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Evolutionary BiologyNature Communications
Peer-reviewed journal article

Systems acclimation to osmotic stress in zygnematophyte cells

Jaccoline M. S. ZegersiD, Lukáš PfeiferiD, Tatyana DarienkoiD, Kerstin SchmittiD, Craig A DorschiD, Cäcilia F. KunziD, Gerhard H. BrausiD, Birgit ClasseniD, Oliver ValeriusiD, Jan de VriesiD

Abstract

Zygnematophytes are the closest algal relatives of land plants. They hold key information to infer how the earliest land plants overcame the barrage of terrestrial stressors, prime of which is osmotic stress. Here, we applied two osmotic stressors on a unicellular and a multicellular representative of zygnematophytes and studied their response over a 25-hour time course generating 130, 60, and 30 of transcriptomic, proteomic, and metabolomic samples combined with photophysiology, sugar analysis, immunocytochemical glycoprotein analysis, and microscopy. Our data highlight a shared protein chassis that shows divergent responses with the same outcome: successful acclimation to osmotic challenges. We establish a model of how the algal sisters of land plants can overcome a prime stressor in the terrestrial habitat and highlight components of the plant terrestrialization toolkit.

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Claude Opus 5.5 · xhigh effort · 5 Nov 2026 · from the full text of version 1 (7 Feb 2025) · CC BY 4.0

Multi-omic profiling of unicellular Mesotaenium and filamentous Zygnema under osmotic and salt stress reveals a conserved protein and cell-wall remodeling chassis driving acclimation in land plants' closest algal relatives.

Zygnematophytes are the closest algal sister group to land plants, but the protein-level and cell-wall physiology enabling them to survive terrestrial osmotic stress has remained poorly resolved. Integrating time-resolved transcriptomics, proteomics, metabolomics, and cell-wall glycan profiling across unicellular and filamentous species defines the shared molecular toolkit supporting poikilohydric osmotic acclimation.

Key results

  1. ShownOsmotic and salt stress reduce cellular water content and photosystem II efficiency in both zygnematophytes, while long-term salt exposure reveals higher resilience and multicellular filament formation in Mesotaenium.

    Exposure to 0.8 M mannitol or 0.15 M NaCl over 25 h reduced water content (P < 0.001) and Fv/Fm after 3 h (P < 0.01) with plasmolysis under 0.8 M mannitol; during prolonged 0.15 M NaCl exposure (26 d to 8 wk), Zygnema suffered cell-wall deterioration and bleached after 48 h in liquid, whereas Mesotaenium maintained growth and formed short filaments of up to 8-10 cells. · Quantitative impacts of osmotic stress in…; Conserved feedback ah2t the cell wall under…; Long term salt stress; Figure legends

  2. ShownTranscriptomic responses peak earlier than proteomic responses, converging on five conserved stress-responsive protein groups across Mesotaenium and Zygnema.

    Across 21,651 transcripts and 2,171 proteins in Mesotaenium and 9,631 transcripts and 1,713 proteins in Zygnema, >4,000 transcripts changed significantly (Padj < 0.01) with stronger fold changes at 6 hours (including shared LEA transcript upregulation) versus stronger protein changes at 25 hours, sharing upregulated AKR, EXL, XTH, and FAS1 proteins and downregulated chloroplast GTPase SVR3. · Dynamics in stress-responsive proteins and…; Figure legends

  3. ShownStress-induced transcript and protein fold changes correlate more strongly at 25 hours than at 6 hours, while FAS1 and cell-wall proteins show discordant post-transcriptional regulation.

    Relative transcript-protein log2 fold change correlations reached R = 0.63 in Mesotaenium and R = 0.39 in Zygnema (improving 1.8x on average at 25 h vs 6 h), whereas FAS1 proteins in both species, PsbS in Mesotaenium, and RPS5B and expansin in Zygnema increased in protein abundance despite lower transcript levels; absolute rank correlation in Mesotaenium was R <= 0.28 before filtering contigs <4096 bp. · Integrated analysis of transcript and protein…; Figure legends

  4. ShownTemporal transcript clustering identifies a core conserved osmotic stress module alongside opposing regulation of Hsp20 and photosynthetic PetC between the two species.

