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Enhanced Desiccation Tolerance in Mature Cultures of the Streptophytic Green Alga Zygnema circumcarinatum Revealed by Transcriptomics.

ABSTRACT: Desiccation tolerance is commonly regarded as one of the key features for the colonization of terrestrial habitats by green algae and the evolution of land plants. Extensive studies, focused mostly on physiology, have been carried out assessing the desiccation tolerance and resilience of the streptophytic genera Klebsormidium and Zygnema. Here we present transcriptomic analyses of Zygnema circumcarinatum exposed to desiccation stress. Cultures of Z. circumcarinatum grown in liquid medium or on agar plates were desiccated at ?86% relative air humidity until the effective quantum yield of PSII [Y(II)] ceased. In general, the response to dehydration was much more pronounced in Z. circumcarinatum cultured in liquid medium for 1 month compared with filaments grown on agar plates for 7 and 12 months. Culture on solid medium enables the alga to acclimate to dehydration much better and an increase in desiccation tolerance was clearly correlated to increased culture age. Moreover, gene expression analysis revealed that photosynthesis was strongly repressed upon desiccation treatment in the liquid culture while only minor effects were detected in filaments cultured on agar plates for 7 months. Otherwise, both samples showed induction of stress protection mechanisms such as reactive oxygen species scavenging (early light-induced proteins, glutathione metabolism) and DNA repair as well as the expression of chaperones and aquaporins. Additionally, Z. circumcarinatum cultured in liquid medium upregulated sucrose-synthesizing enzymes and strongly induced membrane modifications in response to desiccation stress. These results corroborate the previously described hardening and associated desiccation tolerance in Zygnema in response to seasonal fluctuations in water availability.

SUBMITTER: Rippin M

PROVIDER: S-EPMC5722205 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Enhanced Desiccation Tolerance in Mature Cultures of the Streptophytic Green Alga Zygnema circumcarinatum Revealed by Transcriptomics.

Rippin Martin M Becker Burkhard B Holzinger Andreas A

Plant & cell physiology 20171201 12

Desiccation tolerance is commonly regarded as one of the key features for the colonization of terrestrial habitats by green algae and the evolution of land plants. Extensive studies, focused mostly on physiology, have been carried out assessing the desiccation tolerance and resilience of the streptophytic genera Klebsormidium and Zygnema. Here we present transcriptomic analyses of Zygnema circumcarinatum exposed to desiccation stress. Cultures of Z. circumcarinatum grown in liquid medium or on a ...[more]

PMID: 29036673

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Project description:BACKGROUND:Water loss has significant effects on physiological performance and survival rates of algae. However, despite the prominent presence of aeroterrestrial algae in terrestrial habitats, hardly anything is known about the molecular events that allow aeroterrestrial algae to survive harsh environmental conditions. We analyzed the transcriptome and physiology of a strain of the alpine aeroterrestrial alga Klebsormidium crenulatum under control and strong desiccation-stress conditions. PRINCIPAL FINDINGS:For comparison we first established a reference transcriptome. The high-coverage reference transcriptome includes about 24,183 sequences (1.5 million reads, 636 million bases). The reference transcriptome encodes for all major pathways (energy, carbohydrates, lipids, amino acids, sugars), nearly all deduced pathways are complete or missing only a few transcripts. Upon strong desiccation, more than 7000 transcripts showed changes in their expression levels. Most of the highest up-regulated transcripts do not show similarity to known viridiplant proteins, suggesting the existence of some genus- or species-specific responses to desiccation. In addition, we observed the up-regulation of many transcripts involved in desiccation tolerance in plants (e.g. proteins similar to those that are abundant in late embryogenesis (LEA), or proteins involved in early response to desiccation ERD), and enzymes involved in the biosynthesis of the raffinose family of oligosaccharides (RFO) known to act as osmolytes). Major physiological shifts are the up-regulation of transcripts for photosynthesis, energy production, and reactive oxygen species (ROS) metabolism, which is supported by elevated cellular glutathione content as revealed by immunoelectron microscopy as well as an increase in total antiradical power. However, the effective quantum yield of Photosystem II and CO2 fixation decreased sharply under the applied desiccation stress. In contrast, transcripts for cell integrative functions such as cell division, DNA replication, cofactor biosynthesis, and amino acid biosynthesis were down-regulated. SIGNIFICANCE:This is the first study investigating the desiccation transcriptome of a streptophyte green alga. Our results indicate that the cellular response is similar to embryophytes, suggesting that embryophytes inherited a basic cellular desiccation tolerance from their streptophyte predecessors.

Project description:The osmotic potential and effects of plasmolysis on photosynthetic oxygen evolution and chlorophyll fluorescence were studied in two Arctic Zygnema sp. (strain B, strain G) and two Antarctic Zygnema sp. (strain E, strain D). Antarctic strain D was newly characterized by rbcL sequence analysis in the present study. The two Antarctic strains, D and E, are most closely related and may represent different isolates of the same species, in contrast, strain B and G are separate lineages. Incipient plasmolysis in the cells was determined by light microscopy after incubating cells in sorbitol solutions ranging between 200 mM and 1000 mM sorbitol for 3, 6 and 24h. In Zygnema strain B and G incipient plasmolysis occurred at ~600 mM sorbitol solution (720 mOsmol kg(-1), ?=-1.67 MPa) and in strains D and E at ~300 mM (318 mOsmol kg(-1), ?=-0.8 MPa) sorbitol solution. Hechtian strands were visualized in all plasmolysed cells, which is particularly interesting, as these cells lack pores or plasmodesmata. Ultrastructural changes upon osmotic stress were a retraction of the condensed cytoplasm from the cell walls, damages to chloroplast and mitochondrial membranes, increasing numbers of plastoglobules in the chloroplasts and membrane enclosed particles in the extraplasmatic space. Maximum photosynthetic rates (P(max)) in light saturated range were between 145.5 ?mol O(2) h(-1)mg(-1)Chl a in Zygnema G and 752.9 ?mol O(2) h(-1)mg(-1)Chl a in Zygnema E. After incubation in 800 mM sorbitol for 3h P(max) decreased to the following percentage of the initial values: B: 16.3%, D: 16.8%, E: 26.1% and G: 35.0%. Osmotic stress (800 mM sorbitol) decreased maximum photochemical quantum yield of photosystem II (F(v)/F(m)) when compared to controls. Maximum values of relative electron transport rates of photosystem II (rETR(max)) decreased after incubation in 400 mM sorbitol in Zygnema D and E, while they decreased in Zygnema B and G only after incubation in 800 mM sorbitol. The kinetics of the rETR curves were similar for the Arctic strains Zygnema B and G, but distinct from the Antarctic strains Zygnema D and E, which were similar when compared with each other. This suggests that the investigated Arctic Zygnema sp. strains might be better adapted to tolerate osmotic water stress than the investigated strains from the Antarctic.

Project description: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.

Dataset Information

Enhanced Desiccation Tolerance in Mature Cultures of the Streptophytic Green Alga Zygnema circumcarinatum Revealed by Transcriptomics.

Publications

Enhanced Desiccation Tolerance in Mature Cultures of the Streptophytic Green Alga Zygnema circumcarinatum Revealed by Transcriptomics.

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