Sporobolus stapfianus: Insights into desiccation tolerance in the resurrection grasses from linking transcriptomics to metabolomics

Authors: Yobi, Abou; SCHLAUCH, KAREN - University Of Nevada; TILLET, RICHARD - University Of Nevada; YIM, WON - University Of Nevada; ESPINOZA, CATHERINE - University Of Missouri; WONE, BERNIE - University Of South Dakota; CUSHMAN, JOHN - University Of Nevada; Oliver, Melvin

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/16/2017
Publication Date: 3/28/2017
Publication URL: http://handle.nal.usda.gov/10113/5661756
Citation: Yobi, A., Schlauch, K.A., Tillet, R.L., Yim, W.C., Espinoza, C., Wone, B.W., Cushman, J.C., Oliver, M.J. 2017. Sporobolus stapfianus: Insights into desiccation tolerance in the resurrection grasses from linking transcriptomics to metabolomics. Biomed Central (BMC) Plant Biology. 17:67. https://doi.org/10.1186/s12870-017-1013-7.
DOI: https://doi.org/10.1186/s12870-017-1013-7

Interpretive Summary: A major problem facing the global efforts to improve the drought tolerance of crops to combat the changing world climate is our lack of understanding of how plants cope with the rigors of water loss from their vegetative tissues. To address this issue, we are looking at the response to dehydration and rehydration of a forage grass species, Sporobolus stapfianus, that has the capability to tolerate the complete loss of water from its leaves and root systems and revive when water is reapplied: a "resurrection" grass. We have combined the global assessment of metabolism (metabolome) with a full assessment of gene expression (transcriptome) of the plants during a dehydration and rehydration event in an attempt to get a full picture of the response. The rehydration transcriptome and metabolome are primarily geared towards the rapid return of photosynthesis, energy metabolism, protein turnover and protein synthesis during the rehydration phase. However, there are some metabolites associated with protection from oxidation (redox homeostasis)that remain elevated during rehydration, most notably the tocopherols that protect cell membranes. The analysis of the dehydration transcriptome reveals a strong concordance between gene expressiion and the associated metabolite abundance, but only in responses that are directly related to cellular and chloroplast protection during dehydration. The gene expression response also provides strong support for the involvement of cellular protection processes as exemplified by the increased expression of genes involved in cellular protection, anti-oxidant enzymes, and cell-wall modification enzymes. The gene expression response during both dehydration and rehydration offer insight into the complexity of the regulation of the tolerance mechanism of these plants and offers novel strategies for crop improvement directed at developing plants that tolerate and survive severe drought events.

Technical Abstract: Understanding the response of resurrection angiosperms to dehydration and rehydration is critical in order to decipher the mechanistic aspects of how plants cope with the rigors of water loss from their vegetative tissues. We have focused our studies on the C4 resurrection grass, Sprobolus stapfianus Gandoger, as a member of a group of important forage grasses. We have combined non-targeted metabolomics with transcriptomics, via a Nimblegen array platform, to develop an understanding of how gene expression and metabolite profiles can be linked to generate a more detailed mechanistic appreciation of the cellular response to both desiccation and rehydration. The rehydration transcriptome and metabolome are primarily geared towards the rapid return of photosynthesis, energy metabolism, protein turnover and protein synthesis during the rehydration phase. However, there are some metabolites associated with ROS protection that remain elevated during rehydration, most notably the tocopherols. The analysis of the dehydration transcriptome reveals a strong concordance between transcript abundance and the associated metabolite abundance reported earlier, but only in responses that are directly related to cellular protection during dehydration; carbohydrate metabolism and redox homeostasis. The transcriptome response also provides strong support for the involvement of cellular protection processes as exemplified by the increase in abundance of transcripts encoding late embryogenesis abundant (LEA) proteins, anti-oxidant enzymes, early light-induced proteins (ELIP) proteins, and cell-wall modification enzymes. There is little concordance between transcript and metabolite abundance for processes that do not appear to contribute directly to cellular protection, but are nonetheless important for the DT phenotype of S. stapfianus such as amino acid metabolism. The transcriptomes of both dehydration and rehydration offer insight into the complexity of the regulation of the response to these processes that involve complex signaling pathways and associated transcription factors. ABA appears to be not only principally important in the control of gene expression in the latter stages of the dehydration process approaching desiccation, but also is important during the early stages of rehydration. These findings add to the growing body of information detailing how plants tolerate and survive the severe cellular perturbations of dehydration and desiccation, respectively.