Abstract
Soil salinity is among the abiotic stressors that threaten agriculture the most, and purslane (Portulaca oleracea L.) is a dicot species adapted to inland salt desert and saline habitats that hyper accumulates salt and has high phytoremediation potential. Many researchers consider purslane a suitable model species to study the mechanisms of plant tolerance to drought and salt stresses. Here, a robust salinity stress protocol was developed and used to characterize the morphophysiological responses of young purslane plants to salinity stress; then, leaf tissue underwent characterization by distinct omics platforms to gain further insights into its response to very high salinity stress. The salinity stress protocol did generate different levels of stress by gradients of electrical conductivity at field capacity and water potential in the saturation extract of the substrate, and the morphological parameters indicated three distinct stress levels. As expected from a halophyte species, these plants remained alive under very high levels of salinity stress, showing salt crystal-like structures constituted mainly by Na+, Cl−, and K+ on and around closed stomata. A comprehensive and large-scale metabolome and transcriptome single and integrated analyses were then employed using leaf samples. The multi-omics integration (MOI) system analysis led to a data-set of 51 metabolic pathways with at least one enzyme and one metabolite differentially expressed due to salinity stress. These data sets (of genes and metabolites) are valuable for future studies aimed to deepen our knowledge on the mechanisms behind the high tolerance of this species to salinity stress. In conclusion, besides showing that this species applies salt exclusion already in young plants to support very high levels of salinity stress, the initial analysis of metabolites and transcripts data sets already give some insights into other salt tolerance mechanisms used by this species to support high levels of salinity stress.
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Data Availability
The data-sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code Availability
Not applicable.
Abbreviations
- AE:
-
Age effect
- STS:
-
Short-term stress
- LTS:
-
Long-term stress
- FDR:
-
False discovery rate
- FC:
-
Fold change
- GSEA:
-
Gene set enrichment analysis
- HRMS:
-
High-resolution mass spectrometry
- KEGG:
-
Kyoto encyclopedia of genes and genomes
- MS:
-
Mass spectrometry
- PLS-DA:
-
Partial least squares discriminant analysis
- UHPLC:
-
Ultra-high performance liquid chromatography
- VIP:
-
Variable importance in projection
- RT:
-
Reference transcriptome
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Acknowledgements
The authors acknowledge funding to V.N.B.S., T.L.C.S., T.M.M.F. and J.C.R.N. by the Coordination for the Improvement of Higher Education Personnel (CAPES), via the Graduate Program in Plant Biotechnology at the Federal University of Lavras (UFLA) and the Graduate Program in Chemistry at the Federal University of Goiás (UFG).
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The authors disclose receipt of the following financial support for the research, authorship, and/or publication of this article: the grant (01.13.0315.00—DendePalm Project) for this study was awarded by the Brazilian Research and Innovation Agency (FINEP). The authors confirm that the funder had no influence over the study design, the content of article, or selection of this journal.
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CAFS and MTSJr designed the research; VNBS, TLCS, TMMF, APL and JAAR performed the experiments; VNBS, TLCS, JCRN, PVA, LFV, CAFS and MTSJr analyzed the data; PVA, LFV, CAFS and MTSJr drafted the manuscript. CAFS and MTSJr have revised the manuscript. All authors read and approved the final manuscript.
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Supplementary file1 Representative images (1) of the mean of variables derived from the chlorophyll fluorescence technique (saturation pulse method) in purslane plants after 1 and 4 days of submission to increasing levels of NaCl in the growing substrate. The images of Fo, Fv/Fm, and Fm' were obtained in plants adapted to the dark for 30 min, while the images of Y(II), Y(NO) and Y(NPQ) were captured after 5 min of actinic illumination at 280 μmol of light m-2 s-1. The values of the chlorophyll fluorescence parameters in the images can be compared with the color scale in the right bar. Changes over time in chlorophyll fluorescence parameters (2) for control and salinity stressed young purslane plants. The values represent an average of five replicates, and bars represent the standard error of the mean. (a) F - fluorescence intensity; (b) Fo - minimum fluorescence yield on dark-adapted plants; (c) Fm - maximum fluorescence yield on the dark-adapted plants; (d) Fv/Fm - maximum PSII quantum yield; (e) qP - proportion of open PSII; (f) qL - indicator of the PSII redox state; (g) Y(II) - PSII effective quantum yield; (h) qN - non-photochemical quenching that requires measurement of Fo; (i) NPQ - non‐photochemical quenching; (j) Y(NPQ) - regulated energy dissipation quantum yield; (k) Y(NO) - unregulated energy dissipation quantum yield; and (l) ETR - electron transport rate. The images of Fo, Fv/Fm, and Fm were obtained in plants adapted to the dark, while the images of Y(II), Y(NO) and Y(NPQ) were captured after 5 min of actinic illumination at 280 µmol of light/m2/s (JPG 693 kb)
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Supplementary file2 Scanning electron microscope (SEM) images of the leaf surface of purslane plants. (a) Control; (b) stressed plant (2.0 g NaCl) showing wrinkle due to dehydration; (c) degree of stomata opening in control compared to (d) stressed (0.5 g NaCl). Formation of salt crystals around (e) and above (f) a closed stomata in stressed plants (JPG 684 kb)
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Supplementary file3 Summary of Pathway Analysis using the Pathway Topology Analysis modules of MetaboAnalyst 5.0. The metabolome view resulted from the analysis in the Pathway Topology Analysis module using the Hypergeometric test, the relative betweenness centrality node importance measure, and the latest KEGG version of the A. thaliana pathway library. The three pathways with an FDR (False Discovery Rate) lower than 0.05 are indicated by name: The Nicotinate and nicotinamide metabolism, C5-Branched dibasic acid metabolism, and Phenylpropanoid biosynthesis pathways (JPG 141 kb)
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Supplementary file4 List of differentially expressed peaks (m.z) resulted from the Pathway Analysis using the MS Peaks to Pathway module of MetaboAnalyst 5.0. Data-set showing the pathway code, KEGG id of the matched compound, matched form, mass difference, name of the compound, correlation, t.score, p.value, FDR (False Discovery Rate), fold change - FC, Log2 (FC), and profile, in each one of the three scenarios evaluated: short-term stress – STS (control vs stress plants at 1 DAT); long-term stress 1 – LTS1 (control vs stress plants at 4 DAT); and long-term stress 2 – LTS2 (stressed plants at 1 and 4 DAT) (ODS 37 kb)
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Silva, V.N.B., da Silva, T.L.C., Ferreira, T.M.M. et al. Multi-omics Analysis of Young Portulaca oleracea L. Plants’ Responses to High NaCl Doses Reveals Insights into Pathways and Genes Responsive to Salinity Stress in this Halophyte Species. Phenomics 3, 1–21 (2023). https://doi.org/10.1007/s43657-022-00061-2
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DOI: https://doi.org/10.1007/s43657-022-00061-2