Persulfidation protects from oxidative stress under nonphotorespiratory conditions in Arabidopsis.
Arabidopsis
high CO2
hydrogen sulfide
persulfidation
photorespiration
reactive oxygen species
stomatal movement
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
received:
21
11
2022
accepted:
18
02
2023
medline:
14
4
2023
pubmed:
26
2
2023
entrez:
25
2
2023
Statut:
ppublish
Résumé
Hydrogen sulfide is a signaling molecule in plants that regulates essential biological processes through protein persulfidation. However, little is known about sulfide-mediated regulation in relation to photorespiration. Here, we performed label-free quantitative proteomic analysis and observed a high impact on protein persulfidation levels when plants grown under nonphotorespiratory conditions were transferred to air, with 98.7% of the identified proteins being more persulfidated under suppressed photorespiration. Interestingly, a higher level of reactive oxygen species (ROS) was detected under nonphotorespiratory conditions. Analysis of the effect of sulfide on aspects associated with non- or photorespiratory growth conditions has demonstrated that it protects plants grown under suppressed photorespiration. Thus, sulfide amends the imbalance of carbon/nitrogen and restores ATP levels to concentrations like those of air-grown plants; balances the high level of ROS in plants under nonphotorespiratory conditions to reach a cellular redox state similar to that in air-grown plants; and regulates stomatal closure, to decrease the high guard cell ROS levels and induce stomatal aperture. In this way, sulfide signals the CO
Substances chimiques
Reactive Oxygen Species
0
Arabidopsis Proteins
0
Hydrogen Sulfide
YY9FVM7NSN
Sulfides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1431-1445Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Aebi H. 1984. Catalase in vitro. In: Packer L, ed. Methods in enzymology, vol. 105. San Diego, CA, USA: Academic Press, 121-126.
Ainsworth EA. 2008. Rice production in a changing climate: a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biology 14: 1642-1650.
Álvarez C, Garcia I, Moreno I, Perez-Perez ME, Crespo JL, Romero LC, Gotor C. 2012. Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24: 4621-4634.
Aroca A, Benito JM, Gotor C, Romero LC. 2017. Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. Journal of Experimental Botany 68: 4915-4927.
Aroca A, Gotor C, Bassham DC, Romero LC. 2020. Hydrogen sulfide: from a toxic molecule to a key molecule of cell life. Antioxidants 9: 621.
Aroca A, Gotor C, Romero LC. 2018. Hydrogen sulfide signaling in plants: emerging roles of protein persulfidation. Frontiers in Plant Science 9: 1369.
Aroca A, Jurado-Flores A, Filipovic MR, Gotor C, Romero LC. 2022. Detection of protein persulfidation in plants by the dimedone switch method. Methods in Enzymology 676: 385-402.
Aroca A, Serna A, Gotor C, Romero LC. 2015. S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiology 168: 334-342.
Aroca A, Yruela I, Gotor C, Bassham DC. 2021a. Persulfidation of ATG18a regulates autophagy under ER stress in Arabidopsis. Proceedings of the National Academy of Sciences, USA 118: e2023604118.
Aroca A, Zhang J, Xie Y, Romero LC, Gotor C. 2021b. Hydrogen sulfide signaling in plant adaptations to adverse conditions: molecular mechanisms. Journal of Experimental Botany 72: 5893-5904.
Bartsch O, Mikkat S, Hagemann M, Bauwe H. 2010. An autoinhibitory domain confers redox regulation to maize glycerate kinase. Plant Physiology 153: 832-840.
Bernal-Perez LF, Prokai L, Ryu Y. 2012. Selective N-terminal fluorescent labeling of proteins using 4-chloro-7-nitrobenzofurazan: a method to distinguish protein N-terminal acetylation. Analytical Biochemistry 428: 13-15.
Bloom AJ. 2009. As carbon dioxide rises, food quality will decline without careful nitrogen management. California Agriculture 63: 67-72.
Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA. 2012. CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93: 355-367.
