Methyl viologen-induced changes in the Arabidopsis proteome implicate PATELLIN 4 in oxidative stress responses
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, N.I.H., Extramural
Grantová podpora
P20 GM103476
NIGMS NIH HHS - United States
P20GM103476
NIGMS NIH HHS - United States
P20GM103476
NIH HHS - United States
PubMed
37728561
PubMed Central
PMC10735431
DOI
10.1093/jxb/erad363
PII: 7278524
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, IRON SUPEROXIDE DISMUTASE 1, PATELLIN 4, chloroplast, methyl viologen, oxidative stress, photosynthesis, plasma membrane, proteomics,
- MeSH
- Arabidopsis * metabolismus MeSH
- chlorofyl a metabolismus farmakologie MeSH
- chloroplasty metabolismus MeSH
- fotosyntéza MeSH
- oxidační stres MeSH
- paraquat farmakologie metabolismus MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- proteom metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- chlorofyl a MeSH
- paraquat MeSH
- proteiny huseníčku * MeSH
- proteom MeSH
The photosynthesis-induced accumulation of reactive oxygen species in chloroplasts can lead to oxidative stress, triggering changes in protein synthesis, degradation, and the assembly/disassembly of protein complexes. Using shot-gun proteomics, we identified methyl viologen-induced changes in protein abundance in wild-type Arabidopsis and oxidative stress-hypersensitive fsd1-1 and fsd1-2 knockout mutants, which are deficient in IRON SUPEROXIDE DISMUTASE 1 (FSD1). The levels of proteins that are localized in chloroplasts and the cytoplasm were modified in all lines treated with methyl viologen. Compared with the wild-type, fsd1 mutants showed significant changes in metabolic protein and chloroplast chaperone levels, together with increased ratio of cytoplasmic, peroxisomal, and mitochondrial proteins. Different responses in proteins involved in the disassembly of photosystem II-light harvesting chlorophyll a/b binding proteins were observed. Moreover, the abundance of PATELLIN 4, a phospholipid-binding protein enriched in stomatal lineage, was decreased in response to methyl viologen. Reverse genetic studies using patl4 knockout mutants and a PATELLIN 4 complemented line indicate that PATELLIN 4 affects plant responses to oxidative stress by effects on stomatal closure.
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Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW.. 1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32, 85–100.
Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C, Santoni V.. 2016. Novel aquaporin regulatory mechanisms revealed by interactomics. Molecular and Cellular Proteomics 15, 3473–3487. PubMed PMC
Buhr F, El Bakkouri M, Valdez O, Pollmann S, Lebedev N, Reinbothe S, Reinbothe C.. 2008. Photoprotective role of NADPH:protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 105, 12629–12634. PubMed PMC
Caverzan A, Bonifacio A, Carvalho FE, et al. . 2014. The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice. Plant Science 214, 74–87. PubMed
Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ.. 2016. Learning the languages of the chloroplast: Retrograde signaling and beyond. Annual Review of Plant Biology 67, 25–53. PubMed
Che Y, Kusama S, Matsui S, Suorsa M, Nakano T, Aro EM, Ifuku K.. 2020. Arabidopsis PsbP-Like Protein 1 facilitates the assembly of the photosystem II supercomplexes and optimizes plant fitness under fluctuating light. Plant and Cell Physiology 61, 1168–1180. PubMed
Chen H, Zhang D, Guo J, Wu H, Jin M, Lu Q, Lu C, Zhang L.. 2006. A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. Plant Molecular Biology 61, 567–575. PubMed
Chu M, Li J, Zhang J, Shen S, Li C, Gao Y, Zhang S.. 2018. AtCaM4 interacts with a Sec14-like protein, PATL1, to regulate freezing tolerance in Arabidopsis in a CBF-independent manner. Journal of Experimental Botany 69, 5241–5253. PubMed
