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

Abou Yobi,Catherine Espinoza,Bernard W M Wone,John C Cushman,Won C Yim,Richard L Tillett,Karen A Schlauch,Melvin J Oliver

doi:10.1186/s12870-017-1013-7

Abstract

BackgroundUnderstanding 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.MethodsWe 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.ResultsThe 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.ConclusionsThe 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.

Highlights

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
The leaf rehydration metabolome The results of global unbiased metabolic profiling of rehydrating dried Desiccation tolerance (DT) young leaves of S. stapfianus, derived from the identical samples reported for the dehydration metabolome [12], are presented in Additional file 1: Table S1
This is evident in the dehydration-induced accumulation of transcripts for enzymes that synthesize carbohydrates, whose peaks in abundance just precede those of their carbohydrate metabolites (Fig. 4 and [12])

Summary

Introduction

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. Sporobolus stapfianus belongs to one of the largest and most ubiquitous families of angiosperms, the Poaceae, which includes some of the most important crop and forage species. Despite their global distribution, species in this family are generally sensitive to water deficit, and most individuals die when leaf water potentials fall below -4 MPa [1]. Some species within the family (e.g., S. stapfianus), have evolved the ability to survive desiccation or the equilibration of the water potential in their vegetative tissues to that of the surrounding air (often below -100 MPa at Relative Humidity (RH) of 50% at 20 oC). Similarities between aspects of dehydration-inducible gene expression profiles associated with vegetative DT in resurrection angiosperms and the gene expression patterns related to developmentally determined dehydration and onset of quiescence in orthodox seeds during maturation support this hypothesis [6] (and references therein)

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Discussion

Conclusion