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Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the colinear region of rice chromosome 12

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An Erratum to this article was published on 29 November 2005

An Erratum to this article was published on 29 November 2005

Abstract

With an aim to clone the sorghum fertility restorer gene Rf1, a high-resolution genetic and physical map of the locus was constructed. The Rf1 locus was resolved to a 32-kb region spanning four open reading frames: a plasma membrane Ca2+-ATPase, a cyclin D-1, an unknown protein, and a pentatricopeptide repeat (PPR13) gene family member. An ~19-kb region spanning the cyclin D-1 and unknown protein genes was completely conserved between sterile and fertile plants as was the sequence spanning the coding region of the Ca2+-ATPase. In contrast, 19 sequence polymorphisms were located in an ~7-kb region spanning PPR13, and all markers cosegregated with the fertility restoration phenotype. PPR13 was predicted to encode a mitochondrial-targeted protein containing a single exon with 14 PPR repeats, and the protein is classified as an E-type PPR subfamily member. To permit sequence-based comparison of the sorghum and rice genomes in the Rf1 region, 0.53 Mb of sorghum chromosome 8 was sequenced and compared to the colinear region of rice chromosome 12. Genome comparison revealed a mosaic pattern of colinearity with an ~275-kb gene-poor region with little gene conservation and an adjacent, ~245-kb gene-rice region that is more highly conserved between rice and sorghum. Despite being located in a region of high gene conservation, sorghum PPR13 was not located in a colinear position on rice chromosome 12. The present results suggest that sorghum PPR13 represents a potential candidate for the sorghum Rf1 gene, and its presence in the sorghum genome indicates a single gene transposition event subsequent to the divergence of rice and sorghum ancestors.

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References

  • Allen E, Xie Z, Gustafson AM, Sung G-H, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nature Genet 36:1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2000) Comparative sequence analysis of plant nuclear genomes: microcolinearity and its many exceptions. Plant Cell 12:1021–1029

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL (2002) Opening the door to comparative plant biology. Science 296:60–63

    Article  PubMed  Google Scholar 

  • Bennetzen JL, Ma J (2003) The genetic colinearity of rice and other cereals on the basis of genomic sequence analysis. Curr Opin Plant Biol 6:128–133

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL, Ramakrishna W (2002) Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48:821–827

    Article  PubMed  CAS  Google Scholar 

  • Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892

    Article  PubMed  ADS  CAS  Google Scholar 

  • Bonhomme S, Budar F, Lancelin D, Small I, Defrance MC, Pelletier G (1992) Sequence and transcript analysis of the Nco2. Mol Gen Genet 235:340–348

    Article  PubMed  CAS  Google Scholar 

  • Bowers JE, Abbey C, Anderson S, Chang C, Draye X, Hoppe AH, Jessup R, Lemke C, Lennington J, Li ZK, Lin YR, Liu SC, Luo LJ, Marler BS, Ming R, Mitchell SE, Qiang D, Reischmann K, Schulze SR, Skinner DN, Wang YW, Kresovich S, Schertz KF, Paterson AH (2003a) A high-density genetic recombination map of sequence-tagged sites for Sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics 165:367–386

    PubMed  CAS  Google Scholar 

  • Bowers JE, Chapman BA, Rong JK, Paterson AH (2003b) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    Article  PubMed  ADS  CAS  Google Scholar 

  • Brown GG (1999) Unique aspects of cytoplasmic male sterility and fertility restoration in Brassica napus. J Hered 90:351–356

    Article  CAS  Google Scholar 

  • Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, Patil P, Laforest M, Zhang JF, 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

    Article  PubMed  CAS  Google Scholar 

  • Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333

    Article  PubMed  ADS  CAS  Google Scholar 

  • Chen M, SanMiguel P, Bennetzen JL (1998) Sequence organization and conservation in sh2/a1-homologous regions of sorghum and rice. Genetics 148:435–443

    PubMed  CAS  Google Scholar 

  • Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336

    PubMed  ADS  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Draye X, Lin YR, Qian XY, Bowers JE, Burow GB, Morrell PL, Peterson DG, Presting GG, Ren SX, Wing RA, Paterson AH (2001) Toward integration of comparative genetic, physical, diversity, and cytomolecular maps for grasses and grains, using the sorghum genome as a foundation. Plant Physiol 125:1325–1341