Bloom AJ, Burger M, Kimball BA, Pinter PJ. 2014. Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nature Climate Change 4: 477-480.
Bloom AJ, Burger M, Rubio Asensio JS, Cousins AB. 2010. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328: 899-903.
Chater C, Peng K, Movahedi M, Dunn Jessica A, Walker Heather J, Liang Y-K, McLachlan Deirdre H, Casson S, Isner Jean C, Wilson I et al. 2015. Elevated CO2-induced responses in stomata require ABA and ABA signaling. Current Biology 25: 2709-2716.
Cheeseman JM. 2006. Hydrogen peroxide concentrations in leaves under natural conditions. Journal of Experimental Botany 57: 2435-2444.
Chen J, Shang Y-T, Wang W-H, Chen X-Y, He E-M, Zheng H-L, Shangguan Z. 2016. Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. Frontiers in Plant Science 7: 1173.
Chen S, Jia H, Wang X, Shi C, Wang X, Ma P, Wang J, Ren M, Li J. 2020. Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Molecular Plant 13: 732-744.
Cheng SH, Moore B, Seemann JR. 1998. Effects of short- and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiology 116: 715-723.
Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C. 2013. Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiology and Biochemistry 70: 278-286.
Chistoserdova LV, Lidstrom ME. 1991. Purification and characterization of hydroxypyruvate reductase from the facultative methylotroph Methylobacterium extorquens AM1. Journal of Bacteriology 173: 7228-7232.
Dahal K, Vanlerberghe GC. 2018. Growth at elevated CO2 requires acclimation of the respiratory chain to support photosynthesis. Plant Physiology 178: 82-100.
Dellero Y, Mauve C, Jossier M, Hodges M. 2021. The impact of photorespiratory glycolate oxidase activity on Arabidopsis thaliana leaf soluble amino acid pool sizes during acclimation to low atmospheric CO2 concentrations. Metabolites 11: 501.
Dikalov SI, Harrison DG. 2014. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxidants & Redox Signaling 20: 372-382.
Ding H, Ma D, Huang X, Hou J, Wang C, Xie Y, Wang Y, Qin H, Guo T. 2019. Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings. Acta Physiologiae Plantarum 41: 123.
Dreyer A, Schackmann A, Kriznik A, Chibani K, Wesemann C, Vogelsang L, Beyer A, Dietz KJ. 2020. Thiol redox regulation of plant β-carbonic anhydrase. Biomolecules 10: 1125.
Dusenge ME, Duarte AG, Way DA. 2019. Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytologist 221: 32-49.
Filipovic MR. 2015. Persulfidation (S-sulfhydration) and H2S. Handbook of Experimental Pharmacology 230: 29-59.
Filipovic MR, Jovanović VM. 2017. More than just an intermediate: hydrogen sulfide signalling in plants. Journal of Experimental Botany 68: 4733-4736.
Filipovic MR, Zivanovic J, Alvarez B, Banerjee R. 2018. Chemical biology of H2S signaling through persulfidation. Chemical Reviews 118: 1253-1337.
da Fonseca-Pereira P, Souza PVL, Hou L-Y, Schwab S, Geigenberger P, Nunes-Nesi A, Timm S, Fernie AR, Thormählen I, Araújo WL et al. 2020. Thioredoxin h2 contributes to the redox regulation of mitochondrial photorespiratory metabolism. Plant, Cell & Environment 43: 188-208.
Foyer CH, Bloom AJ, Queval G, Noctor G. 2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology 60: 455-484.
Foyer CH, Noctor G. 2020. Redox homeostasis and signaling in a higher-CO2 world. Annual Review of Plant Biology 71: 157-182.
García-Calderón M, Chiurazzi M, Espuny MR, Márquez AJ. 2012. Photorespiratory metabolism and nodule function: behavior of Lotus japonicus mutants deficient in plastid glutamine synthetase. Molecular Plant-Microbe Interactions 25: 211-219.
