Skip to main content
SpringerLink
Log in

The rice R gene family: two distinct subfamilies containing several miniature inverted-repeat transposable elements

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The R and B genes of maize regulate the anthocyanin biosynthetic pathway and constitute a small gene family whose evolution has been shaped by polyploidization and transposable element activity. To compare the evolution of regulatory genes in the distinct but related genomes of rice and maize, we previously isolated two R homologues from rice (Oryza sativa). The Ra1 gene on chromosome 4 can activate the anthocyanin pathway, whereas the Rb gene, of undetermined function, maps to chromosome 1. In this study, rice R genes have been further characterized. First, we found that an Rb cDNA can induce pigmentation in maize suspension cells. Second, another rice R homologue (Ra2) was identified that is more closely related to Ra1 than to Rb. Domesticated rice and its wild relatives harbor multiple Ra-like and Rb-like genes despite the fact that rice is a true diploid with the smallest genome of all the grass species analyzed to date. Finally, several miniature inverted-repeat transposable elements (MITEs) were found in R family members. Their possible role in hastening the divergence of R genes is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahn, S. and Tanksley, S.D. 1993. Comparative linkage maps of the rice and maize genomes. Proc. Natl. Acad. Sci. USA 90: 7980–7984.

    Google Scholar 

  • Anderson, E. 1945. What is Zea mays? A report of progress. Chron. Bot. 9: 88–92.

    Google Scholar 

  • Arumuganathan, K. and Earle, E.D. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208–218.

    Google Scholar 

  • Bilang, R., Zhang, S., Leduc, N., Iglesias, V.A., Gisel, A., Simmonds, J., Potrykus, I. and Sautter, C. 1993. Transient gene expression in vegetative shoot apical meristems of wheat after biolistic microtargeting. Plant J. 4: 735–744.

    Google Scholar 

  • Bureau, T.E. and Wessler, S.R. 1994. Stowaway: a family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell 6: 907–916.

    Google Scholar 

  • Bureau, T.E., Ronald, P.C. and Wessler, S.R. 1996. A computerbased systematic survey reveals the predominance of small inverted-repeat elements in wild-type rice genes. Proc. Natl. Acad. Sci. USA 93: 8524–8529.

    Google Scholar 

  • Casas, A.M., Kononowicz, A.K., Zehr, U.B., Tomes, D.T., Axtell, J.D., Butler, L.G., Bressan, R.A. and Hasegawa, P.M. 1993. Transgenic sorghum plants via microprojectile bombardment. Proc. Natl. Acad. Sci. USA 90: 11212–11216.

    Google Scholar 

  • Chandler, V.L., Radicella, J.P., Robbins, T.P., Chen, J. and Turks, D. 1989. Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell 1: 1175–1183.

    Google Scholar 

  • Chen, M. and Bennetzen, J.L. 1996. Sequence composition and organization in the Sh2/A1-homologous regions or rice. Plant Mol. Biol. 32: 999–1001.

    Google Scholar 

  • Chen, M., SanMiguel, P., de Oliveira, A.C., Woo, S.S., Zhang, H., Wing, R.A. and Bennetzen, J.L. 1997. Microcollinearity in sh2-homologous regions of the maize, rice and sorghum genomes. Proc. Natl. Acad. Sci. USA 94: 3431–3455.

    Google Scholar 

  • Damiani, R.D. Jr. and Wessler, S.R. 1993. An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proc. Natl. Acad. Sci. USA 90: 8244–8248.

    Google Scholar 

  • Dellaporta, S.L., Greenblatt, I., Kermicle, J.L., Hicks, J.B. and Wessler, S.R. 1988. Molecular cloning of the maize R-nj allele by transposon tagging with Ac. In: J.P. Gustafson and R. Apples (Eds.), Chromosome Structure and Function: Impact of New Concepts, 18th Stadler Genetics Symposium, Plenum Press, New York, pp. 263–282.

    Google Scholar 

  • Dickinson, W.J., 1991. The evolution of regulatory genes and patterns in Drosophila. In: M. Hecht, B. Wallace and R. MacIntyre (Eds.), Evolutionary Biology, vol 25, Plenum Press, New York, pp. 127–173.

    Google Scholar 

  • Dooner, H.K. and Robbins, T.P. 1991. Genetic and developmental control of anthocyanin biosynthesis. Annu. Rev. Genet. 25: 173–199.

    Google Scholar 

  • Flavell, R.B. 1994. Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc. Natl. Acad. Sci. USA 91: 3490–3496.

    Google Scholar 

  • Galway, M.E., Masucci, J.D., Lloyd, A.M., Walbot, V., Davis, R.W. and Schiefelbein, J.W. 1994. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev. Biol. 166: 740–754.

    Google Scholar 

  • Goff, S.A., Klein, T.M., Roth, B.A., Fromm, M.E., Cone, K.C., Radicella, J.P. and Chandler, V.L. 1990. Transactivation of anthocyanin biosynthetic genes following transfer of B regulatory genes into maize tissues. EMBO J. 9: 2517–2522.

