|Wone, Bernard -|
|Xu, Wenxin -|
|Alexander, Danny -|
|Lining, Guo -|
|Ryals, John -|
|Cushman, John -|
Submitted to: Molecular Plant
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 10, 2012
Publication Date: March 1, 2013
Repository URL: http://handle.nal.usda.gov/10113/56969
Citation: Yobi, A., Wone, B., Xu, W., Alexander, D.C., Lining, G., Ryals, J.A., Oliver, M.J., Cushman, J.C. 2013. Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Molecular Plant. 6(2):369-385. 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, The purpose of this study is to uncover important metabolic responses related to dehydration tolerance 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 251 metabolites including 167 named (66.5%) and 84 (33.4%) unnamed compounds were characterized. Only 42 (16.7%) and 74 (29.5%) of compounds showed significantly increased or decreased abundance, respectively, indicating that most compounds were produced constitutively including highly abundant glucose, glucosylglycerol, sucrose, and trehalose. These compounds are thought to enable the plant to lose water at a slower rate than desiccation sensitive species allowing them to put in place the cellular protectants they need to survive extreme dehydration. Vanillate, a potent antioxidant was also more abundant in the hydrated state. In contrast, nitrogen-rich and gamma-glutamyl amino acids were more abundant in the dry states, suggesting that these compounds play important roles in nitrogen remobilization during rehydration or in scavenging oxidative compounds that damage cells. 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. These results offer 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: Selaginella lepidophylla is one of only a few species of spike mosses (Selaginellaceae) that have evolved desiccation tolerance (DT) or the ability to ‘resurrect’ from an air-dried state. In order to understand the metabolic basis of DT, S. lepidophylla was subjected to a five-stage, rehydration/dehydration cycle, then analyzed using non-biased, global metabolomics profiling technology based on GC/MS and UHLC/MS/MS2 platforms. A total of 251 metabolites including 167 named (66.5%) and 84 (33.4%) unnamed compounds were characterized. Only 42 (16.7%) and 74 (29.5%) of compounds showed significantly increased or decreased abundance, respectively, indicating that most compounds were produced constitutively including highly abundant glucose, glucosylglycerol, sucrose, and trehalose. Several glycolysis/ gluconeogenesis and tricarboxylic acid (TCA) cycle intermediates showed increased abundance at 100% relative water content (RWC) and 50% RWC. Vanillate, a potent antioxidant was also more abundant in the hydrated state. Many different sugar alcohols and sugar acids were more abundant in the hydrated state. These polyols likely decelerate the rate of water loss during the drying process, promote more rapid and efficient water absorption during rehydration, and stabilize protein and scavenge reactive oxygen species (ROS). In contrast, nitrogen-rich and '-glutamyl amino acids, citrulline and nucleotide catabolism products (e.g., allantoin) were more abundant in the dry states, suggesting that these compounds play important roles in nitrogen remobilization during rehydration or in ROS scavenging. UV-protective compounds such as 3-(3-hydroxyphenyl)propionate, apigenin and naringenin, were more abundant in the dry states. Most lipids were produced constitutively with the exception of choline phosphate, which likely plays a role in membrane hydration and stabilization. In contrast, several polyunsaturated fatty acids were more abundant in the hydrated states, suggesting that these compounds likely help maintain membrane fluidity during dehydration. Lastly, S. lepidophylla contained 7 unnamed compounds that displayed 2-fold or greater abundance in dry or rehydrating states, suggesting that these compounds might play adaptive roles in DT.