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

BMC Plant Biol. 2017 Mar 28;17(1):67. doi: 10.1186/s12870-017-1013-7.

Abstract

Background: Understanding the response of resurrection angiosperms to dehydration and rehydration is critical for deciphering the mechanisms of how plants cope with the rigors of water loss from their vegetative tissues. We have focused our studies on the C4 resurrection grass, Sporobolus stapfianus Gandoger, as a member of a group of important forage grasses.

Methods: 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.

Results: 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 increases in the 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 such as amino acid metabolism that do not appear to contribute directly to cellular protection, but are nonetheless important for the desiccation tolerant phenotype of S. stapfianus.

Conclusions: The transcriptomes of both dehydration and rehydration offer insight into the complexity of the regulation of responses to these processes that involve complex signaling pathways and associated transcription factors. ABA appears to be important in the control of gene expression in both the latter stages of the dehydration and 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, desiccation, and rehydration.

Keywords: Abiotic stress; Dehydration stress; Gene expression; Rehydration; Resurrection plants; Sporobolus stapfianus.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Abscisic Acid / metabolism
  • Antioxidants / metabolism
  • Carbohydrate Metabolism / genetics
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • Dehydration
  • Energy Metabolism / genetics
  • Enzymes / genetics
  • Enzymes / metabolism
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Plant*
  • Metabolomics / methods
  • Plant Leaves / physiology
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • Poaceae / genetics
  • Poaceae / metabolism
  • Poaceae / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Antioxidants
  • Enzymes
  • Plant Proteins
  • Transcription Factors
  • Abscisic Acid