Abstract
The radish Rfo gene restores male fertility in radish or rapeseed plants carrying Ogura cytoplasmic male-sterility. This system was first discovered in radish and was transferred to rapeseed for the production of F1 hybrid seeds. We aimed to identify the region of the Arabidopsis genome syntenic to the Rfo locus and to characterize the radish introgression in restored rapeseed. We used two methods: amplified consensus genetic markers (ACGMs) in restored rapeseed plants and construction of a precise genetic map around the Rfo gene in a segregating radish population. The use of ACGMs made it possible to detect radish orthologs of Arabidopsis genes in the restored rapeseed genome. We identified radish genes, linked to Rfo in rapeseed and whose orthologs in Arabidopsis are carried by chromosomes 1, 4 and 5. This indicates several breaks in colinearity between radish and Arabidopsis genomes in this region. We determined the positions of markers relative to each other and to the Rfo gene, using the progeny of a rapeseed plant with unstable meiotic transmission of the radish introgression. This enabled us to produce a schematic diagram of the radish introgression in rapeseed. Markers which could be mapped both on radish and restored rapeseed indicate that at least 50 cM of the radish genome is integrated in restored rapeseed. Using markers closely linked to the Rfo gene in rapeseed and radish, we identified a contig spanning six bacterial artificial chromosome (BAC) clones on Arabidopsis chromosome 1, which is likely to carry the orthologous Rfo gene.
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Bennetzen JL (2000) Comparative sequence analysis of plant nuclear genomes: microcolinearity and its many exceptions. Plant Cell 12:1021–9
Bennetzen JL, Ramakrishna W (2002) Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48:821–7
Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 22:22
Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000) Extensive duplication and re-shuffling in the Arabidopsis genome. Plant Cell 12:1093–1101
Bonhomme S, Budar F, Férault M, Pelletier G (1991) A 2.5-kb NcoI fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr Genet 19:121–127
Bonhomme S, Budar F, Lancelin D, Small I, Defrance M-C, Pelletier G (1992) Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male-sterility in Brassica cybrids. Mol Gen Genet 235:340–348
Brunel D, Froger N, Pelletier G (1999) Development of amplified consensus genetic markers (ACGMs) in Brassica napus from Arabidopsis thaliana sequences of known biological function. Genome 42:387–402
Delourme R, Eber F (1992) Linkage between an isozyme marker and a restorer gene in radish cytoplasmic male-sterility of rapeseed (Brassica napus L.). Theor Appl Genet 85:222–228
Delourme R, Eber F, Renard M (1991) Radish cytoplasmic male-sterility in rapeseed: breeding restorer lines with a good female fertility. 8th Int Rapeseed Conf, Saskatoon, Saskatechewan, Canada, 1056
Delourme R, Bouchereau A, Hubert N, Renard M, Landry BS (1994) Identification of RAPD markers linked to a fertility restorer gene for the Ogura radish cytoplasmic male-sterility of rapeseed (Brassica napus L.). Theor Appl Genet 88:741–748
Delourme R, Eber F, Renard M (1995) Breeding double-low restorer lines in radish cytoplasmic male-sterility of rapeseed (Brassica napus L.). 9th Int Rapeseed Cong, Cambridge, UK, 6–8
Delourme R, Foisset N, Horvais R, Barret P, Champagne G, Cheung WY, Landry BS, Renard M (1998) Characterisation of the radish introgression carrying the Rfo restorer gene for the Ogu-INRA cytoplasmic male-sterility in rapeseed (Brassica napus L.). Theor Appl Genet 97:129–134
Desloire S, Gherbi H, Laloui W, Marhadour S, Clouet V, Cattolico L, Falentin C, Giancola S, Renard M, Budar F, Small S, 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
Devos KM, Beales J, Nagamura Y, Sasaki T (1999) Arabidopsis-rice: will colinearity allow gene prediction across the eudicot-monocot divide? Genome Res 9:825–829
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Fourmann M, Barret P, Renard M, Pelletier G, Delourme R, Brunel D (1998) The two genes homologous to Arabidopsis FAE-1 co-segregate with the two loci governing erucic acid content in Brassica napus. Theor Appl Genet 96:852–858
Fourmann M, Barret P, Froger N, Baron C, Chariot F, Delourme R, Brunel D (2002) From Arabidopsis thaliana to Brassica napus: development of amplified consensus genetic markers (ACGMs) for construction of a gene map. Theor Appl Genet 105:1196–1206
Fourmann M, Chariot F, Froger N, Delourme R, Brunel D (2001) Expression, mapping, and genetic variability of Brassica napus disease resistance gene analogues. Genome 44:1083–99
Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–4
Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Nat Acad Sci USA 97:4168–4173
Heyn FW (1976) Transfer of restorer genes from Raphanus to cytoplasmic male-sterile Brassica napus. Cruciferae Newslett 1:15–16
Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–51
Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Imamura J (2002) Isolation of a novel PPR protein gene, rfk1, required for fertility restoration of cytoplasmic male sterility in Kosena radish. 6th Int Congr on Plant Mitochondria, Perth, Western Australia
Kole C, Williams PH, Rimmer SR, Osborn TC (2002) Linkage mapping of genes controlling resistance to white rust (Albugo candida) in Brassica rapa (syn. campestris) and comparative mapping to Brassica napus and Arabidopsis thaliana. Genome 45:22–47
Kowalski SP, Lan T-H, Feldmann KA, Paterson AH (1994) Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics:499–510
Ku HM, Liu J, Doganlar S, Tanksley SD (2001) Exploitation of Arabidopsis-tomato synteny to construct a high-resolution map of the ovate-containing region in tomato chromosome 2. Genome 44:470–5
Ku HM, Vision T, Liu J, Tanksley SD (2000) Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc Nat Acad Sci USA 97:9121–9126
Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–28
Lagercrantz U, Lydiate DJ (1996) Comparative genome mapping in Brassica. Genetics 144:1903–10
Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine-scale genome colinearity and congruence of genes controlling flowering time. Plant J 9:13–20
Lan T-H, Delmonte TA, Reischmann KP, Kowalski S, McFerson J, Kresovich S, Paterson AH (2000) EST-enriched comparative map of Brassica oleracea and Arabidopsis thaliana. Genome Res 10:776–788
Lincoln S, Daly M, Lander E (1992) Constructing genetic linkage maps with Mapmaker/exp 3.0: a tutorial and reference manual, 3rd edn. Whitehead Institute Technical Report
Michelmore RW, Paran I, Ksseli RV (1991) Identification of marker linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832
Parkin IA, Lydiate DJ, Trick M (2002) Assessing the level of colinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 45:356–366
Paterson AH, Lan T-H, Amasino R, Osborn TC, Quiros C (2001) Brassica genomics: a complement to, and early beneficiary of, the Arabidopsis sequence. Genome Biol 2:1011.1–1011.4
Pellan-Delourme R, Renard M (1988) Cytoplasmic male-sterility in rapeseed (Brassica napus L.): female fertility of restored rapeseed with "Ogura" and cybrid cytoplasms. Genome 30:234–238
Pelletier G, Primard C, Vedel F, Chétrit P, Rémy R, Rousselle P, Renard M (1983) Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol Gen Genet 191:244–250
Pelletier G, C. P, Vedel F, Chétrit P, Renard M, Pellan-Delourme R, Mesquida J (1987) Molecular, phenotypic and genetic characterization of mitochondrial recombinants in rapeseed. 7th Int Rapeseed Conf, Poznan, Poland, pp 113–118
Robert LS, Robson F, Sharpe A, Lydiate D, Coupland G (1998) Conserved structure and function of the Arabidopsis flowering-time gene CONSTANS in Brassica napus. Plant Mol Biol 37:763–72
Rychlik W, Rhoads RE (1989) A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res 17:8543–51
Rychlik W, Spencer WJ, Rhoads RE (1990) Optimization of the annealing temperature for DNA amplification in vitro. Nucleic Acids Res 18:6409–6412
Sillito D, Parkin IA, Mayerhofer R, Lydiate DJ, Good AG (2000) Arabidopsis thaliana: a source of candidate disease-resistance genes for Brassica napus. Genome 43:452–60
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–80
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–82
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Acknowledgements
This work was supported by Génoplante, the French Consortium for Plant Genomics. We would like to thank R. Horvais for producing the radish mapping populations. We greatly appreciated support from, and stimulating discussions with, D. Brunel during experimental work and the writing of the manuscript. We would like to thank A. Bérard, M. Caffé, N. Froger and S. Perrinet for technical support, and M. Fourmann for kindly providing us with consensus primers for some target genes. We would also like to thank R. Berthomé, S. Bonhomme, M. Grelon, H. McKhann, C. Mézard and H. Mireau for critical reading of the manuscript, and I. Small for stimulating discussions. We thank P. Guerche for constant support. The work was carried out in compliance with the current laws governing research and development programs in France.
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Communicated by H. C. Becker
S. Giancola and S. Marhadour contributed equally to this work
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Giancola, S., Marhadour, S., Desloire, S. et al. Characterization of a radish introgression carrying the Ogura fertility restorer gene Rfo in rapeseed, using the Arabidopsis genome sequence and radish genetic mapping. Theor Appl Genet 107, 1442–1451 (2003). https://doi.org/10.1007/s00122-003-1381-2
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DOI: https://doi.org/10.1007/s00122-003-1381-2