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: a graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G (1998) Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 26:865–878

    Article  PubMed  CAS  Google Scholar 

  • Han F, Kilian A, Chen JP, Kudrna D, Steffenson B, Yamamoto K, Matsumoto T, Sasaki T, Kleinhofs A (1999) Sequence analysis of a rice BAC covering the syntenous barley Rpg1 region. Genome 42:1071–1076

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16(Suppl):S154–S169

    Article  PubMed  CAS  Google Scholar 

  • Hardison RC (2000) Conserved noncoding sequences are reliable guides to regulatory elements. Trends Genet 16:369–372

    Article  PubMed  CAS  Google Scholar 

  • Ilic K, SanMiguel PJ, Bennetzen JL (2003) A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. Proc Natl Acad Sci USA 100:12265–12270

    Article  PubMed  ADS  CAS  Google Scholar 

  • Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12:1437–1446

    PubMed  CAS  Google Scholar 

  • Kaplinsky NJ, Braun DM, Penterman J, Goff SA, Freeling M (2002) Utility and distribution of conserved noncoding sequences in the grasses. Proc Natl Acad Sci USA 99:6147–6151

    Article  PubMed  ADS  CAS  Google Scholar 

  • Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544:99–102

    Article  PubMed  CAS  Google Scholar 

  • Kilian A, Chen J, Han F, Steffenson B, Kleinhofs A (1997) Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol 35:187–195

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Klein PE, Klein RE, Price HJ, Mullet JE, Stelly DM (2005a) Chromosome identification and nomenclature of Sorghum bicolor. Genetics 169:1169–1173

    Google Scholar 

  • Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005b) Molecular cytogenetic maps of sorghum linkage groups 2 and 8. Genetics 169:955–965

    Google Scholar 

  • Klein PE, Klein RR, Cartinhour SW, Ulanch PE, Dong J, Obert JA, Morishige DT, Schlueter SD, Childs KL, Ale M, Mullet JE (2000) A high-throughput AFLP-based method for constructing integrated genetic and physical maps: progress toward a sorghum genome map. Genome Res 10:789–807

    Article  PubMed  CAS  Google Scholar 

  • Klein RR, Klein PE, Chhabra AK, Dong J, Pammi S, Childs KL, Mullet JE, Rooney WL, Schertz KF (2001) Molecular mapping of the rf1 gene for pollen fertility restoration in sorghum (Sorghum bicolor L.). Theor Appl Genet 102:1206–1212

    Article  CAS  Google Scholar 

  • Klein PE, Klein RR, Vrebalov J, Mullet JE (2003) Sequence-based alignment of sorghum chromosome 3 and rice chromosome 1 reveals extensive conservation of gene order and one major chromosomal rearrangement. Plant J 34:605–621

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38:425–454

    Article  Google Scholar 

  • Li W, Gill BS (2002) The colinearity of the Sh2/A1 orthologous region in rice, sorghum and maize is interrupted and accompanied by genome expansion in the Triticeae. Genetics 160:1153–1162

    PubMed  CAS  Google Scholar 

  • Liu F, Cui X, Horner HT, Weiner H, Schnable PS (2001) Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13:1063–1078

    Article  PubMed  CAS  Google Scholar 

  • Luo MC, Thomas C, You FM, Hsiao J, Ouyang S, Buell CR, Malandro M, McGuire PE, Anderson OD, Dvorak J (2003) High-throughput fingerprinting of bacterial artificial chromosomes using the SNaPshot labeling kit and sizing of restriction fragments by capillary electrophoresis. Genomics 82:378–389

    Article  PubMed  CAS  Google Scholar 

  • 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-Magniette ML, Mireau H, Peeters N, Renou JP, 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

    Article  PubMed  CAS  Google Scholar 

  • Meierhoff K, Felder S, Nakamura T, Bechtold N, Schuster G (2003) HCF152, an Arabidopsis RNA binding pentatricopeptide repeat protein involved in the processing of chloroplast psbB-it psbT-it psbH-it petB-it petD RNAs. Plant Cell 15:1480–1495

