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Title: A sister group metabolomic contrast delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus

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

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/11/2011
Publication Date: 4/5/2011
Citation: Oliver, M.J., Guo, L., Alexander, D.C., Ryals, J.A., Wone, B., Cushman, J.C. 2011. A sister group metabolomic contrast delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. The Plant Cell. 23(4):1231-1248.

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 closely related relatives to look for strategies to improve this aspect of drought tolerance in our commercial targtes, in this case maize. In this study we have taken the desiccation tolerant grass Sporobolus stapfianus and the desiccation sensitive S. pyramidalis and used them to form a "sister-group contrast", two closely related species that differ only in the target trait (dehydration tolerance) to reveal adaptive metabolic responses to dehydration using an untargeted global metabolome analysis. Samples from young leaves of fully hydrated plants and at plants at 60% relative water content (RWC) for both species, along with leaf samples from S. stapfianus at lower RWCs leading to the desiccated state, were analyzed using a combination of liquid and gas chromatography linked to mass spectrometry. Comparison of the two species prior to dehydration displayed an innate difference between the two metabolomes. Chiefly, S. stapfianus had higher levels of osmolytes, lower levels of metabolites associated with energy metabolism, and higher levels of nitrogen metabolites, suggesting that its metabolic composition is primed for dehydration stress. Further, reduction of the leaf RWC to 60%, S. stapfianus instigated a metabolic shift towards the production of many protective compounds, while S. pyramidalis failed to respond significantly. The metabolomes of S. stapfianus leaves at levels of dehydration beyond 40% RWC, which is lethal to S. pyrimidalis, are notable for a strong up-regulation of biochemical pathways associated with antioxidant production, nitrogen detoxification, and soluble sugar production . Collectively, the metabolic profiles obtained in this study uncovered a cascade of biochemical regulation critical to the survival of S. stapfianus under desiccation. Understanding the critical metabolic processes that lead to dehydration tolerance will allow plant geneticists and breeders to target key metabolic steps in maize that should rapidly lead to crop improvement strategies for drought tolerance.

Technical Abstract: Understanding how plant cells tolerate dehydration is a vital prerequisite for developing strategies for improving drought tolerance. The desiccation tolerant grass Sporobolus stapfianus and the desiccation sensitive S. pyramidalis were used to form a sister-group contrast to reveal adaptive metabolic responses to dehydration using untargeted global metabolomic analysis. Samples from young leaves of fully hydrated plants and at plants at 60% relative water content (RWC) for both species, along with leaf samples from S. stapfianus at lower RWCs leading to the desiccated state, were analyzed using a combination of liquid and gas chromatography linked to mass spectrometry. Comparison of the two species prior to dehydration displayed an innate difference between the two metabolomes. Chiefly, S. stapfianus had higher levels of osmolytes, lower levels of metabolites associated with energy metabolism, and higher levels of nitrogen metabolites, suggesting that its metabolic composition is primed for dehydration stress. Further, reduction of the leaf RWC to 60%, S. stapfianus instigated a metabolic shift towards the production of many protective compounds, while S. pyramidalis failed to respond significantly. The metabolomes of S. stapfianus leaves at levels of dehydration beyond 40% RWC, which is lethal to S. pyrimidalis, are notable for a strong up-regulation of biochemical pathways associated with antioxidant production, nitrogen detoxification, and soluble sugar production. Collectively, the metabolic profiles obtained in this study uncovered a cascade of biochemical regulation critical to the survival of S. stapfianus under desiccation.