Cramer WA, Zhang H.. 2006. Consequences of the structure of the cytochrome b6f complex for its charge transfer pathways. Biochimica et Biophysica Acta – Bioenergetics 1757, 339–345. PubMed
de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L.. 2011. Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. The Plant Cell 23, 2659–2679. PubMed PMC
Dietz KJ, Hell R.. 2015. Thiol switches in redox regulation of chloroplasts: balancing redox state, metabolism and oxidative stress. Biological Chemistry 396, 483–494. PubMed
Drake PL, Froend RH, Franks PJ.. 2013. Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. Journal of Experimental Botany 64, 495–505. PubMed PMC
Dvořák P, Krasylenko Y, Ovečka M, Basheer J, Zapletalová V, Šamaj J, Takáč T.. 2021. In vivo light-sheet microscopy resolves localisation patterns of FSD1, a superoxide dismutase with function in root development and osmoprotection. Plant, Cell and Environment 44, 68–87. PubMed
Ehonen S, Yarmolinsky D, Kollist H, Kangasjärvi J.. 2019. Reactive oxygen species, photosynthesis, and environment in the regulation of stomata. Antioxidants and Redox Signaling 30, 1220–1237. PubMed
Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM.. 2017. Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nature Communications 8, 49. PubMed PMC
Fristedt R, Vener AV.. 2011. High light induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-Dependent phosphorylation of CP29. PLoS One 6, e24565. PubMed PMC
Gollan PJ, Tikkanen M, Aro EM.. 2015. Photosynthetic light reactions: integral to chloroplast retrograde signalling. Current Opinion in Plant Biology 27, 180–191. PubMed
Grondin A, Rodriguez O, Verdoucq L, Merlot S, Leonhardt N, Maurel C.. 2015. Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. The Plant Cell 27, 1945–1954. PubMed PMC
Haldrup A, Simpson DJ, Scheller HV.. 2000. Down-regulation of the PSI-F subunit of photosystem I (PSI) in Arabidopsis thaliana. Journal of Biological Chemistry 275, 31211–31218. PubMed
Hornbergs J, Montag K, Loschwitz J, et al. . 2023. SEC14-GOLD protein PATELLIN2 binds IRON-REGULATED TRANSPORTER1 linking root iron uptake to vitamin E. Plant Physiology 192, 504–526. PubMed PMC
Hsu P-K, Takahashi Y, Munemasa S, Merilo E, Laanemets K, Waadt R, Pater D, Kollist H, Schroeder JI.. 2018. Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase. Proceedings of the National Academy of Sciences, USA 115, E9971–E9980. PubMed PMC
Huang J, Niazi AK, Young D, et al. . 2018. Self-protection of cytosolic malate dehydrogenase against oxidative stress in Arabidopsis. Journal of Experimental Botany 69, 3491–3505. PubMed
Huang J, Zhao X, Chory J.. 2019. The Arabidopsis transcriptome responds specifically and dynamically to high light stress. Cell Reports 29, 4186–4199.e3. PubMed PMC
Ifuku K. 2014. The PsbP and PsbQ family proteins in the photosynthetic machinery of chloroplasts. Plant Physiology and Biochemistry 81, 108–114. PubMed
Ifuku K, Endo T, Shikanai T, Aro EM.. 2011. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant and Cell Physiology 52, 1560–1568. PubMed
Inagaki N. 2022. Processing of D1 protein: a mysterious process carried out in thylakoid lumen. International Journal of Molecular Sciences 23, 2520. PubMed PMC
Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K, Sato F.. 2007. Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiology 145, 668–679. PubMed PMC
Järvi S, Isojärvi J, Kangasjärvi S, Salojärvi J, Mamedov F, Suorsa M, Aro EM.. 2016. Photosystem II repair and plant immunity: lessons learned from Arabidopsis mutant lacking the THYLAKOID LUMEN PROTEIN 18.3. Frontiers in Plant Science 7, 405. PubMed PMC
Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W.. 2009. The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiology 151, 1790–1801. PubMed PMC
