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Label-free quantitative proteomic analysis of nitrogen starvation in Arabidopsis root reveals new aspects of H2S signaling by protein persulfidation

ABSTRACT: Hydrogen sulfide (H2S)-mediated signaling pathways regulate many physiological and pathophysiological processes in mammalian and plant systems. The molecular mechanism by which hydrogen sulfide exerts its action involves the post-translational modification of cysteine residues to form a persulfidated thiol motif, and it is named protein Persulfidation. We have developed a comparative and label-free quantitative proteomic analysis approach for the detection of endogenous persulfidated proteins in Arabidopsis thaliana nitrogen-starved roots and carbon-starved leaves by using the tag-switch method. In this work, we have identified 5214 and 4691 unique proteins from root and leaf tissue, respectively, that represent almost a 13% of the entire annotate proteome in Arabidopsis. Bioinformatic analysis revealed that persulfidated cysteines are part of a wide range of biological functions, regulating important processes such as carbon metabolism, plant responses to abiotic and biotic stresses, plant growth and development, RNA translation and protein degradation. Quantitative analysis in both tissues showed important H2S-regulated metabolic processes through changes in the persulfidation level of key protein targets involved in ubiquitin-dependent protein degradation and autophagy, among others.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

TISSUE(S): Root

SUBMITTER: Riccardo Zenezini Chiozzi

LAB HEAD: Luis C. Romero

PROVIDER: PXD024061 | Pride | 2021-09-09

REPOSITORIES: pride

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			Action	DRS
	20200721_OR15_UM2_zenez001_SA_EPICXS_persulfProject_MN1.raw	Raw
	20200721_OR15_UM2_zenez001_SA_EPICXS_persulfProject_MN2.raw	Raw
	20200721_OR15_UM2_zenez001_SA_EPICXS_persulfProject_MN3.raw	Raw
	20200721_OR15_UM2_zenez001_SA_EPICXS_persulfProject_MN4.raw	Raw
	20200721_OR15_UM2_zenez001_SA_EPICXS_persulfProject_PN1.raw	Raw

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Project description:Hydrogen sulfide (H2S) is a signaling molecule that regulates essential plant processes, such as autophagy and responses to abiotic stresses. Although there is much information about the processes in which H2S is involved, the mechanism of action of H2S is still unclear. However, the posttranslational modification of cysteine residues, named persulfidation, is the main proposed mechanism. In this study, the role of H2S during drought that allows plant stress adaptation has been analyzed, with the focus on the underlying mechanism. H2S pretreatment before imposing drought on plants significantly improved phenotypic traits and decreased the content of biochemical and molecular drought stress markers. In addition, H2S regulated amino acid metabolism and repressed drought-induced degradation pathways, such as bulk autophagy and protein ubiquitination. The label-free quantitative proteomic analysis of plants growing under control and drought stress identified 887 proteins significantly different persulfidated between both conditions. Bioinformatic analyses revealed that the biological processes most enriched containing the proteins more persulfidated in drought corresponded to cellular response to oxidative stress, and hydrogen peroxide catabolism. In addition, protein degradation, abiotic stress responses, anthocyanin-containing compound biosynthetic process, and flavonoid biosynthesis were highlighted. On the contrary, the most enriched biological process containing proteins with lower levels of persulfidation in drought corresponded to the biosynthetic processes of glucosinolates and chlorophyll. Therefore, our findings emphasize the role of H2S as a promoter of enhanced tolerance to drought, enabling plants to respond more rapidly and efficiently after exposure to drought. Furthermore, the proteomic analysis supports the main role of protein persulfidation as the molecular mechanism of H2S to alleviate ROS accumulation and balance redox homeostasis under drought stress.

Project description:Hydrogen sulfide is an important signaling molecule in plants that regulates essential biological processes through protein persulfidation. Although numerous persulfidated proteins were found to be involved in photorespiration, little was known about sulfide-mediated regulation of photorespiration. Label-free quantitative proteomic analysis has revealed a high impact on the protein persulfidation level when plants grown under non-photorespiratory conditions are transferred to air, with the 97 % of total identified proteins more persulfidated under suppressed photorespiration. A detailed study of the effect of sulfide on important aspects associated with photorespiratory growth conditions has provided insight into the role of sulfide in protecting plants grown under suppressed photorespiration. In these conditions, sulfide amends the metabolic imbalance of carbon/nitrogen and restores ATP levels to concentrations similar to those in air grown conditions. Sulfide also plays an essential role in balancing the significant high level of ROS measured in plants under non-photorespiratory conditions to reach a similar cellular redox state in air-grown plants, through the regulation of antioxidative defenses. Furthermore, sulfide regulates another important characteristic resulting from suppression of photorespiration, such as the stomata closure, to decrease the high guard cell ROS levels and inducing the stomata aperture. In this way, sulfide signals the movement of the CO2-dependent stomata to achieve a scenario similar to that of plants growing under normal air conditions, in the opposite direction of the already established ABA-dependent movement of the stomata. Therefore, our findings suggest that the high persulfidation level under suppressed photorespiration reveals an essential role of sulfide signaling under these conditions, and with respect to stomatal movement, the outcome of this signaling is dependent on the growth/stress condition under study.

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Label-free quantitative proteomic analysis of nitrogen starvation in Arabidopsis root reveals new aspects of H2S signaling by protein persulfidation

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