Evolutionary analysis of conserved non-coding elements subsequent to whole-genome duplication in opium poppy

Abstract

AbstractWhole-genome duplication (WGD) leads to the duplication of both coding and non-coding sequences within an organism’s genome, providing an abundant supply of genetic material that can drive evolution, ultimately contributing to plant adaptation and speciation. Although non-coding sequences contain numerous regulatory elements, they have been understudied compared to coding sequences. In order to address this gap, we explored the evolutionary patterns of regulatory sequences, coding sequences, and transcriptomes using conserved non-coding elements (CNEs) as regulatory element proxies following the recent WGD event in opium poppy (Papaver somniferum). Our results showed similar evolutionary patterns in subgenomes of regulatory and coding sequences. Specifically, the biased or unbiased retention of coding sequences reflected the same pattern as retention levels in regulatory sequences. Further, the divergence of gene expression patterns mediated by regulatory element variations occurred at a more rapid pace than that of gene coding sequences. However, gene losses were purportedly dependent on relaxed selection pressure in coding sequences. Specifically, the rapid evolution of tissue-specific benzylisoquinoline alkaloids production inP. somniferumwas associated with regulatory element changes. The origin of a novel stem-specific ACR, which utilized ancestral cis-elements as templates, is likely to be linked to the evolutionary trajectory behind the transition of thePSMT1-CYP719A21cluster from high levels of expression solely inP. rhoeasroot tissue to its elevated expression inP. somniferumstem tissue. Our findings demonstrate that rapid regulatory element evolution can contribute to the emergence of new phenotypes and provide valuable insights into the high evolvability of regulatory elements.Significance StatementThis study demonstrates that rapid evolution of regulatory elements can drive the emergence of novel phenotypes in plants. Our investigation, in particular, revealed that the evolution of stem-specific high expression patterns of BIAs genes inP. somniferumwas linked to rapid changes in regulatory elements.