Phylotranscriptomics provides a treasure trove of flood tolerance mechanisms in the Cardamineae tribe

Abstract

Flooding events are highly detrimental to most terrestrial plant species. However, there is an impressive diversity of plant species that thrive in flood-prone regions and represent a treasure trove of unexplored flood-resilience mechanisms. Here we surveyed a panel of four species from the Cardamineae tribe representing a broad tolerance range. This included the flood-tolerant Cardamine pratensis, Rorippa sylvestris and Rorippa palustris and the flood-sensitive species Cardamine hirsuta. All four species displayed a quiescent strategy, evidenced by the repression of shoot growth underwater. Comparative transcriptomics analyses between the four species and the sensitive model species Arabidopsis thaliana were facilitated via de-novo transcriptome assembly and identification of 16,902 universal orthogroups at a high resolution. Our results suggest that tolerance likely evolved separately in the Cardamine and Rorippa species. While the Rorippa response was marked by a strong downregulation of cell-cycle genes, Cardamine minimized overall transcriptional regulation. However, a weak starvation signature was a universal trait of tolerant species, potentially achieved in multiple ways. It could result from a strong decline in cell-cycle activity, but is also intertwined with autophagy, senescence, day-time photosynthesis and night-time fermentation capacity. Our dataset provides a rich source to study adaptational mechanisms of flooding tolerance.