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Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana

Abstract

Polyploidization is found frequently in plants1,2, and species previously considered to be diploid may show remnants of earlier polyploidization events on closer inspection of their genomes3. The success of polyploids may lie in increased genetic redundancy supporting subsequent genetic diversification4,5,6. Although doubling the genome does not generate diversity per se, recent studies show that rapid genomic rearrangements and changes in DNA modification and gene expression patterns are associated with polyploid formation7,8,9,10,11,12,13. But recessive modifications will not become phenotypically apparent in early polyploid generations. Here we show that epialleles in tetraploid plants (but not in diploids) interact in trans and lead to heritable gene silencing persisting after segregation from the inactivating allele. This mechanism, resembling paramutation, leads to the establishment of functional epigenetic homozygosity and, thus, to conversion of new recessive alleles into traits expressed in early polyploid generations. Such interactions probably contribute to rapid adaptation and evolution of polyploid plant species.

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Figure 1
Figure 2: Molecular analysis of the epialleles.
Figure 3: Methylation analysis of genomic DNA flanking HPT.
Figure 4: Segregation expected for independent transmission in F2 progeny of a tetraploid F1 duplex (genotype RR00 or RRSS) in case of pure chromosome segregation.
Figure 5: Allelic interaction leading to progressive or complete loss of resistance in F2 populations from crosses between C4R and C4S1 or C4R and C4S2.
Figure 6: Methylation analysis of HPT in plants with R and S epialleles combined.

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Acknowledgements

We thank our colleagues S. Adams, P. King, F. Meins and F.-L. Sun for critical comments on the manuscript and H. Angliker for help with the DNA sequence analysis. We acknowledge financial support from the Swiss Federal Office for Education and Science and the commission of the European Union to O.M.S.

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Correspondence to Ortrun Mittelsten Scheid.

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Mittelsten Scheid, O., Afsar, K. & Paszkowski, J. Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana. Nat Genet 34, 450–454 (2003). https://doi.org/10.1038/ng1210

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