Genetics, Vol. 167, 1961-1973, August 2004, Copyright © 2004
doi:10.1534/genetics.104.027896

Stochastic and Epigenetic Changes of Gene Expression in Arabidopsis Polyploids

Jianlin Wang^*, Lu Tian^*, Andreas Madlung^,, Hyeon-Se Lee^*, Meng Chen^*, Jinsuk J. Lee^*, Brian Watson, Trevor Kagochi, Luca Comai and Z. Jeffrey Chen^*,1

^* Genetics Program and Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas 77843-2474
Department of Biology, University of Washington, Seattle, Washington 98195-5325
Department of Biology, University of Puget Sound, Tacoma, Washington 98416

¹ Corresponding author: Molecular Genetics/MS 2474, Department of Soil and Crop Sciences, Texas A&M University, College Station, TX 77843-2474.
E-mail: zjchen{at}tamu.edu

Polyploidization is an abrupt speciation mechanism for eukaryotes and is especially common in plants. However, little is known about patterns and mechanisms of gene regulation during early stages of polyploid formation. Here we analyzed differential expression patterns of the progenitors' genes among successive selfing generations and independent lineages. The synthetic Arabidopsis allotetraploid lines were produced by a genetic cross between A. thaliana and A. arenosa autotetraploids. We found that some progenitors' genes are differentially expressed in early generations, whereas other genes are silenced in late generations or among different siblings within a selfing generation, suggesting that the silencing of progenitors' genes is rapidly and/or stochastically established. Moreover, a subset of genes is affected in autotetraploid and multiple independent allotetraploid lines and in A. suecica, a natural allotetraploid derived from A. thaliana and A. arenosa, indicating locus-specific susceptibility to ploidy-dependent gene regulation. The role of DNA methylation in silencing progenitors' genes is tested in DNA-hypomethylation transgenic lines of A. suecica using RNA interference (RNAi). Two silenced genes are reactivated in both ddm1- and met1-RNAi lines, consistent with the demethylation of centromeric repeats and gene-specific regions in the genome. A rapid and stochastic process of differential gene expression is reinforced by epigenetic regulation during polyploid formation and evolution.

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