Co-option of ancestral stem regulators drove recurrent evolution of underground storage organs

Abstract

Geophytes are plants that produce underground storage organs such as tubers, rhizomes, and bulbs, to facilitate asexual reproduction and withstand a myriad of environmental challenges. While the potato ( Solanum tuberosum L.) serves as the primary model for studying tuberization, the genetic mechanisms encoding this trait across diverse angiosperm lineages remains unclear. This study utilized a phylogenomic-transcriptomic approach to compare tuber development across nine tuberizing species with five nontuberizing sister taxa. We identified orthologs of key potato tuberization genes that exhibit similar expression in the stolons or tubers of these distant relatives. In nontuberizing species, these orthologs exhibit distinct expression profiles and are primarily expressed in the stem. This suggests that the independent evolution of tubers across angiosperms resulted from shifts in the expression of preexisting genes that led to their co-option. This process, also known as exaptation, occurs when existing genetic suites are recruited for entirely new biological functions. This mechanism stands in contrast to the repeated loss or gain of genes, which has been associated with the origin of other adaptive plant traits. Furthermore, the co-option of the same genes was observed in species with other stem-derived storage organs, such as rhizomes and runners. These findings reveal a conserved evolutionary model for the development of stem-derived geophyte organs that evolved independently across the flowering plants over the past 160 My.