Multi‐Omics Insights into the Evolution of Angiosperm Resurrection Plants

Abstract

A small group of angiosperms possess vegetative desiccation tolerance (VDT). This unique ability allows them to withstand near total loss of cellular water and recover unharmed upon rehydration. Recently, omics technologies have begun to give greater insight into the mechanisms that regulate VDT. Several angiosperm resurrection plant genomes, from both monocot and eudicot lineages, have been sequenced in the past decade. Multiple transcriptomic and metabolomic analyses of desiccation and rehydration in resurrection plants have emphasised the importance and ubiquity of known VDT responses, such as the induction of late embryogenesis abundants (LEAs), sugars, and antioxidants. These studies have also confirmed the similarity between VDT and the process of orthodox seed maturation drying, and highlighted the connection between embryonic, seedling, and vegetative DT. However, the exact genes and pathways that regulate the acquisition of seed traits in leaves remain elusive. This article attempts to integrate what is currently understood about the evolution and regulation of VDT in angiosperm resurrection plants, drawing from the rapidly growing collection of omics datasets derived from these species. The limits of current knowledge, future research perspectives, and the utility of VDT research as a resource for the improvement of drought tolerance in crop species are also discussed.

Unexplored dimensions of variability in vegetative desiccation tolerance

“…Of the ~600 known resurrection plants, these represent a very small subset, and yet substantial variation in the mechanism of desiccation tolerance is evident even among these selected species. In fact, unique patterns of gene expression, metabolism, stress physiology, and genome structure have been observed within this subset (Dinakar and Bartels, 2013; Lyall and Gechev, 2018; Oliver et al, 2020). The variation contained within these species is a valuable source of information that can be leveraged to distinguish among the core vs. species‐specific mechanisms of tolerance.…”

Systems biology of resurrection plants

“…Interestingly, most proteins appeared to have a low correlation between their abundance and the expression levels of the associated mRNA transcript. This suggests extensive utilisation of post-transcriptional/translational regulation during VDT, something that has been observed in seeds and other plant tissues under stress and that has been suggested to occur in resurrection plants [ 1 , 5 , 185 ]. This study reinforces the need for a systems-based methodology to disentangle such instances where the results of a single approach are incomplete.…”

“…The increased accessibility of next-generation RNA-seq has resulted in increased numbers of resurrection plant transcriptome studies [ 5 ]. Most datasets are devoted to dehydration, desiccation and rehydration responses in leaf tissues, but a limited number of experiments also target additional stresses like extended darkness [ 21 ], heat stress [ 91 ], the influence of hormones like ABA (abscisic acid) and auxins [ 92 , 93 ], or other organs and developmental stages, including maturing seeds [ 39 ] and roots [ 94 ].…”

“…1 ). Desiccation-tolerant species comprise algae, mosses, ferns, and lycopods, as well as angiosperm plants (both monocots and dicots), but not in gymnosperms [ 1 , 5 ]. About 300 angiosperm resurrection plants have been described evolving independently in at least 13 different lineages making up less than 0.2% of the total Flora [ 6 , 7 ].…”

Comparative Analysis of ROS Network Genes in Extremophile Eukaryotes

“…Several microscopic animals are DT, including tardigrades, nematodes and rotifers, though in complex animals only the larvae of the chironomid insect Polypedilum vanderplanki show DT [36,37]. The damaging effects of ROS are thought to be a major barrier to survival during anhydrobiosis [38], and the up-regulation of genes associated with maintenance of ROS homoeostasis is commonly reported in DT species [39]. Antioxidant status is a predictor of survival of the resurrection plant Myrothamnus flabellifolia [40], and poikilochlorophyllous resurrection plants in regions with high irradiance degrade chlorophyll during desiccation to prevent passive production of ROS [34,35].…”