A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker)

Abstract

Main conclusionProvides a first comprehensive review of integrated physiological and molecular aspects of desiccation toleranceXerophyta viscosa. A synopsis of biotechnological studies being undertaken to improve drought tolerance in maize is given.Xerophyta viscosa (Baker) is a monocotyledonous resurrection plant from the family Vellociacea that occurs in summer-rainfall areas of South Africa, Lesotho and Swaziland. It inhabits rocky terrain in exposed grasslands and frequently experiences periods of water deficit. Being a resurrection plant it tolerates the loss of 95 % of total cellular water, regaining full metabolic competency within 3 days of rehydration. In this paper, we review some of the molecular and physiological adaptations that occur during various stages of dehydration of X. viscosa, these being functionally grouped into early and late responses, which might be relevant to the attainment of desiccation tolerance. During early drying (to 55 % RWC) photosynthesis is shut down, there is increased presence and activity of housekeeping antioxidants and a redirection of metabolism to the increased formation of sucrose and raffinose family oligosaccharides. Other metabolic shifts suggest water replacement in vacuoles proposed to facilitate mechanical stabilization. Some regulatory processes observed include increased presence of a linker histone H1 variant, a Type 2C protein phosphatase, a calmodulin- and an ERD15-like protein. During the late stages of drying (to 10 % RWC) there was increased expression of several proteins involved in signal transduction, and retroelements speculated to be instrumental in gene silencing. There was induction of antioxidants not typically found in desiccation-sensitive systems, classical stress-associated proteins (HSP and LEAs), proteins involved in structural stabilization and those associated with changes in various metabolite pools during drying. Metabolites accumulated in this stage are proposed, inter alia, to facilitate subcellular stabilization by vitrification process which can include glass- and ionic liquid formation.

A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose

“…Indeed, they both have a stabilizing effect on proteins and membranes in vitro, particularly trehalose, which finds practical application as a stabilizer for vaccines and other labile pharmaceuticals, allowing their storage and transport without refrigeration. Desiccation-tolerant resurrection plants accumulate massive amounts of trehalose or Suc when exposed to drought, and their cells remain viable despite losing $95% of their water content (Drennan et al, 1993;Iturriaga et al, 2000;Farrant et al, 2015). One way in which trehalose protects cells is by initiating controlled autophagy, thereby avoiding uncontrolled damage that would otherwise trigger programmed cell death (Williams et al, 2015).…”

Orthodox Seeds and Resurrection Plants: Two of a Kind?

“…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.…”

“…Resurrection plants also experience a metabolic switch during dehydration. When water content drops below ;55% RWC, stomata close, carbon gain from photosynthesis ceases, and metabolism shifts from normal growth to cell defense and the accumulation of protective molecules, such as Suc, raffinose family oligosaccharides, and amino acids (Gechev et al, 2013;Farrant et al, 2015;Mladenov et al, 2015;Yobi et al, 2017). For instance, H. rhodopensis leaves start to accumulate Suc at ;60% RWC during desiccation in parallel with the significant consumption of glycolytic intermediates (Mladenov et al, 2015).…”

“…Seeds and resurrection plants use a complex array of inherent antioxidant molecules to protect themselves from abiotic stress, such as superoxide dismutases, catalases, glutathione and ascorbate peroxidases, flavonoids, and tocopherols (Illing et al, 2005;Djilianov et al, 2011;Dinakar and Bartels, 2012;Gechev et al, 2013;Sano et al, 2016;Farrant et al, 2017). In angiosperm resurrection plants, genes encoding antioxidant enzymes are either constitutively expressed or induced by drought (;50% RWC), particularly desiccation (Dinakar and Bartels, 2012;Gechev et al, 2013;Farrant et al, 2015). In the angiosperm resurrection species Ramonda nathaliae (an HDT), a time-course analysis of different antioxidant enzyme activities revealed the sequential involvement of these enzymes in dehydration and subsequent rehydration (Jovanovic et al, 2011).…”

Extremophyte adaptations to salt and water deficit stress

“…It is thus not surprising that resurrection plants have highly efficient antioxidant systems, which in turn have been proposed to be a valuable source of antioxidant potential for biotechnological applications both in plant stress tolerance as well as in the medicinal and cosmetic markets (Toldi et al 2009;Gechev et al 2014). Studies have shown that these comprise use of 'housekeeping' antioxidants (Illing et al 2005), often presenting unusual characteristics at low plant water contents (Farrant et al 2007(Farrant et al , 2012, as well as antioxidants such as 1-and 2-cys-peroxiredoxins, glyoxylase I family proteins, metallothionine-like antioxidants, oxidoreductases, several members of the aldehyde-dehydrogenases, and various polyphenols that are not typically highly expressed during dehydration of desiccation-sensitive material (reviewed in Farrant et al 2012Farrant et al , 2015Dinakar and Bartels 2013). Here, Govender et al (2016) report on a novel type II peroxiredoxin (XvPrx2) identified from the poikilochlorophyllous monocot resurrection plant Xerophyta viscosa, a species that has been relatively well characterised at the physiological and molecular levels (reviewed in Farrant et al 2015), and the genome of which has recently been sequenced .…”