Genome-Wide and Specific Effects of cis and trans Regulation on Phenotypic Diversity in Arabidopsis Allopolyploids and Their Progenitors

Interspecific hybridization and polyploidization most often lead to genome-wide epitome and transcriptome changes, shaping the evolution and adaptation of many plant species. In an interspecific cross between a synthetic autotetraploid Arabidopsis thaliana (At) and a natural autotetraploid Arabidopsis arenosa (Aa), a genome-wide change in gene expression was detected in the synthetic Arabidopsis suecica allotetraploid hybrids when compared to the progenitors. Using mRNA-seq, we showed genome-wide cis and trans effects on gene regulation in the two Arabidopsis autotetraploids and their tetraploid hybrids. Cis regulatory effects tend to be dominant in mediating expression divergence between At and Aa. For genes subjected to both cis and trans regulation, purifying selection acts through compensating cis and trans effects in reducing their allelic expression divergence. In the F1 allotetraploids, merging of the two diverse genomes (At4 and Aa) provides an opportunity for genetic interactions. Aa trans factors tends to up-regulate At alleles, whereas At trans factors tends to down-regulate Aa alleles. In the resynthesized and natural allotetraploids, trans effects drive expression of homoeologous alleles into the same direction. A specific example of this cis and trans regulation is the Arabidopsis miR163, which its expression mediates target genes regulation involving secondary metabolites accumulation in the allotetraploids and their progenitors. The availability of these related Arabidopsis species and the establishment of the synthetic allotetraploids thus provide an excellent and tractable genetic system for studying gene regulations upon species divergence and hybridization at the molecular level.