    Article  PubMed  CAS  Google Scholar 

  • Menz MA, Klein RR, Mullet JE, Obert JA, Unruh NC, Klein PE (2002) A high-density genetic map of Sorghum bicolor (L.) Moench based on 2926 AFLP, RFLP and SSR markers. Plant Mol Biol 48:483–499

    Article  PubMed  CAS  Google Scholar 

  • Mullet JE, Klein RR, Klein PE (2001) Sorghum bicolor—an important species for comparative grass genomics and a source of beneficial genes for agriculture. Curr Opin Plant Biol 5:118–121

    Article  Google Scholar 

  • Nakamura T, Meierhoff K, Westhoff P, Schuster G (2003) RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur J Biochem 270:4070–4081

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004a) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908

    Article  PubMed  ADS  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA, Peterson DG, Rong JK, Wicker TM (2004b) Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity. Curr Opin Biotechnol 15:120–125

    Article  PubMed  CAS  Google Scholar 

  • Pring DR, Van TH, Schertz KF (1995) Cytoplasmic male sterility and organelle DNAs of sorghum. In: Levings CS III, Vasil IK (eds) Advances in cellular and molecular biology of plants. Kluwer Academic, Dordrecht, pp 461–495

    Google Scholar 

  • Ramakrishna W, Dubcovsky J, Park YJ, Busso C, Emberton J, SanMiguel P, Bennetzen JL (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400

    PubMed  CAS  Google Scholar 

  • Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K (2002) RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102

    Article  PubMed  CAS  Google Scholar 

  • Schwartz S, Zhang Z, Frazer KA, Smit A, Riemer C, Bouck J, Gibbs R, Hardison R, Miller W (2000) PipMaker—a web server for aligning two genomic DNA sequences. Genome Res 10:577–586

    Article  PubMed  CAS  Google Scholar 

  • Small ID, Peeters N (2000) The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47

    Article  PubMed  CAS  Google Scholar 

  • Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genomes. Genome Res 12:1549–1555

    Article  PubMed  CAS  Google Scholar 

  • Tang HV, Pring DR, Shaw LC, Salazar RA, Muza FR, Yan B, Schertz KF (1996) Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J 10:123–133

    Article  PubMed  CAS  Google Scholar 

  • Tang HV, Chen W, Pring DR (1999) Mitochondrial orf107 transcription, editing, and nucleolytic cleavage conferred by the gene Rf3 are expressed in sorghum pollen. Sex Plant Reprod 12:53–59

    Article  CAS  Google Scholar 

  • Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein NM, Bennetzen JL, Avramova Z (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414

    Article  PubMed  ADS  CAS  Google Scholar 

  • Tsuchiya N, Fukuda H, Nakashima K, Nagao M, Sugimura T, Nakagama H (2004) LRP130, a single-stranded DNA/RNA-binding protein, localizes at the outer nuclear and endoplasmic reticulum membrane, and interacts with mRNA in vivo. Biochem Biophys Res Commun 317:736–743

    Article  PubMed  CAS  Google Scholar 

  • Tu Z (2001) Eight novel families of miniature inverted repeat transposable elements in the African malaria mosquito, Anopheles gambiae. Proc Natl Acad Sci USA 98:1699–1704

    Article  PubMed  ADS  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Ms. Julie McCollum (USDA–ARS) and Tracie Miner (Washington University) for expert technical assistance. Special thanks to Professor Ian Small (Unité de Recherches en Gènomique Végétale INRA CNRS, Evry, France) for critical guidance and thoughtful insight concerning PPR genes. The research is supported by the United States Department of Agriculture’s Agricultural Research Service (R.R.K.). This work was also supported in part by National Science Foundation Plant Genome Grant DBI-0077713 (J.E.M. and P.E.K) and DBI-0321578 (P.E.K., R.R.K. and J.E.M.).

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Correspondence to R. R. Klein.

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Communicated by E. Guiderdoni

An erratum to this article can be found at http://dx.doi.org/10.1007/s00122-005-0134-9

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Klein, R.R., Klein, P.E., Mullet, J.E. et al. Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the colinear region of rice chromosome 12. Theor Appl Genet 111, 994–1012 (2005). https://doi.org/10.1007/s00122-005-2011-y

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