Coevolution of tandemly repeated <i>hlips</i> and RpaB-like transcriptional factor confers desiccation tolerance to subaerial <i>Nostoc</i> species.

Abstract

Desert-inhabiting cyanobacteria can tolerate extreme desiccation and quickly revive after rehydration. The regulatory mechanisms that enable their vegetative cells to resurrect upon rehydration are poorly understood. In this study, we identified a single gene family of high light-inducible proteins (Hlips) with dramatic expansion in the <i>Nostoc flagelliforme</i> genome and found an intriguingly special convergence formed through four tandem gene duplication. The emerged four independent <i>hlip</i> genes form a gene cluster (<i>hlips-cluster</i>) and respond to dehydration positively. The gene mutants in <i>N. flagelliforme</i> were successfully generated by using gene-editing technology. Phenotypic analysis showed that the desiccation tolerance of <i>hlips-cluster</i>-deleted mutant decreased significantly due to impaired photosystem II repair, whereas heterologous expression of <i>hlips-cluster</i> from <i>N. flagelliforme</i> enhanced desiccation tolerance in <i>Nostoc</i> sp. PCC 7120. Furthermore, a transcription factor Hrf1 (<i>hlips-cluster</i> repressor factor 1) was identified and shown to coordinately regulate the expression of <i>hlips-cluster</i> and desiccation-induced <i>psbAs</i>. Hrf1 acts as a negative regulator for the adaptation of <i>N. flagelliforme</i> to the harsh desert environment. Phylogenetic analysis revealed that most species in the <i>Nostoc</i> genus possess both tandemly repeated Hlips and Hrf1. Our results suggest convergent evolution of desiccation tolerance through the coevolution of tandem Hlips duplication and Hrf1 in subaerial <i>Nostoc</i> species, providing insights into the mechanism of desiccation tolerance in photosynthetic organisms.