23: 221-233.
57. Sharopova N (2008) Plant simple sequence repeats: distribution, variation, and effects on gene expression. Genome 51: 79-90.
58. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19: 1251-1264.
59. Small ID, Peeters N (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25: 45-47.
60. Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58: 69-76.
61. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.
62. Vergnaud G, Denoeud F (2000) Minisatellites: mutability and genome architecture. Genome Res 10: 899-907.
63. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu Y (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18: 676-687.
64. Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25: 793-803.
65. Zaegel V, Guermann B, Le Ret M, Andrés C, Meyer D, Erhardt M, Canaday J, Gualberto JM, Imbault P (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18: 3548-3563.
66. Zakrzewski F, Wenke T, Holtgraewe D, Weisshaar B, Schmidt T (2010) Analysis of a c0t-1 library enables the targeted identification of minisatellites and satellite families in Beta vulgaris. BMC Plant Biol 10: 8. doi: 10. 1186/1471-2229-10-8.