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

Author
item YOBI, ABOU - University Of Nevada
item WONE, BERNARD - University Of Nevada
item XU, WENXIN - Metabolon, Inc
item ALEXANDER, DANNY - Metabolon, Inc
item GUO, LINING - Metabolon, Inc
item RYALS, JOHN - Metabolon, Inc
item Oliver, Melvin
item CUSHMAN, JOHN - University Of Nevada

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/29/2012
Publication Date: 10/19/2012
Citation: Yobi, A., Wone, B., Xu, W., Alexander, D.C., Guo, L., Ryals, J.A., Oliver, M.J., Cushman, J.C. 2012. Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. Plant Journal. 72:983-999.

Interpretive Summary: Understanding how plant cells tolerate dehydration is a vital prerequisite for developing strategies for improving drought tolerance and at the present time little is known about this important process. This is made all the more difficult because all of our crop species have little in the way of dehydration tolerance and so we have to turn to other plant models to look for strategies to improve this aspect of drought tolerance in our commercial targets, in this case maize. In this study we have taken the desiccation tolerant spike-moss, Selaginella lepidophylla, Spike-mosses representing an ancient lineage of vascular plants in which some species have evolved or revolved desiccation tolerance (DT) and compared its metabolic response to drying to that of a desiccatyion sensitive (DS) relative, Selaginella moellendorffii. The purpose of this study is to uncover important metabolic responses related to dehydration tolernce and to compare them to our data with other species in order to determine what metabolic alterations are conserved in evolution and are thus central to dehydration tolerance. A total of 301 metabolites including 170 named (56.5%) and 131 (43.5%) unnamed compounds were characterized in both species. S. lepidophylla retained significantly higher concentrations of sucrose, monosaccharides, 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, '-glutamyl amino acids, which are linked with glutathione metabolism to detoxify reactive oxygen species and possible remobilization of nitrogen following rehydration, were markedly higher in S. lepidophylla. The later aspect of the metabolic response of the DT spike-moss appears conserved as we have previously reported the same observation in a DT grass and a DT bryophyte. This result offers a new avenue for research and the possibility of developing new strategies for drought tolerance that links dehydration tolerance and nitrogen utilization. The ultimate aim of the research is to provide maize breeders (and others) with the tools to develop drought tolerant crops that are also efficient in their use of applied nitrogen fertilizer.

Technical Abstract: Spike-mosses (Selaginellaceae) represent an ancient lineage of vascular plants in which some species have evolved or revolved desiccation tolerance (DT). A sister group comparison was conducted between a desiccation-tolerant species, Selaginella lepidophylla, and a desiccation-sensitive species, S. moellendorffii, at 100% relative water content (RWC) and 50% RWC using non-biased, global metabolomics profiling technology based on GC/MS and UHLC/MS/MS2 platforms to reveal the metabolic basis of DT. A total of 301 metabolites including 170 named (56.5%) and 131 (43.5%) unnamed compounds were characterized in both species. S. lepidophylla retained significantly higher concentrations of sucrose, monosaccharides, 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, '-glutamyl amino acids, which are linked with glutathione metabolism to detoxify reactive oxygen species and possible remobilization of nitrogen following rehydration, were markedly higher in S. lepidophylla. Markers of 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 slightly greater abundance than in S. lepidophylla. In contrast, S. lepidophylla contained 14 unnamed compounds with 5-fold or greater abundance than in S. moellendorffii suggesting that these novel compounds play critical roles in desiccation tolerance. 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 is metabolically geared towards growth and mounts only limited metabolic responses to dehydration stress.