Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis

Aroca, Ángeles; Benito, Juan M.; Gotor, Cecilia; Romero, Luís C.

doi:10.1093/jxb/erx294

Cited by 237 publications

(251 citation statements)

References 81 publications

(140 reference statements)

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“…In this sense, it should be point out the relevance of 6PGDH and NADP‐ME especially in situation with high content of NO and H 2 S, i.e. under stress conditions, because 6PGDH activity seems to be unaffected for these molecules whereas the NADP‐ME activity is only inhibited with higher concentration of both NO and H 2 S. Moreover, these data suggests that NADP‐ME could be modulated by S ‐nitrosation and persulfidation supporting previous reports in Arabidopsis, which indicate that this enzyme could be a target of these posttranslational modifications (Chaki et al , Aroca et al ).…”

Section: Resultssupporting

confidence: 89%

“…As in this study of NADP‐ME, using in vitro assays, we previously found that NADP‐ICDH activity in pepper fruits is inhibited in the presence of H 2 S donors. In both cases, the in vitro data are closely in line with the findings of proteomic analysis carried out in Arabidopsis (Aroca et al ). However, it is important to point out that no NADP‐dehydrogenase in the oxidative pentose phosphate pathway (OxPPP) was affected by H 2 S, indicating that the data obtained are reliable and contain no artifacts.…”

Section: Discussionsupporting

confidence: 85%

“…Thus, it has been shown that H 2 S positively regulates ascorbate peroxidase activity (Aroca et al ) but exerts an inhibitory effect on catalase activity (Corpas et al ). A recent proteomic study of A. thaliana leaves reported that both NADP‐ICDH and NADP‐ME are targets of persulfidation (Aroca et al ) [which is a posttranslational protein modification, similar to protein S ‐nitrosation (Cys‐SNO), mediated by H 2 S that affects thiol groups (Cys‐SSH)]. However, to our knowledge, no information exists on the specific effects of H 2 S on NADP‐ME activity in plant systems.…”

Section: Discussionmentioning

confidence: 99%

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Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Muñoz‐Vargas

González‐Gordo

Palma

et al. 2019

Physiologia Plantarum

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NADPH is an essential cofactor in many physiological processes. Fruit ripening is caused by multiple biochemical pathways in which, reactive oxygen and nitrogen species (ROS/RNS) metabolism is involved. Previous studies have demonstrated the differential modulation of nitric oxide (NO) and hydrogen sulfide (H2S) content during sweet pepper (Capsicum annuum L.) fruit ripening, both of which regulate NADP‐isocitrate dehydrogenase activity. To gain a deeper understanding of the potential functions of other NADPH‐generating components, we analyzed glucose‐6‐phosphate dehydrogenase (G6PDH) and 6‐phosphogluconate dehydrogenase (6PGDH), which are involved in the oxidative phase of the pentose phosphate pathway (OxPPP) and NADP‐malic enzyme (NADP‐ME). During fruit ripening, G6PDH activity diminished by 38%, while 6PGDH and NADP‐ME activity increased 1.5‐ and 2.6‐fold, respectively. To better understand the potential regulation of these NADP‐dehydrogenases by H2S, we obtained a 50–75% ammonium‐sulfate‐enriched protein fraction containing these proteins. With the aid of in vitro assays, in the presence of H2S, we observed that, while NADP‐ME activity was inhibited by up to 29–32% using 2 and 5 mM Na2S as H2S donor, G6PDH and 6PGDH activities were unaffected. On the other hand, NO donors, S‐nitrosocyteine (CysNO) and DETA NONOate also inhibited NADP‐ME activity by 35%. These findings suggest that both NADP‐ME and 6PGDH play an important role in maintaining the supply of NADPH during pepper fruit ripening and that H2S and NO partially modulate the NADPH‐generating system.

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Section: Resultssupporting

confidence: 89%

Section: Discussionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Muñoz‐Vargas

González‐Gordo

Palma

et al. 2019

Physiologia Plantarum

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“…The majority of studies identifying and examining the biochemical functions of sulfhydration are primarily constructed on cell culture models and/or with purified proteins in vitro. One of the few studies to examine the total number and identity of sulfhydrated proteins, or sulfhydrome, of an organism in vivo was completed in the plant Arabidopsis thaliana, with the discovery of 2,015 proteins, or approximately 5% of the entire proteome, as sulfhydrated (Aroca et al, 2017). However, the sulfhydrome profiles and their associated biological functions of major organs in a mammal, particularly under dietary and/or genetic conditions known to impact endogenous H2S production, have not been described.…”

Section: Introductionmentioning

confidence: 99%

Dietary restriction transforms the protein sulfhydrome in a tissue-specific and cystathionine γ-lyase-dependent manner

