Genome-wide Non-additive Gene Regulation in Arabidopsis Allotetraploids

Polyploidy has occurred throughout the evolutionary history of all eukaryotes and is extremely common in plants. Reunification of the evolutionarily-divergent genomes in allopolyploids creates regulatory incompatibilities that must be reconciled. Here we report genome-wide gene expression analysis of Arabidopsis synthetic allotetraploids using spotted 70-mer oligo-gene microarrays. We detected >15% transcriptome divergence between the progenitors, and 2,105 and 1,818 genes were highly expressed in Arabidopsis thaliana and A. arenosa, respectively. Approximately 5.2% (1,362) and 5.6% (1,469) genes displayed expression divergence from the mid-parent value in two independently-derived synthetic allotetraploids, suggesting non-additive gene regulation following interspecific hybridization. Remarkably, the majority of non-additively expressed genes in the allotetraploids also display expression changes between the parents, indicating that transcriptome divergence is reconciled during allopolyploid formation. Moreover, >65% of the non-additively expressed genes in the allotetraploids are repressed, and >94% of the repressed genes in the allotetraploids match the genes that are expressed at higher levels in A. thaliana than in A. arenosa, consistent with the silencing of A. thaliana subjected to nucleolar dominance and overall suppression of the A. thaliana phenotype in the synthetic allotetraploids and natural A. suecica. The non-additive gene regulation is involved in various biological pathways, and the changes in gene expression are developmentally regulated. In contrast to the small effects of genome doubling on gene regulation in autotetraploids, the combination of two divergent genomes in allotetraploids by interspecific hybridization induces genome-wide non-additive gene regulation, providing a molecular basis for de novo variation and allopolyploid evolution.

Key Words: Epigenetic regulation, Genetic dominance, Interspecific hybrids, Microarray, Polyploidy

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