    Gaussian Mixture Model clustering resolved 12 temporal modules in Mesotaenium (670 enriched terms, p < 0.01) and 9 in Zygnema (320 enriched terms, p < 0.01), with the most interconnected stress-upregulated modules (Mesotaenium Module 9 and Zygnema Module 7) uniquely sharing AHA, sucrose synthase (SuSy), TIP, and synaptotagmin (SYT), while Hsp20 (up in Zygnema) and PetC (up in Mesotaenium) showed opposite regulation. · Temporal clustering unveils conserved osmotic…; Figure legends

  5. ShownOsmotic and ionic stress trigger embryophyte-like XTH upregulation, oligosaccharide osmolyte accumulation, and arabinogalactan protein remodeling and extracellular release.

    Phylogenetics across 16 embryophytes, 11 streptophyte algae, and 8 chlorophytes placed osmotic-stress-upregulated XTHs (GH16 subfamily 20) exclusively in Embryophyta and Zygnematophyceae; under stress, Mesotaenium accumulated di- to pentasaccharides without increasing proline, increased hydroxyproline per glycan while reducing KM1/JIM13 reactivity, and released beta-Yariv-reactive AGPs under 0.15 M NaCl. · Conserved feedback ah2t the cell wall under…; Phylogenetic analysis XTH; Figure legends

Methods, data and reproducibility

Mesotaenium endlicherianum SAG12.97 and Zygnema circumcarinatum SAG698-1b on cellophane disks were exposed to control, 0.15 M NaCl, or 0.8 M D-mannitol over 25 h for PAM fluorometry, microscopy, RNA-seq (0-25 h; Kallisto/Sleuth), LC-MS/MS proteomics (0, 6, 25 h; MaxQuant/Perseus), and LC-QTOF-MS metabolomics (3, 9 h; MZmine 3). GMM clustering, IQ-Tree phylogenetics, and beta-Yariv/ELISA glycan assays were integrated.

  • Time-course bulk RNA-seq transcriptomes of Mesotaenium endlicherianum SAG12.97 and Zygnema circumcarinatum SAG698-1b at 0, 3, 6, 9, and 25 hours under control, 0.15 M NaCl, and 0.8 M mannitol · Mesotaenium endlicherianum and Zygnema circumcarinatum · n = 130 samples (5 biological replicates per condition/timepoint; 2 excluded in QC) · PRJNA1217932
  • Paired shotgun LC-MS/MS proteomes of Mesotaenium (0, 6, 25 h) and Zygnema (6, 25 h) · Mesotaenium endlicherianum and Zygnema circumcarinatum · n = 60 samples (2,171 quantified proteins in Mesotaenium, 1,713 in Zygnema) · PXD060327
  • Paired LC-QTOF-MS methanol and MTBE lipid metabolomes of Mesotaenium at 3 and 9 hours · Mesotaenium endlicherianum · n = 30 samples
  • Light microscopy micrographs of cellular morphology and beta-Yariv extracellular staining at 25 hours · Mesotaenium endlicherianum and Zygnema circumcarinatum · n = 176 micrographs for beta-Yariv quantification · 10.5281/zenodo.14777872
Methods & tools
Kallisto, Sleuth, MaxQuant, Perseus, MZmine 3, Trinity, TransDecoder, BUSCO, InterProScan, FuncE, SWING, IQ-Tree
Reagents & environment
MZmine 3, Gryphax ver. 2.2.0.1234, BUSCO with viridiplantae_odb10 dataset, Python scipy.stats, statsmodels, Seaborn, scikit-learn, R ggplot2, MSnbase, PTXQC, igraph
Assay conditions & compute
MaxQuant proteomics searches were executed on a high-performance computing cluster
Reproducibility gaps
Data are deposited under bare accessions PRJNA1217932, PXD060327, and 10.5281/zenodo.14777872 without full http(s) URLs; custom analysis scripts and raw metabolomics files are not linked.
Limitations (3)
  • Gene regulatory network reconstruction using SWING on the temporal transcriptomic dataset retained no shared osmotic-stress edges after filtering, likely due to an insufficient number of earlier time points. · stated by the authors
  • Initial Mesotaenium proteomics runs exhibited strong SDS-PAGE gel batch effects requiring removal of samples from two gels, and absolute protein-RNA rank correlations in Mesotaenium were confounded by genes on small contigs (<4096 bp) or the plastome. · stated by the authors
  • Identifying the specific glycosyl hydrolases responsible for cleaving arabinogalactan protein side-chains was limited by incomplete functional annotations and the absence of predicted signal peptides in upregulated GH30 candidates. · stated by the authors

Who should read:Read this if you study plant terrestrialization, algal stress physiology, or cell-wall evolution and want paired time-series transcriptome, proteome, and metabolome datasets in zygnematophytes.

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