Vegetative desiccation tolerance in the resurrection plant Xerophyta humilis has not evolved through reactivation of the seed canonical LAFL regulatory network

Abstract

Summary It has been hypothesised that vegetative desiccation tolerance in resurrection plants evolved via reactivation of the canonical LAFL (i.e. LEC1, ABI3, FUS3 and LEC2) transcription factor (TF) network that activates the expression of genes during the maturation of orthodox seeds leading to desiccation tolerance of the plant embryo in most angiosperms. There is little direct evidence to support this, however, and the transcriptional changes that occur during seed maturation in resurrection plants have not previously been studied. Here we performed de novo transcriptome assembly for Xerophyta humilis, and analysed gene expression during seed maturation and vegetative desiccation. Our results indicate that differential expression of a set of 4205 genes is common to maturing seeds and desiccating leaves. This shared set of genes is enriched for gene ontology terms related to abiotic stress, including water stress and abscisic acid signalling, and includes many genes that are seed‐specific in Arabidopsis thaliana and targets of ABI3. However, while we observed upregulation of orthologues of the canonical LAFL TFs and ABI5 during seed maturation, similar to what is seen in A. thaliana, this did not occur during desiccation of leaf tissue. Thus, reactivation of components of the seed desiccation program in X. humilis vegetative tissues likely involves alternative transcriptional regulators.

Intertwined signatures of desiccation and drought tolerance in grasses

“…Although most ABI3-responsive genes are induced under water deficit, thomaeum. This is consistent with recent findings from Xerophyta humilis, where there was no evidence that ABI3 or the canonical LAFL seed maturation regulatory network was responsible for desiccation tolerance (48). Taken together, this suggests that many "seed-related" genes are expressed as a universal response to water deficit, but the regulation of these processes is likely distinct from seed regulatory networks.…”

MfPIF1 of Resurrection Plant Myrothamnus flabellifolia Plays a Positive Regulatory Role in Responding to Drought and Salinity Stresses in Arabidopsis

“…Lyall et al performed gene expression analysis in the monocot resurrection plant Xerophya humilis during vegetative desiccation, and speculated that the expression of the ABI3 regulator in leaf tissues is activated by a desiccation-responsive pathway. Based on the above research, we hypothesize that MfPIF1 may respond to drought stress by directly activating these ABRE-binding factors [76]. Altogether, our results presented evidence that MfPIF1 enhanced tolerance of Arabidopsis to drought and salinity stresses by participating in ABA biosynthesis and ABA-dependent stress-responding pathway.…”

Editorial: Unifying Insights into the Desiccation Tolerance Mechanisms of Resurrection Plants and Seeds

“…Their contribution underscores the view that resurrection species share “core” mechanisms for withstanding extreme water loss, but also employ species-specific features, even among closely related species. In light of the universality of DT among plant taxa, and indeed variation among seeds in precise mechanisms of DT, the view that DT in angiosperms evolved through rewiring of their seed genes is being questioned ( Lyall et al, 2019 ; Pardo et al, 2020 ). Rather, seeds should be considered as a subset of desiccation tolerant entities, each being equipped with similar core mechanisms but with their specific variation on the DT theme.…”