A Horizontal View of Primary Metabolomes in Vegetative Desiccation Tolerance

Abstract

Vegetative desiccation tolerance (VDT), the ability of such tissues to survive the near complete loss of cellular water, is a rare but polyphyletic phenotype. It is a complex multifactorial trait, typified by some near universal (core) factors but with many and varied adaptations due to plant architecture, biochemistry and biotic/abiotic dynamics of particular ecological niches. The ability to enter into a quiescent biophysically stable state is what ultimately determines desiccation tolerance. Thus, understanding of the metabolomic complement of plants with VDT gives insight into the nature of survival as well as evolutionary aspects of VDT. In this study we measured the soluble carbohydrate profiles and the polar, TMS-derivatisable metabolomes of 7 phylogenetically diverse species with VDT, in contrast with 3 desiccation sensitive (DS) species, under conditions of full hydration, severe water deficit stress, and desiccated. Our study confirmed the existence of core mechanisms of VDT systems relying on either constitutively abundant trehalose, or the accumulation of raffinose family oligosaccharides and sucrose, with threshold ratios conditioned by other features of the metabolome. DS systems did not meet these ratios. Considerable chemical variations among VDT species suggest that similar stresses, e.g. photosynthetic stress, are dealt with using different chemical regimes. Furthermore, differences in timing of metabolic shifts suggest there is not a single desiccation programme, but that subprocesses are coordinated differently at different phases of drying. There is likely to be constraints on the composition of a viable dry state and how different adaptive strategies interact with the biophysical constraints of VDT.

Convergent evolution of desiccation tolerance in grasses

“…Interestingly, we observed an increase of malate to pyruvate catalysis with concomitant regeneration of NADPH, which could be related to NADPH's REDOX potential for antioxidant enzymes such as glutathione reductase. We also detected noticeable changes to carbohydrate and energy metabolism, including a shift towards the production of raffinose and stachyose under dehydrating conditions as seen in other resurrection plants (reviewed in 16 . Central carbohydrate metabolism appeared operational suggesting that at low water contents, other solvents, such as natural deep eutectic solvents within the mitochondria may facilitate glycolysis, the TCA, and electron transport 31 .…”

“…Despite more than 500 million years of evolution and divergence across extant resurrection plants, multiple biochemical and physiological mechanisms of desiccation tolerance are shared across distantly related species. For example, all surveyed resurrection plants accumulate small non-reducing sugars and other osmoprotectants to vitrify the cytoplasm and safeguard macromolecules during drying 10 . Dramatic shifts in carbohydrate and lipid metabolism as well as the protection (or in some cases degradation) of photosynthetic apparati are also observed in all resurrection plants during drying [11][12][13][14] .…”

“…All surveyed desiccation tolerant plants leverage robust anti-oxidant scavenging systems, mobilize numerous intrinsically disordered and protective proteins, and have specialized cell wall properties that maximize flexibility and mitigate the mechanical strain of shrinkage 3,14,15 . These broad features of anhydrobiosis are largely shared across organisms and tissues, but the specific metabolic pathways, regulatory networks, and activated genes are notably complex and variable among species 3,10,16 and tissues 17 .…”