Hu H, Rappel WJ, Occhipinti R, Ries A, Böhmer M, You L, Xiao C, Engineer CB, Boron WF, Schroeder JI. 2015. Distinct cellular locations of carbonic anhydrases mediate carbon dioxide control of stomatal movements. Plant Physiology 169: 1168-1178.
Hu J, Li Y, Liu Y, Kang DI, Wei H, Jeong BR. 2020. Hydrogen sulfide affects the root development of strawberry during plug transplant production. Agriculture 10: 12.
Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using David bioinformatics resources. Nature Protocols 4: 44-57.
Iqbal N, Fatma M, Gautam H, Umar S, Sofo A, D'Ippolito I, Khan NA. 2021. The crosstalk of melatonin and hydrogen sulfide determines photosynthetic performance by regulation of carbohydrate metabolism in wheat under heat stress. Plants 10: 1778.
Jurado-Flores A, Romero LC, Gotor C. 2021. Label-free quantitative proteomic analysis of nitrogen starvation in Arabidopsis root reveals new aspects of H2S signaling by protein persulfidation. Antioxidants 10: 508.
Karpievitch YV, Nikolic SB, Wilson R, Sharman JE, Edwards LM. 2015. Metabolomics data normalization with eigenms. PLoS ONE 9: e116221.
Karpievitch YV, Taverner T, Adkins JN, Callister SJ, Anderson GA, Smith RD, Dabney AR. 2009. Normalization of peak intensities in bottom-up MS-based proteomics using singular value decomposition. Bioinformatics 25: 2573-2580.
Kaundal A, Rojas CM, Mysore KS. 2012. Glycolate oxidase activity assay in plants. Bio-Protocol 2: e277.
Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology 25: 593-599.
Keech O, Gardeström P, Kleczkowski LA, Rouhier N. 2017. The redox control of photorespiration: from biochemical and physiological aspects to biotechnological considerations. Plant, Cell & Environment 40: 553-569.
Klie S, Nikoloski Z. 2012. The choice between MapMan and gene ontology for automated gene function prediction in plant science. Frontiers in Genetics 3: 115.
Lacuesta M, Munoz-Rueda A, Gonzalez-Muruá C, Sivak MN. 1992. Effect of phosphlnothricin (glufosinate) on photosynthesis and chlorophyll fluorescence emission by barley leaves illuminated under photorespiratory and non-photorespiratory conditions. Journal of Experimental Botany 43: 159-165.
Li J, Shi C, Wang X, Liu C, Ding X, Ma P, Wang X, Jia H. 2020. Hydrogen sulfide regulates the activity of antioxidant enzymes through persulfidation and improves the resistance of tomato seedling to copper oxide nanoparticles (CuO NPs)-induced oxidative stress. Plant Physiology and Biochemistry 156: 257-266.
Li X, Zhang G, Sun B, Zhang S, Zhang Y, Liao Y, Zhou Y, Xia X, Shi K, Yu J. 2013. Stimulated leaf dark respiration in tomato in an elevated carbon dioxide atmosphere. Scientific Reports 3: 3433.
Liu Y, Mauve C, Lamothe-Sibold M, Guérard F, Glab N, Hodges M, Jossier M. 2019. Photorespiratory serine hydroxymethyltransferase 1 activity impacts abiotic stress tolerance and stomatal closure. Plant, Cell & Environment 42: 2567-2583.
Long SP, Zhu XG, Naidu SL, Ort DR. 2006. Can improvement in photosynthesis increase crop yields? Plant, Cell & Environment 29: 315-330.
Lu Y, Wang Q-F, Li J, Xiong J, Zhou L-N, He S-L, Zhang J-Q, Chen Z-A, He S-G, Liu H. 2019. Effects of exogenous sulfur on alleviating cadmium stress in tartary buckwheat. Scientific Reports 9: 7397.
Ma X, Bai L. 2021. Elevated CO2 and reactive oxygen species in stomatal closure. Plants 10: 410.
Márquez AJ, Betti M, García-Calderón M, Pal'ove-Balang P, Díaz P, Monza J. 2005. Nitrate assimilation in Lotus japonicus. Journal of Experimental Botany 56: 1741-1749.
