Letter | Published:

An epigenetic mutation responsible for natural variation in floral symmetry

Nature volume 401, pages 157161 (09 September 1999) | Download Citation

Subjects

Abstract

Although there have been many molecular studies of morphological mutants generated in the laboratory, it is unclear how these are related to mutants in natural populations, where the constraints of natural selection and breeding structure are quite different. Here we characterize a naturally occurring mutant of Linaria vulgaris, originally described more than 250 years ago by Linnaeus1,2,3, in which the fundamental symmetry of the flower is changed from bilateral to radial. We show that the mutant carries a defect in Lcyc, a homologue of the cycloidea gene which controls dorsoventral asymmetry in Antirrhinum4. The Lcyc gene is extensively methylated and transcriptionally silent in the mutant. This modification is heritable and co-segregates with the mutant phenotype. Occasionally the mutant reverts phenotypically during somatic development, correlating with demethylation of Lcyc and restoration of gene expression. It is surprising that the first natural morphological mutant to be characterized should trace to methylation, given the rarity of this mutational mechanism in the laboratory. This indicates that epigenetic mutations may play a more significant role in evolution than has hitherto been suspected.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    De Peloria (Diss. Ac. Amoenitates Academicae III, Uppsala, 1749).

  2. 2.

    Linnaeus' peloria: the history of a monster. Theor. Appl. Genet. 54, 241–248 (1979).

  3. 3.

    in Species and Varieties: Their Origin by Mutations 459–487 (Open Court, Chicago, 1904).

  4. 4.

    et al. Origin of floral asymmetry in Antirrhinum. Nature 383, 794–799 (1996).

  5. 5.

    , & Genetic control of flower shape in Antirrhinum majus. Development 124, 1387–1392 (1997).

  6. 6.

    & Variegated phenotype and developmental changes of a maize allele originating from epimutation. Genetics 136, 1121–1141 (1994).

  7. 7.

    & Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100–1103 (1997).

  8. 8.

    & Alterations in DNA methylation may play a variety of roles in carcinogenesis. Cell 83, 13–15 (1995).

  9. 9.

    & Cancer epigenetics comes of age. Nature Genet. 21, 163–167 (1999).

  10. 10.

    Self-incompatibility in Linaria. Heredity 49, 349–352 (1982).

  11. 11.

    , , & Repeat-induced G-C to A-T mutations in Neurospora. Science 244, 1571–1575 (1989).

  12. 12.

    & CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. EMBO J. 11, 315–325 (1992).

  13. 13.

    & Epigenetic variation in evolution. J. Evol. Biol. 11, 159–183 (1997).

  14. 14.

    & The inheritance of acquired epigenetic variations. J. Theor. Biol. 139, 69–83 (1989).

  15. 15.

    & Sequencial scanning electron microscopy of a growing plant meristem. Protoplasma 147, 77–79 (1988).

  16. 16.

    The inheritance of self-sterility and the peloric flower shape in Antirrhinum. Genetics 17, 385–408 (1935).

  17. 17.

    The inheritance of self-sterility in certain species of Antirrhinum. Z. Indukt Abstammungs-Verebunst 77, 1–17 (1939).

  18. 18.

    et al. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72, 85–95 (1993).

  19. 19.

    A one tube reaction for the synthesis of blunt-ended double-stranded cDNA. Nucleic Acids Res. 16, 2726 (1988).

  20. 20.

    , & Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl Acad. Sci. USA 85, 8998–9002 (1988).

  21. 21.

    , , & The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18, 215–222 (1999).

  22. 22.

    et al. Floricaula: a homeotic gene required for flower development in Antirrhinum majus. Cell 63, 1311–1322 (1990).

  23. 23.

    et al. Control of flower development and phyllotaxy by meristem identity genes in Antirrhinum. The Plant Cell 7, 2001–2011 (1995).

  24. 24.

    et al. Control of inflorescence architecture in Antirrhinum. Nature 379, 791–797 (1996).

Download references

Acknowledgements

We thank the Linnean Society of London for permission to photograph the specimen of peloric Linaria kept in Linnaeus' herbarium and thank C. Jarvis from the Natural History Museum in London for providing the photograph; we also thank M. Cragg-Barber for providing a living peloric specimen from the UK; N. Hartley for sequencing the genomic Lcyc region; D. Bradley for the Lcentroradialis probe; C. Martin for the Antirrhinum ubiquitin probe; and R. Carpenter, D. Bradley, O. Ratcliffe, I. Amaya and U. Nath for comments on the manuscript. This work was supported by the Gatsby Charitable Foundation. P.C. was an EMBO postdoctoral fellow and a EU postdoctoral fellow.

Author information

Author notes

    • Pilar Cubas

    Present address: Centro Nacional de Biotecnologia Campus de la Universidad Autónoma de Madrid, Cantoblanco, 28049, Madrid, Spain.

Affiliations

  1. John Innes Centre, Colney Lane, Norwich NR4 7UH, UK

Authors

  1. Search for Pilar Cubas in:

  2. Search for Coral Vincent in:

  3. Search for Enrico Coen in:

Corresponding author

Correspondence to Enrico Coen.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/43657

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.