Abstract
Key message
Based on the nature of the proteins that are altered in abundance, we conclude that guard cells switch their energy source from fatty acid metabolism to chloroplast activity, at the onset of dawn.
Abstract
During stomatal opening at dawn, evidence was recently presented for a breakdown and liquidation of stored triacylglycerols in guard cells to supply ATP for use in stomatal opening. However, proteome changes that happen in the guard cells during dawn were until now poorly understood. Bad accessibility to pure and intact guard cell samples can be considered as the primary reason behind this lack of knowledge. To overcome these technical constraints, epidermal guard cell samples with ruptured pavement cells were isolated at 1 h pre-dawn, 15 min post-dawn and 1 h post-dawn from Arabidopsis thaliana. Proteomic changes were analysed by ultra-performance-liquid–chromatography-mass-spectrometry. With 994 confidently identified proteins, we present the first analysis of the A. thaliana guard cell proteome that is not influenced by side effects of guard cell protoplasting. Data are available via ProteomeXchange with identifier PXD009918. By elucidating the identities of enzymes that change in abundance by the transition from dark to light, we corroborate the hypothesis that respiratory ATP production for stomatal opening results from fatty acid beta-oxidation. Moreover, we identified many proteins that were never reported in the context of guard cell biology. Among them are proteins that might play a role in signalling or circadian rhythm.
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Abbreviations
- ABA:
-
Abscisic acid
- LC–MS:
-
Liquid-chromatography–mass-spectrometry
- PCA:
-
Principal component analysis
- PC:
-
Principal component
- PRIDE:
-
PRoteomics IDEntifications database
- SEA:
-
Singular enrichment analysis
- SEACOMPARE:
-
Cross comparison of SEA
- DDT:
-
Dithiothreitol
- PLS:
-
Partial least squares analysis
- CSP41:
-
Chloroplast stem-loop binding proteins
- g s :
-
Stomatal conductance
- GO:
-
Gene ontology
- GC:
-
Guard cells
- DAVID:
-
Database for annotation, visualization and integrated discovery
- GAPCP:
-
Plastidial glyceraldehyde-3-phosphate dehydrogenases
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Acknowledgements
The authors are grateful to Kusay Arat for excellent technical assistance and the Coopération européenne dans le domaine de la recherche scientifique et technique is acknowledged for granting a STSM scholarship to Christoph-Martin Geilfus (Action FA1306). Dr. Deirdre McLachlan, University Bristol, is acknowledged for giving critical comments. We are grateful to Bastian Franzisky, University Hohenheim, for helping with guard cell preparation. This work was supported by the DFG research Grant GE 3111/1–1 to C.-M. Geilfus.
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JL designed the study, grew plants and collected epidermal peels; CMG collected proteomic data; CMG and SC contributed data analysis, SC calculated statistics; CMG, SC and JL wrote the paper.
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11103_2018_794_MOESM1_ESM.pdf
Figure S1 Majority of the proteomic changes in the guard cells (GCs) are related to lipid metabolism and ATP production during dawn. Evaluation based on the 225 proteins that decreased in abundance at 1 h after dawn when compared to the sampling at 1 h before dawn. Hierarchical tree graph of overrepresented GO terms in (A) biological process-, (B) molecular function- or (C) cellular component-category. Clustering as generated by the singular enrichment analysis (SEA) tool. Boxes represent GO terms labelled by their GO ID, term definition and statistical information. The significant terms (adjusted P ≤ 0.05) are marked with colour, while non-significant terms are shown as white boxes. The degree of colour saturation of a box is positively correlated to the enrichment level of the term. Solid, dashed, and dotted lines represent two, one and zero enriched terms at both ends connected by the line (inset in (A)). The rank direction of the graph is set from left to right (PDF 1029 KB)
11103_2018_794_MOESM4_ESM.pdf
Figure S2 Majority of the proteomic changes in the GCs are related to carbohydrate and amino acid metabolism. Evaluation based on the 84 proteins that increased in abundance at 1 h after dawn when compared to the sampling at 1 h before dawn. Hierarchical tree graph of overrepresented GO terms in (A) biological process- or (B) molecular function-category. Clustering as generated by the singular enrichment analysis (SEA) tool. Boxes represent GO terms labelled by their GO ID, term definition and statistical information. The significant term (adjusted P ≤ 0.05) are marked with colour as described in legend of figure S1. (PDF 450 KB)
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Geilfus, CM., Lan, J. & Carpentier, S. Dawn regulates guard cell proteins in Arabidopsis thaliana that function in ATP production from fatty acid beta-oxidation. Plant Mol Biol 98, 525–543 (2018). https://doi.org/10.1007/s11103-018-0794-x
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DOI: https://doi.org/10.1007/s11103-018-0794-x