Abstract
A fundamental tenet of classical mendelian genetics is that allelic information is stably inherited from one generation to the next, resulting in predictable segregation patterns of differing alleles1. Although several exceptions to this principle are known, all represent specialized cases that are mechanistically restricted to either a limited set of specific genes (for example mating type conversion in yeast2) or specific types of alleles (for example alleles containing transposons3 or repeated sequences4). Here we show that Arabidopsis plants homozygous for recessive mutant alleles of the organ fusion gene HOTHEAD5 (HTH) can inherit allele-specific DNA sequence information that was not present in the chromosomal genome of their parents but was present in previous generations. This previously undescribed process is shown to occur at all DNA sequence polymorphisms examined and therefore seems to be a general mechanism for extra-genomic inheritance of DNA sequence information. We postulate that these genetic restoration events are the result of a template-directed process that makes use of an ancestral RNA-sequence cache.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Non-coding RNAs match the deleted genomic regions in humans
Scientific Reports Open Access 17 November 2016
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout


References
Mendel, G. Versuche über Pflanzen Hybriden. Verhandl. Naturforsch. Ver. Brünn 4, 3–47 (1866)
Klar, A. J., Fogel, S. & Lusnak, K. Gene conversion of the mating-type locus in Saccharomyces cerevisiae . Genetics 92, 777–782 (1979)
McClintock, B. The origin and behavior of mutable loci in maize. Proc. Natl Acad. Sci. USA 36, 344–355 (1950)
Gondo, Y. et al. High-frequency genetic reversion mediated by a DNA duplication: the mouse pink-eyed unstable mutation. Proc. Natl Acad. Sci. USA 90, 297–301 (1993)
Lolle, S. J., Hsu, W. & Pruitt, R. E. Genetic analysis of organ fusion in Arabidopsis thaliana . Genetics 149, 607–619 (1998)
Krolikowski, K. A., Victor, J. L., Nussbaum Wagler, T., Lolle, S. J. & Pruitt, R. E. Isolation and characterization of the Arabidopsis organ fusion gene HOTHEAD . Plant J. 35, 501–511 (2003)
Song, K., Lu, P., Tang, K. & Osborn, T. C. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl Acad. Sci. USA 92, 7719–7723 (1995)
Taller, J., Hirata, Y., Yagishita, N., Kita, M. & Ogata, S. Graft-induced genetic changes and the inheritance of several characteristics in pepper (Capsicum annuum L.). Theor. Appl. Genet. 97, 705–713 (1998)
Auerbach, C. & Kilbey, B. J. Mutation in eukaryotes. Annu. Rev. Genet. 5, 163–218 (1971)
Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans . Nature 391, 806–811 (1998)
Cogoni, C. et al. Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J. 15, 3153–3163 (1996)
Palauqui, J. C., Elmayan, T., Pollien, J. M. & Vaucheret, H. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16, 4738–4745 (1997)
Cogoni, C. & Macino, G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399, 166–169 (1999)
Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D. C. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101, 543–553 (2000)
Mourrain, P. et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533–542 (2000)
Wassenegger, M., Heimes, S., Riedel, L. & Sanger, H. L. RNA-directed de novo methylation of genomic sequences in plants. Cell 76, 567–576 (1994)
Mette, M. F., Aufsatz, W., van der Winden, J., Matzke, M. A. & Matzke, A. J. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19, 5194–5201 (2000)
Bao, N., Lye, K.-W. & Barton, M. K. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell 7, 653–662 (2004)
Cole-Strauss, A. et al. Correction of the mutation responsible for sickle cell anemia by an RNA-DNA oligonucleotide. Science 273, 1386–1389 (1996)
Beetham, P. R., Kipp, P. B., Sawycky, X. L., Arntzen, C. J. & May, G. D. A tool for functional plant genomics: chimeric RNA/DNA oligonucleotides cause in vivo gene-specific mutations. Proc. Natl Acad. Sci. USA 96, 8774–8778 (1999)
Zhu, T. et al. Targeted manipulation of maize genes in vivo using chimeric RNA/DNA oligonucleotides. Proc. Natl Acad. Sci. USA 96, 8768–8773 (1999)
Hall, B. G. Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics 126, 5–16 (1990)
Foster, P. L. & Cairns, J. Mechanisms of directed mutation. Genetics 131, 783–789 (1992)
Galitski, T. & Roth, J. R. A search for a general phenomenon of adaptive mutability. Genetics 143, 645–659 (1996)
Ries, G. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000)
Bjedov, I. et al. Stress-induced mutagenesis in bacteria. Science 300, 1404–1409 (2003)
Kovalchuk, I. et al. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423, 760–762 (2003)
Queitsch, C., Sangster, T. A. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618–624 (2002)
Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998)
Pruitt, R. E., Vielle-Calzada, J. P., Ploense, S. E., Grossniklaus, U. & Lolle, S. J. FIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme. Proc. Natl Acad. Sci. USA 97, 1311–1316 (2000)
Acknowledgements
We thank R. M. Lee and T. Nussbaum Wagler for technical assistance, and J. A. Banks, J. L. Bowman, U. Grossniklaus, R. A. Jorgensen, J. Ogas, D. R. Smyth, A. Steimer, V. Sundaresan and M. A. Webb for discussions. This work was supported by the National Science Foundation. Any opinion, findings, conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Lolle, S., Victor, J., Young, J. et al. Genome-wide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434, 505–509 (2005). https://doi.org/10.1038/nature03380
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03380
This article is cited by
-
Non-coding RNAs match the deleted genomic regions in humans
Scientific Reports (2016)
-
Genetic response of Paspalum plicatulum to genome duplication
Genetica (2014)
-
Do plants 'veto' bad genes?
Nature (2013)
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.