Desiccation-driven senescence and its repression in Xerophyta schlechteri are regulated at extremely low water contents

Abstract

Vegetative desiccation tolerance, the ability to survive loss of over 90% of cellular water, is an extremely rare trait in Angiosperms. Xerophyta schlechteri survives such extreme water deficit by entering prolonged quiescence and suppressing drought-induced senescence in most of the leaf area, except the apical tip. Information on the molecular regulation of senescence in such plants is scarce and this is the first study to investigate such regulation in senescing and non-senescing tissues of the same leaf. Genome-wide RNA sequencing enabled comparison of senescent and non-senescent tissues during desiccation and early rehydration, establishment of the water content range in which senescence is initiated and identification of molecular mechanisms employed to bring about cellular death. Senescence-associated genes (XsSAG) specific to this species were identified and two potential regulatory sites were enriched in regions upstream to these XsSAGs, allowing us to create a model of senescence regulation in X. schlechteri based on homology with known Arabidopsis senescence regulators. We hypothesise that desiccation-driven senescence occurs as a result of a convergence of signals around MAPK6 to trigger WRKY-mediated ethylene synthesis and XsSAG expression, not unlike aging and stress-related senescence in Arabidopsis, but at remarkably lower water contents (<35% RWC).

Core cellular and tissue‐specific mechanisms enable desiccation tolerance in Craterostigma

“…Desiccation tolerance is often viewed as a binary trait, but it varies across tissues and life stages of an individual plant, and some species have lower rates of tissue recovery, sensitivity to drying rate or decreased viability over time (Marks et al., 2021). This variability in tolerance is especially common in the life phases of bryophytes (Coe et al., 2021) and different leaf tissues in monocots (Radermacher et al., 2021). Craterostigma species are arguably more resilient to desiccation than other resurrection plant lineages (including L. breviden s; Cooper & Farrant, 2002; Phillips et al., 2008), and this improved tolerance may be related to polyploidy.…”

A Label-Free Proteomic and Complementary Metabolomic Analysis of Leaves of the Resurrection Plant Xerophyta schlechteri during Dehydration

“…Among these are the clear osmotic adjustment, induction of secondary metabolism and antioxidant potential during early dehydration, marked downregulation of photosynthetic metabolism and switches from growth promotion (carbon source) to accumulation of protective processes (sink) during further dehydration to 40% RWC and below this, with notable but limited ongoing metabolism geared toward entry into a biophysically stable quiescent state fully prepared for recovery upon rehydration. Furthermore, our study adds to the existing transcriptomic and genomic information of desiccation tolerance in X. schlechteri [16,40] which, together with numerous physiological studies [14,15,18], makes this the most comprehensively documented monocot resurrection plant to date and widens its known potential as a model [13] for the ultimate production of drought-tolerant cereals.…”

“…It has been shown to accumulate during the MRD and LRD in Xerophyta viscosa [74]. Increased levels of RUB2 could relate to the observed phenomenon in this and other resurrection plants of activation of the ubiquitin proteasomal system (UPS), proposed to be a less severe response than autophagy and allowing for the release of nutrients for protective purposes [40,42,76].…”

“…Furthermore, this suggests that there was an increase chaperonin-like activity and favorable molecular associations with increased water loss, with an increase in the catalytic potential in such water-limited environments. Ongoing transcription [16,40] and translation [41,42] in the LRD is a phenomenon observed in resurrection plants, but it is not entirely understood.…”

“…The upregulation of RNA processes could also involve the transcription of RNA required for recovery, particularly for photosynthesis (a category also upregulated in the LRD). X. schlechteri has been shown to continue to select RNA transcription in the LRD, with transcripts associated with photosynthesis being stably stored until translation upon recovery [16,40]. Intriguingly, cellular respiration is upregulated at the LRD, as indicated by an increase in phosphoglycerate kinase (GO: 0006096), a protein involved in glycolysis, and Mundree and Farrant (2000) have shown that measurable respiration in this species continues until the RWC is as low as 10% [14].…”