The complex octoploid Craterostigma genome and tissue-specific mechanisms underlying desiccation tolerance

Abstract

Resurrection plants can survive prolonged anhydrobiosis, and desiccation tolerance has evolved recurrently across land plants as a common adaptation for survival in regions with seasonal drying. Craterostigma plantagineum was among the first model resurrection plants, and many of the genetic mechanisms underlying desiccation tolerance were discovered in this important system. Here, we analyzed the complex, octoploid Craterostigma (C. plantagineum) genome and surveyed spatial and temporal expression dynamics to identify genetic elements underlying desiccation tolerance. Homeologous genes within the Craterostigma genome have divergent expression profiles, suggesting the subgenomes contribute differently to desiccation tolerance traits. The Craterostigma genome contains almost 200 tandemly duplicated early light induced proteins (ELIPs), a hallmark trait of desiccation tolerance, with massive upregulation under water deficit. We identified a core network of desiccation responsive genes across all tissues but observed almost entirely unique expression dynamics in each tissue during recovery. Roots and leaves have differential responses related to light and photoprotection, autophagy, and nutrient transport, reflecting their divergent functions. Our findings highlight a universal set of likely ancestral desiccation tolerance mechanisms to protect cellular macromolecules under anhydrobiosis, with secondary adaptations related to tissue function.