Comparative metabolic profiling between desiccation‐sensitive and desiccation‐tolerant species of Selaginella reveals insights into the resurrection trait

Abstract

SUMMARYSpike mosses (Selaginellaceae) represent an ancient lineage of vascular plants in which some species have evolved desiccation tolerance (DT). A sister-group contrast to reveal the metabolic basis of DT was conducted between a desiccation-tolerant species, Selaginella lepidophylla, and a desiccation-sensitive species, Selaginella moellendorffii, at 100% relative water content (RWC) and 50% RWC using non-biased, global metabolomics profiling technology, based on GC/MS and UHLC/MS/MS 2 platforms. A total of 301 metabolites, including 170 named (56.5%) and 131 (43.5%) unnamed compounds, were characterized across both species. S. lepidophylla retained significantly higher abundances of sucrose, mono-and polysaccharides, and sugar alcohols than did S. moellendorffii. Aromatic amino acids, the well-known osmoprotectant betaine and flavonoids were also more abundant in S. lepidophylla. Notably, levels of c-glutamyl amino acid, linked with glutathione metabolism in the detoxification of reactive oxygen species, and with possible nitrogen remobilization following rehydration, were markedly higher in S. lepidophylla. Markers for lipoxygenase activity were also greater in S. lepidophylla, especially at 50% RWC. S. moellendorffii contained more than twice the number of unnamed compounds, with only a slightly greater abundance than in S. lepidophylla. In contrast, S. lepidophylla contained 14 unnamed compounds of fivefold or greater abundance than in S. moellendorffii, suggesting that these compounds might play critical roles in DT. Overall, S. lepidophylla appears poised to tolerate desiccation in a constitutive manner using a wide range of metabolites with some inducible components, whereas S. moellendorffii mounts only limited metabolic responses to dehydration stress.

The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon

“…Metabolome comparisons between these two grass species when both were fully hydrated, found higher concentrations of osmotically-active solute (osmoregulation and protection roles) and of nitrogen metabolites (retranslocation into young tissue and reserve roles) in Sporobolus stapfianus than in the sensitive species (Oliver et al 2011a). Similar observations have recently been reported for a sister group comparison between Selaginella lepidophylla and Selaginella moellendorffii (Yobi et al 2012).…”

“…(Iturriaga et al 2000). However, recent work has demonstrated that trehalose also accumulates to higher levels in the desiccation sensitive species Selaginella moellendorffii than it does in Selaginella lepidophylla under the same conditions (Yobi et al 2012). Thus it appears that trehalose accumulation is not necessarily required for desiccation tolerance and indeed in the same study it became clear that sucrose, as in other resurrection species, is the main protectant.…”

“…These compounds are postulated to be involved in the replenishment of 5-oxyproline in the glutathione biosynthetic pathway but their exact role in desiccation tolerance is not known. That the accumulation of these compounds has significance in desiccation tolerance and its evolutionary journey is implied by the fact that these compounds also accumulate in the later stages of drying of Selaginella (Oliver et al 2011a;Yobi et al 2012) and the moss Tortula ruralis (Oliver et al 2011a). Chaperonins (some of which are stress-inducible) including some heat shock proteins (HSP) that associate with and protect other protein species against denaturation are found from the algae to angiosperm resurrection plants Boea hygrometrica F. Muell.…”

Lipogenesis and Redox Balance in Nitrogen-Fixing Pea Bacteroids

“…For metabolite profiling, identification of known chemical entities was based on comparisons to metabolomic library entries of purified standards as previously described (33,34). Statistical analysis was performed using the software packages Array Studio (Omicsoft) and R (http://www .r-project.org/).…”

Bacterial Biosensors for in Vivo Spatiotemporal Mapping of Root Secretion

“…Samples were analyzed on a Thermo Finnigan Trace DSQ fast-scanning single-quadrupole gas chromatograph-mass spectrometer using electron-impact ionization. For metabolite profiling, the identification of known chemical entities was based on comparison with metabolomic library entries of purified standards as described previously (Evans et al, 2009;Yobi et al, 2012).…”