    Google Scholar 

  • Goodrich, J., Carpenter, R. and Coen, E.S. 1992. A common gene regulates pigmentation pattern in diverse plant species. Cell 98: 955–964.

    Google Scholar 

  • Helentjaris, T., Weber, D. and Wright, S. 1988. Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. Genetics 118: 353–363.

    Google Scholar 

  • Hu, J., Anderson, B. and Wessler, S.R. 1996. Isolation and characterization of rice R genes: evidence for distinct evolutionary paths in rice and maize. Genetics 142: 1021–1031.

    Google Scholar 

  • Klein, T.M., Roth, B.A. and Fromm, M.E. 1989. Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc. Natl. Acad. Sci. USA 86: 6681–6685.

    Google Scholar 

  • Lloyd, A.M., Walbot, V. and Davis, R.W. 1992. Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science 258: 1773–1775.

    Google Scholar 

  • Ludwig, S.R. and Wessler, S.R. 1990. Maize R gene family: tissue specific helix-loop-helix proteins. Cell 62: 849–851.

    Google Scholar 

  • Ludwig, S.R., Habera, L.F., Dellaporta, S.L. and Wessler, S.R. 1989. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc. Natl. Acad. Sci. USA 86: 7092–7096.

    Google Scholar 

  • Oka, H.I. 1988. The genus Oryza. In: Origin of Cultivated Rice, Japanese Science Society Press/Elsevier, Tokyo, pp. 1–14.

    Google Scholar 

  • Purugganan, M.D. and Wessler, S.R. 1994. Molecular evolution of the plant R regulatory gene family. Genetics 138: 849–854.

    Google Scholar 

  • Quattrocchio, F., Wing, J.F., van der Woude, K., Mol, J.N.M. and Koes, R. 1998. Analysis of bHLH and MYB-domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J. 13: 475–488.

    Google Scholar 

  • Robbins, T.P., Chen, J., Norell, M.A. and Dellaporta, S.L. 1989. Molecular and genetic analysis of the R and B loci in maize. In: D.E. Styles, G.A. Gavazzi and M.L. Racchi (Eds.), The Genetics of Flavanoids. Proceedings of a Post Congress Meeting of the XVI International Congress of Genetics, Edizioni Unicopli, Milan, pp. 105–114.

  • Robbins, T.P., Walker, E.L., Kermicle, J.L., Alleman, M. and Dellaporta, S.L. 1991. Meiotic instability of the R-r complex arising from displaced intragenic exchange and intrachromosomal rearrangement. Genetics 129: 271–283.

    Google Scholar 

  • SanMiguel, P., Tikhonov, A., Jin, Y., Motchoulskaia, N., Zakharov, D., Melake-Berhan, A., Springer, P.S., Edwards, K.J., Lee, M., Avramova, Z. and Bennetzen, J.L. 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.

    Google Scholar 

  • Shieh, M.W., Wessler, S.R. and Raikhel, N.V. 1993. Nuclear targeting of the maize R protein requires two nuclear localization sequences. Plant Physiol. 101: 353–361.

    Google Scholar 

  • Styles, E.D., Ceska, O. and Seah, K.T. 1973. Developmental differences in action of R and B alleles in maize. Can. J. Genet. Cytol. 15: 59–72.

    Google Scholar 

  • Takahashi, M. 1982. Gene analysis and its related problems. J. Fac. Agric. Hokkaido Univ. 61: 93–99.

    Google Scholar 

  • Vaucheret, H., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J., Mourrain, P., Palauqui, J. and Vernhettes, S. 1998. Transgene-induced gene silencing in plants. Plant J. 16: 651–659.

    Google Scholar 

  • Vaughan, D.A. 1989. The genus Oryza L.: current status of taxonomy. Int. Rice Res. Inst. Res. Pap. Ser. 138: 3–21.

    Google Scholar 

  • Walker, E.L., Robbins, T.P., Bureau, T.E., Kermicle, J. and Dellaporta, S.L. 1995. Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex. EMBO J. 14: 2350–2363.

    Google Scholar 

  • Wessler, S.R., Bureau, T.E. and White, S.E. 1995. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5: 814–821.

    Google Scholar 

Download references

Author information

Author notes

  1. Jianping Hu

    Present address: Plant Biology Lab, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Road, La Jolla, CA , 92037, USA

Authors and Affiliations

  1. Departments of Botany and Genetics, University of Georgia, Athens, GA , 30602, USA

    Vaka S. Reddy & Susan R. Wessler

Authors
  1. Jianping Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vaka S. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan R. Wessler
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hu, J., Reddy, V.S. & Wessler, S.R. The rice R gene family: two distinct subfamilies containing several miniature inverted-repeat transposable elements. Plant Mol Biol 42, 667–678 (2000). https://doi.org/10.1023/A:1006355510883

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006355510883

Search

Navigation