Mhamdi A, Noctor G. 2016. High CO2 primes plant biotic stress defences through redox-linked pathways. Plant Physiology 172: 929-942.
Mi H, Ebert D, Muruganujan A, Mills C, Albou LP, Mushayamaha T, Thomas PD. 2021. Panther v.16: a revised family classification, tree-based classification tool, enhancer regions and extensive API. Nucleic Acids Research 49: D394-D403.
Movahedi M, Zoulias N, Casson SA, Sun P, Liang YK, Hetherington AM, Gray JE, Chater CCC. 2021. Stomatal responses to carbon dioxide and light require abscisic acid catabolism in Arabidopsis. Interface Focus 11: 20200036.
Murray AJS, Blackwell RD, Joy KW, Lea PJ. 1987. Photorespiratory N donors, aminotransferase specificity and photosynthesis in a mutant of barley deficient in serine: glyoxylate aminotransferase activity. Planta 172: 106-113.
Nie G, Hendrix DL, Webber AN, Kimball BA, Long SP. 1995. Increased accumulation of carbohydrates and decreased photosynthetic gene transcript levels in wheat grown at an elevated CO2 concentration in the field. Plant Physiology 108: 975-983.
Olson KR, Gao Y, Arif F, Arora K, Patel S, DeLeon ER, Sutton TR, Feelisch M, Cortese-Krott MM, Straub KD. 2018. Metabolism of hydrogen sulfide (H2S) and production of reactive sulfur species (RSS) by superoxide dismutase. Redox Biology 15: 74-85.
Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC. 2012. S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany 63: 2089-2103.
Ortiz-Marchena MI, Albi T, Lucas-Reina E, Said FE, Romero-Campero FJ, Cano B, Ruiz MT, Romero JM, Valverde F. 2014a. Photoperiodic control of carbon distribution during the floral transition in Arabidopsis. Plant Cell 26: 565-584.
Ortiz-Marchena MI, Ruiz MT, Valverde F, Romero JM. 2014b. Determination of soluble sugars in Arabidopsis thaliana leaves by anion exchange chromatography. Bio-Protocol 4: e1317.
Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J. 2010. Regulation of plant glycine decarboxylase by S-nitrosylation and glutathionylation. Plant Physiology 152: 1514-1528.
Pérez-Delgado CM, García-Calderón M, Sánchez DH, Udvardi MK, Kopka J, Márquez AJ, Betti M. 2013. Transcriptomic and metabolic changes associated with photorespiratory ammonium accumulation in the model legume Lotus japonicus. Plant Physiology 162: 1834-1848.
Pérez-Delgado CM, Moyano TC, Garcia-Calderon M, Canales J, Gutierrez RA, Marquez AJ, Betti M. 2016. Use of transcriptomics and co-expression networks to analyze the interconnections between nitrogen assimilation and photorespiratory metabolism. Journal of Experimental Botany 67: 3095-3108.
Perez-Riverol Y, Bai J, Bandla C, García-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M et al. 2022. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Research 50: D543-D552.
Predmore BL, Lefer DJ, Gojon GJA. 2012. Hydrogen sulfide in biochemistry and medicine. Antioxidants & Redox Signaling 17: 119-140.
R Core Team. 2021. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, Mysore KS. 2012. Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24: 336-352.
Scuffi D, Nietzel T, Di Fino LM, Meyer AJ, Lamattina L, Schwarzländer M, Laxalt AM, García-Mata C. 2018. Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling. Plant Physiology 176: 2532-2542.
Scuffi D, Nunez A, Laspina N, Gotor C, Lamattina L, Garcia-Mata C. 2014. Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate ABA-dependent stomatal closure. Plant Physiology 166: 2065-2076.
Sharkey TD. 1988. Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73: 147-152.
Shen J, Zhang J, Zhou M, Zhou H, Cui B, Gotor C, Romero LC, Fu L, Yang J, Foyer CH et al. 2020. Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell 32: 1000-1017.
Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T, Chang W. 2022. David: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Research 50: W216-W221.
Somerville CR, Ogren WL. 1979. A phosphoglycolate phosphatase-deficient mutant of Arabidopsis. Nature 280: 833-836.
Supek F, Bošnjak M, Škunca N, Šmuc T. 2011. Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6: e21800.
Takahashi S, Badger MR. 2011. Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16: 53-60.
Tan B, Jin S, Sun J, Gu Z, Sun X, Zhu Y, Huo K, Cao Z, Yang P, Xin X et al. 2017. New method for quantification of gasotransmitter hydrogen sulfide in biological matrices by LC-MS/MS. Scientific Reports 7: 46278.
Taub DR. 2010. Effects of rising atmospheric concentrations of carbon dioxide on plants. Nature Education Knowledge 3: 21.
Taub DR, Wang X. 2008. Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. Journal of Integrative Plant Biology 50: 1365-1374.
Terrer C, Vicca S, Stocker BD, Hungate BA, Phillips RP, Reich PB, Finzi AC, Prentice IC. 2018. Ecosystem responses to elevated CO2 governed by plant-soil interactions and the cost of nitrogen acquisition. New Phytologist 217: 507-522.
Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MapMan: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37: 914-939.
Timm S. 2020. The impact of photorespiration on plant primary metabolism through metabolic and redox regulation. Biochemical Society Transactions 48: 2495-2504.
Timm S, Bauwe H. 2013. The variety of photorespiratory phenotypes - employing the current status for future research directions on photorespiration. Plant Biology 15: 737-747.
Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J. 2016. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nature Methods 13: 731-740.
Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, Dianes JA, Sun Z, Farrah T, Bandeira N et al. 2014. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nature Biotechnology 32: 223-226.
Voss I, Bobba S, Scheibe R, Raghavendra A. 2013. Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biology 15: 713-722.
Waadt R, Seller CA, Hsu PK, Takahashi Y, Munemasa S, Schroeder JI. 2022. Plant hormone regulation of abiotic stress responses. Nature Reviews. Molecular Cell Biology 23: 680-694.
Wang C, Deng Y, Liu Z, Liao W. 2021. Hydrogen sulfide in plants: crosstalk with other signal molecules in response to abiotic stresses. International Journal of Molecular Sciences 22: 12068.
Wang J, Liu X, Zhang X, Li L, Lam SK, Pan G. 2019. Changes in plant C, N and P ratios under elevated [CO2] and canopy warming in a rice-winter wheat rotation system. Scientific Reports 9: 5424.
Wang L, Mu X, Chen X, Han Y. 2022. Hydrogen sulfide attenuates intracellular oxidative stress via repressing glycolate oxidase activities in Arabidopsis thaliana. BMC Plant Biology 22: 98.
Zhang J, Zhou M, Ge Z, Shen J, Zhou C, Gotor C, Romero LC, Duan X, Liu X, Wu D et al. 2020. Abscisic acid-triggered guard cell l-cysteine desulfhydrase function and in situ hydrogen sulfide production contributes to heme oxygenase-modulated stomatal closure. Plant, Cell & Environment 43: 624-636.
Zhou H, Zhang J, Shen J, Zhou M, Yuan X, Xie Y. 2020. Redox-based protein persulfidation in guard cell ABA signaling. Plant Signaling & Behavior 15: 1741987.
Zhu C, Xu X, Wang D, Zhu J, Liu G, Seneweera S. 2016. Elevated atmospheric [CO2] stimulates sugar accumulation and cellulose degradation rates of rice straw. GCB Bioenergy: Bioproducts for a Sustainable Bioeconomy 8: 579-587.
Zivanovic J, Kouroussis E, Kohl JB, Adhikari B, Bursac B, Schott-Roux S, Petrovic D, Miljkovic JL, Thomas-Lopez D, Jung Y et al. 2019. Selective persulfide detection reveals evolutionarily conserved antiaging effects of S-sulfhydration. Cell Metabolism 30: 1152-1170.