Convergent evolution of desiccation tolerance in grasses

Desiccation tolerance has evolved repeatedly in plants as an adaptation to survive extreme environments. Plants use similar biophysical and cellular mechanisms to survive life without water, but convergence at the molecular, gene, and regulatory levels remains to be tested. Here, we explore the evolutionary mechanisms underlying the recurrent evolution of desiccation tolerance across grasses. We present genomes of three resurrection grasses native Sub-Saharan Africa. We leveraged comparative genomic and transcriptomic approaches to identify patterns of convergence and divergence across these species. We observed substantial overlap in gene duplication and expression associated with desiccation, and syntenic genes of shared origin are activated across species, indicative of parallel evolution. In other cases, similar metabolic pathways are induced, but using different gene sets, pointing towards phenotypic convergence. Species-specific mechanisms supplement these shared core mechanisms, underlining the complexity and diversity of evolutionary adaptations. Our findings provide insight into the evolutionary processes driving desiccation tolerance and highlight the roles of parallel mutation and complementary pathway adaptation in response to environmental challenges.

Funding provided by: National Science Foundation
Crossref Funder Registry ID: ror.org
Award Number: 1906094

Funding provided by: National Science Foundation
Crossref Funder Registry ID: ror.org
Award Number: 2213983

Funding provided by: National Science Foundation
Crossref Funder Registry ID: ror.org
Award Number: 1817347

These data were used to identify core mechanisms of desiccation tolerance shared across grasses. We subjected replicated sets of the resurrection grasses Oropetiuum capense, Tripogon minimus, and Microchloa caffra to a controlled dehydration-rehydration timecourse. Tissues were collected at six comparable timepoints (four during drying and two during recovery) for each of the three species. Plants were sampled at targeted hydration states including from well-watered, partially dehydrated, fully desiccated, and 24 and 48 hours post rehydration. The hydration status of tissues was validated by measuring relative water content. Gene expression data (RNAseq) was generated by extracting total RNA using Spectrum Plant Total RNA kit according to the manufacturer's instructions. Total RNA was then cleaned to remove impurities and contaminants using Zymo Clean & Concentrator kit. RNAseq libraries were constructed by Novagene following a standard polyA+ enrichment strategy and sequenced on an Illumina HiSeq 4000 for 150 bp paired end reads. We leveraged comparative genomic and transcriptomic approaches to identify patterns of convergence and divergence across these species.