Bithi

Link

Wang

et al. 2019

Preprint

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One Sentence Summary: Dietary restriction altered the tissue-specific enrichment of sulfhydrated proteins and their downstream signaling pathways in liver, kidney, skeletal muscle, brain, heart, and plasma that was partly dependent on the hydrogen sulfide producing enzyme cystathionine γ-lyase.Abstract: Hydrogen sulfide (H2S) is a cytoprotective redox-active metabolite that signals through protein sulfhydration (R-SSnH). Despite the known importance of sulfhydration on relatively few identified proteins, tissue-specific sulfhydrome profiles and their associated functions are not well characterized, specifically under conditions known to modulate H2S production. We hypothesized that dietary restriction (DR), which increases lifespan and boosts endogenous H2S production, expands functional tissue-specific sulfhydromes. Here, we found that 50% DR enriched total sulfhydrated proteins in liver, kidney, muscle, and brain but decreased these in heart of adult male mice. DR promoted sulfhydration in numerous metabolic and aging-related pathways. Mice lacking the H2S producing enzyme cystathionine γ-lyase (CGL) had decreased liver and kidney protein sulfhydration and failed to functionally augment their sulfhydrome in response to DR. Overall, we defined tissue-and CGLdependent sulfhydromes and how diet transforms their makeup, underscoring the breadth for DR and H2S to impact biological processes and organismal health.

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“…Such modification usually increases the catalytic activity of the target proteins because it merely changes an -SH to an -SSH, enhancing the enzymes' chemical reactivity and possibly improving access to their respective targets [133]. However, the significance of S-sulfhydration in autophagy has not been sufficiently explored and proteomic analysis performed on wild type plants revealed the susceptibility of only four autophagy-related proteins, ATG18a, ATG3, ATG5, and ATG7, to persulfidation [134]. Incidentally, the role of H 2 S in modulating iron availability in maize seedlings grown in iron-deficient conditions was recently reported [135].…”

Section: Selective Degradation Via Autophagy In the Regulation Of Sulmentioning

confidence: 99%

The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants

Wawrzyńska

Sirko

2020

IJMS

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Plants are able to synthesize all essential metabolites from minerals, water, and light to complete their life cycle. This plasticity comes at a high energy cost, and therefore, plants need to tightly allocate resources in order to control their economy. Being sessile, plants can only adapt to fluctuating environmental conditions, relying on quality control mechanisms. The remodeling of cellular components plays a crucial role, not only in response to stress, but also in normal plant development. Dynamic protein turnover is ensured through regulated protein synthesis and degradation processes. To effectively target a wide range of proteins for degradation, plants utilize two mechanistically-distinct, but largely complementary systems: the 26S proteasome and the autophagy. As both proteasomaland autophagy-mediated protein degradation use ubiquitin as an essential signal of substrate recognition, they share ubiquitin conjugation machinery and downstream ubiquitin recognition modules. Recent progress has been made in understanding the cellular homeostasis of iron and sulfur metabolisms individually, and growing evidence indicates that complex crosstalk exists between iron and sulfur networks. In this review, we highlight the latest publications elucidating the role of selective protein degradation in the control of iron and sulfur metabolism during plant development, as well as environmental stresses. are present at certain concentrations, i.e., when the demand meets the supply. Below such levels, the demand for a nutrient exceeds the supply, so plant growth is ultimately limited by a nutritional deficiency. Conversely, an excess of any nutrient is toxic to plants and also negatively affects plant growth and development. Plants can therefore experience transitions between deficiency or toxicity zones due to changes in the availability of nutrients and growth requirements, but they can return to homeostasis so long as the response is adequate and sufficient. Such adjustments may require time, but they are crucial for plant adaptation. A significant part of this adaptation relies on selective protein degradation (Figure 1). Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 21 nutrients are present at certain concentrations, i.e., when the demand meets the supply. Below such levels, the demand for a nutrient exceeds the supply, so plant growth is ultimately limited by a nutritional deficiency. Conversely, an excess of any nutrient is toxic to plants and also negatively affects plant growth and development. Plants can therefore experience transitions between deficiency or toxicity zones due to changes in the availability of nutrients and growth requirements, but they can return to homeostasis so long as the response is adequate and sufficient. Such adjustments may require time, but they are crucial for plant adaptation. A significant part of this adaptation relies on selective protein degradation ( Figure 1). Figure 1.Regulation of nutrient deficiency stress by ubiquitination. The plant perceives nutrient deficienc...

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Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis

Abstract: Protein persulfidation in the Arabidopsis proteome is widespread and is the molecular mechanism by which hydrogen sulfide performs its signaling role.

Cited by 237 publications

References 81 publications

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Dietary restriction transforms the protein sulfhydrome in a tissue-specific and cystathionine γ-lyase-dependent manner

The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants

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Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis

Abstract: Protein persulfidation in the Arabidopsis proteome is widespread and is the molecular mechanism by which hydrogen sulfide performs its signaling role.

Cited by 237 publications

References 81 publications

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

Dietary restriction transforms the protein sulfhydrome in a tissue-specific and cystathionine γ-lyase-dependent manner

The Role of Selective Protein Degradation in the Regulation of Iron and Sulfur Homeostasis in Plants

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Product

Resources

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Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits