A footprint of desiccation tolerance in the genome of Xerophyta viscosa

Abstract

Desiccation tolerance is common in seeds and various other organisms, but only a few angiosperm species possess vegetative desiccation tolerance. These 'resurrection species' may serve as ideal models for the ultimate design of crops with enhanced drought tolerance. To understand the molecular and genetic mechanisms enabling vegetative desiccation tolerance, we produced a high-quality whole-genome sequence for the resurrection plant Xerophyta viscosa and assessed transcriptome changes during its dehydration. Data revealed induction of transcripts typically associated with desiccation tolerance in seeds and involvement of orthologues of ABI3 and ABI5, both key regulators of seed maturation. Dehydration resulted in both increased, but predominantly reduced, transcript abundance of genomic 'clusters of desiccation-associated genes' (CoDAGs), reflecting the cessation of growth that allows for the expression of desiccation tolerance. Vegetative desiccation tolerance in X. viscosa was found to be uncoupled from drought-induced senescence. We provide strong support for the hypothesis that vegetative desiccation tolerance arose by redirection of genetic information from desiccation-tolerant seeds.

Orthodox Seeds and Resurrection Plants: Two of a Kind?

“…An analysis of the genome of the resurrection species Xerophyta viscosa, along with transcriptomic changes that occur during desiccation and rehydration, indicated that transcripts typically associated with seed DT were induced, such as homologs of the transcription factor gene ABSCISIC ACID INSENSITIVE3 (ABI3; see Box 1; Costa et al, 2017). The lack of DT-specific genome organizational features in the resurrection species Boea hygrometrica supports the notion that vegetative DT evolved from preexisting genetic modules (Xiao et al, 2015).…”

“…Phylogenetic evidence suggests that vegetative DT in angiosperm resurrection plants represents an adaptation of developmentally regulated DT mechanisms in seeds that have been adjusted to the whole-plant context (Oliver et al, 2000;Illing et al, 2005;Rascio and La Rocca, 2005;Bartels and Hussain, 2011;Farrant and Moore, 2011;Farrant et al, 2015;Costa et al, 2017). Some similarities between seeds and angiosperm resurrection plants have been analyzed in the past (Illing et al, 2005), and the availability of more comprehensive desiccationassociated transcriptomes from resurrection plants (Rodriguez et al, 2010;Bartels and Hussain, 2011;Yobi et al, 2017) linked to sequenced genomes (Xiao et al, 2015;Costa et al, 2017) and seedlings in which DT is reintroduced (Maia et al, 2011;Terrasson et al, 2013;Costa et al, 2015) is allowing the exact mechanisms inherited by these plants to be refined. For example, a cross-species comparison of DT-related transcriptomes revealed a considerable similarity in the genes involved in vegetative DT and seed DT (Costa et al, 2016).…”

“…Genomic evidence indicates that different changes have taken place behind the evolution of each resurrection plant lineage. For instance, the percentage of the genome that accounts for transposable elements is surprisingly low in X. viscosa (18%; Costa et al, 2017) compared with Oropetium thomaeum (75%; VanBuren et al, 2015) and B. hygrometrica (43%; Xiao et al, 2015). The types of genome duplication events that contributed to the number of genes encoding the protective late embryogenesis abundant (LEA) proteins (see Box 1) in angiosperm resurrection plants also differ: whole-genome duplications played critical roles in X. viscosa, while in O. thomaeum and B. hygrometrica, dispersed duplications were more crucial (Costa et al, 2017).…”

“…For instance, the percentage of the genome that accounts for transposable elements is surprisingly low in X. viscosa (18%; Costa et al, 2017) compared with Oropetium thomaeum (75%; VanBuren et al, 2015) and B. hygrometrica (43%; Xiao et al, 2015). The types of genome duplication events that contributed to the number of genes encoding the protective late embryogenesis abundant (LEA) proteins (see Box 1) in angiosperm resurrection plants also differ: whole-genome duplications played critical roles in X. viscosa, while in O. thomaeum and B. hygrometrica, dispersed duplications were more crucial (Costa et al, 2017). An analysis of gene families that expanded and contracted in X. viscosa in relation to 15 other plant genomes, including O. thomaeum, indicated a small overlap in the gene families that expanded and contracted in only these two resurrection species (Costa et al, 2017).…”

“…The types of genome duplication events that contributed to the number of genes encoding the protective late embryogenesis abundant (LEA) proteins (see Box 1) in angiosperm resurrection plants also differ: whole-genome duplications played critical roles in X. viscosa, while in O. thomaeum and B. hygrometrica, dispersed duplications were more crucial (Costa et al, 2017). An analysis of gene families that expanded and contracted in X. viscosa in relation to 15 other plant genomes, including O. thomaeum, indicated a small overlap in the gene families that expanded and contracted in only these two resurrection species (Costa et al, 2017). A large fraction of the contigs assembled from hydrated, dehydrated, desiccated, and rehydrated samples of the resurrection species Sporobolus stapfianus (Yobi et al, 2017), Craterostigma plantagineum (Giarola and Bartels, 2015), and Haberlea rhodopensis (Gechev et al, 2013) predict the presence of protein sequences that bear little or no similarity to proteins in public databanks.…”