Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids

Abstract

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 genomewide gene expression analysis of Arabidopsis synthetic allotetraploids, using spotted 70-mer oligo-gene microarrays. We detected .15% transcriptome divergence between the progenitors, and 2105 and 1818 genes were highly expressed in Arabidopsis thaliana and A. arenosa, respectively. Approximately 5.2% (1362) and 5.6% (1469) genes displayed expression divergence from the midparent value (MPV) in two independently derived synthetic allotetraploids, suggesting nonadditive gene regulation following interspecific hybridization. Remarkably, the majority of nonadditively 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 nonadditively 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 rRNA genes subjected to nucleolar dominance and with overall suppression of the A. thaliana phenotype in the synthetic allotetraploids and natural A. suecica. The nonadditive 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 genomewide nonadditive gene regulation, providing a molecular basis for de novo variation and allopolyploid evolution.

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

“…(94) We predict that a common theme of gene expression changes in allotetraploids and inbred hybrids is heterotic and/or inter-genomic interactions between the alleles or loci that are dependent on the genetic distances or levels of sequence divergence between the species. (86) These findings may shed light on the relationship between heterosis (94) and evolutionary success of allopolyploids. (22) Indeed, allopolyploidization provides a means of permanent fixation of hybrid vigor between species.…”

“…(86) Over 15% of the transcriptome was differentially expressed between the progenitors, of which 8% and 7% genes were highly expressed in A. thaliana and A. arenosa, respectively. This may represent ''species-specific'' regulatory changes as a consequence of 5.8 million years of evolution since these parental species diverged.…”

“…In a recent study, Wang et al (2006) employed spotted oligo-gene microarrays to study transcriptome divergence in Arabidopsis synthetic allotetraploids and their parents. (86) Over 15% of the transcriptome was differentially expressed between the progenitors, of which 8% and 7% genes were highly expressed in A. thaliana and A. arenosa, respectively.…”

“…(42) Moreover, the differentially expressed genes belong to the ontology of various biological pathways including metabolism, energy, cell defense, signaling and aging, and plant hormonal regulation. Notably, few transposon-encoded genes are identified in the AFLP-cDNA and microarray analyses, (43,86) suggesting interspecific hybridization does not induce genome-wide transposon activation. Alternatively, the transposons may be settled in the late generations (S5) of selfing.…”

“…To determine how genome doubling affects gene expression, Wang et al (2006) analyzed gene expression differences between a diploid and isogenic autotetraploid. (86) Few genes were upregulated or downregulated in the Arabidopsis autotetraploids, consistent with the findings in yeast, in which a dozen genes were expressed differently in response to ploidy changes in a series of haploid, diploid, triploid and autotetraploid. (88) The data suggest that during autopolyploid formation the dosage-dependent regulatory mechanisms prevail.…”