Seed desiccation mechanisms co‐opted for vegetative desiccation in the resurrection grass Oropetium thomaeum

Abstract

Resurrection plants desiccate during periods of prolonged drought stress, then resume normal cellular metabolism upon water availability. Desiccation tolerance has multiple origins in flowering plants, and it likely evolved through rewiring seed desiccation pathways. Oropetium thomaeum is an emerging model for extreme drought tolerance, and its genome, which is the smallest among surveyed grasses, was recently sequenced. Combining RNA-seq, targeted metabolite analysis and comparative genomics, we show evidence for co-option of seed-specific pathways during vegetative desiccation. Desiccation-related gene co-expression clusters are enriched in functions related to seed development including several seed-specific transcription factors. Across the metabolic network, pathways involved in programmed cell death inhibition, ABA signalling and others are activated during dehydration. Oleosins and oil bodies that typically function in seed storage are highly abundant in desiccated leaves and may function for membrane stability and storage. Orthologs to seed-specific LEA proteins from rice and maize have neofunctionalized in Oropetium with high expression during desiccation. Accumulation of sucrose, raffinose and stachyose in drying leaves mirrors sugar accumulation patterns in maturing seeds. Together, these results connect vegetative desiccation with existing seed desiccation and drought responsive pathways and provide some key candidate genes for engineering improved drought tolerance in crop plants.

Plant Desiccation Tolerance and its Regulation in the Foliage of Resurrection “Flowering-Plant” Species

“…Interestingly, in general, these 'omic' studies are also supportive of the earlier hypotheses that vegetative desiccation tolerance has independently evolved in different taxa via reactivation of pathways normally restricted to seed maturation in plants (e.g., [137,155,159,162]. A major challenge over the next few years will undoubtedly be to understand the nature of regulatory genes, and their activation, which control the expression of these 'protective protein' genes at appropriate stages of the desiccation process.…”

“…As methodology and cost effectiveness of DNA analysis has steadily improved over recent years, involving larger scale transcriptomic studies and entire genomic analysis of monocotyledenous and dicotyledonous species from different regions of the globe, so there has been a steady increase in the number and range of gene transcripts that appear to be involved in the onset of desiccation tolerance [59,87,101,[155][156][157][158][159][160][161]. Although there are differences in the specific molecular responses of different types resurrection plants, probably reflecting lineage-specific adaptations to widely variable geographic areas and localised responses to environmental stresses, together analysis of the predicted proteins encoded by many of these genes does point to them playing a role in protection of cellular components from the otherwise destructive effects of water loss and oxidative damage upon cellular biochemical processes and structural integrity of cell walls and entire tissues.…”

“…It is hypothesised that the mechanisms that operate in seed and pollen, resulting in desiccation tolerance, were re-activated in the vegetative tissue of resurrection plants [155,159,162]. To date, several genes involved in seed maturation have been linked to desiccation tolerance in resurrection plants.…”

A chromosome‐scale assembly of the model desiccation tolerant grass Oropetium thomaeum

“…The expression patterns of newly annotated genes were surveyed using high‐resolution RNAseq expression data (VanBuren et al., ). This dataset consists of seven leaf samples collected during desiccation and rehydration timecourses.…”

“…Translated coding exons and proteins from the reference gene annotations and genome assemblies were extracted using the module Extractor function of GeMoMa (module Extractor: Ambiguity = AMBIGUOUS, r = true). RNAseq data from Oropetium desiccation and rehydration timecourses (VanBuren et al., ) were aligned to the V2 Oropetium genome using HISAT2 (Kim, Langmead, & Salzberg, ) with default parameters. The resulting BAM files were used to extract intron and exon boundaries using the module ERE (module ERE: s = FR_FIRST_STRAND, c = true).…”