Desiccation tolerance evolved through gene duplication and network rewiring in Lindernia.

Though several resurrection plant genomes have been sequenced, the lack of suitable dehydration-sensitive outgroups has limited genomic insights into the origin of desiccation tolerance. Here, we utilized a comparative system of closely related desiccation-tolerant (Lindernia brevidens) and -sensitive (L. subracemosa) species to identify gene and pathway level changes associated with the evolution of desiccation tolerance. The two high-quality Lindernia genomes we assembled are largely collinear and over 90% of genes are conserved. L. brevidens and L. subracemosa have evidence of an ancient, shared whole-genome duplication event, and retained genes have neofunctionalized, with desiccation-specific expression in L. brevidens. Tandem gene duplicates are also enriched in desiccation-associated functions including a dramatic expansion of early light induced proteins (ELIPs) from 4 to 26 copies in L. brevidens. A comparative differential gene co-expression analysis between L. brevidens and L. subracemosa supports extensive network rewiring across early dehydration, desiccation, and rehydration timecourses. Many LEA genes show significantly higher expression in L. brevidens compared to their orthologs in L. subracemosa. Co-expression modules uniquely upregulated during desiccation in L. brevidens are enriched with seed-specific and ABA-associated cis regulatory elements. These modules contain a wide array of seed-associated genes that have no expression in the desiccation-sensitive L. subracemosa. Together these findings suggest that desiccation tolerance evolved through a combination of gene duplications and network level rewiring of existing seed desiccation pathways.