Kato Y, Sakamoto W.. 2009. Protein quality control in chloroplasts: a current model of D1 protein degradation in the photosystem II repair cycle. Journal of Biochemistry 146, 463–469. PubMed
Kessler F, Schnell D.. 2009. Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Current Opinion in Cell Biology 21, 494–500. PubMed
Krynická V, Shao S, Nixon PJ, Komenda J.. 2015. Accessibility controls selective degradation of photosystem II subunits by FtsH protease. Nature Plants 1, 15168. PubMed
Li L, Aro EM, Millar AH.. 2018. Mechanisms of photodamage and protein turnover in photoinhibition. Trends in Plant Science 23, 667–676. PubMed
Li L, Nelson CJ, Trösch J, Castleden I, Huang S, Millar AH.. 2017. Protein degradation rate in Arabidopsis thaliana leaf growth and development. The Plant Cell 29, 207–228. PubMed PMC
Lois LM, Lima CD, Chua N-H.. 2003. Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. The Plant Cell 15, 1347–1359. PubMed PMC
López-Calcagno PE, Howard TP, Raines CA.. 2014. The CP12 protein family: a thioredoxin-mediated metabolic switch? Frontiers in Plant Science 5, 9. PubMed PMC
Mao J, Chi W, Ouyang M, He B, Chen F, Zhang L.. 2015. PAB is an assembly chaperone that functions downstream of chaperonin 60 in the assembly of chloroplast ATP synthase coupling factor 1. Proceedings of the National Academy of Sciences, USA 112, 4152–4157. PubMed PMC
McAinsh MR, Clayton H, Mansfield TA, Hetherington AM.. 1996. Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiology 111, 1031–1042. PubMed PMC
Melicher P, Dvořák P, Krasylenko Y, Shapiguzov A, Kangasjärvi J, Šamaj J, Takáč T.. 2022a. Arabidopsis iron superoxide dismutase FSD1 protects against methyl viologen-induced oxidative stress in a copper-dependent manner. Frontiers in Plant Science 13, 823561. PubMed PMC
Melicher P, Dvořák P, Šamaj J, Takáč T.. 2022b. Protein-protein interactions in plant antioxidant defense. Frontiers in Plant Science 13, 1035573. PubMed PMC
Murashige T, Skoog F.. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
Muthuramalingam M, Matros A, Scheibe R, Mock HP, Dietz KJ.. 2013. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science 4, 54. PubMed PMC
Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, Aro EM, Nam HG, Lee CH.. 2013. Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Letters 587, 3372–3381. PubMed
Nelson CJ, Alexova R, Jacoby RP, Millar AH.. 2014. Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiology 166, 91–108. PubMed PMC
Nestler H, Groh KJ, Schönenberger R, Eggen RIL, Suter MJF.. 2012. Linking proteome responses with physiological and biochemical effects in herbicide-exposed Chlamydomonas reinhardtii. Journal of Proteomics 75, 5370–5385. PubMed
Ozfidan-Konakci C, Yildiztugay E, Arikan B, Elbasan F, Alp FN, Kucukoduk M.. 2023. Hydrogen sulfide protects damage from methyl viologen-mediated oxidative stress by improving gas exchange, fluorescence kinetics of photosystem II, and antioxidant system in Arabidopsis thaliana. Journal of Plant Growth Regulation 42, 1031–1050.
Parcerisa IL, Rosano GL, Ceccarelli EA.. 2020. Biochemical characterization of ClpB3, a chloroplastic disaggregase from Arabidopsis thaliana. Plant Molecular Biology 104, 451–465. PubMed
Perez-Riverol Y, Csordas A, Bai J, et al. . 2019. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Research 47, D442–D450. PubMed PMC
Peterman TK, Ohol YM, McReynolds J, Luna EJ.. 2004. Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiology 136, 3080–3094. PubMed PMC
Qi Y, Armbruster U, Schmitz-Linneweber C, Delannoy E, de Longevialle AF, Rühle T, Small I, Jahns P, Leister D.. 2012. Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts. Journal of Experimental Botany 63, 1251–1270. PubMed PMC
Qian H, Chen W, Sun L, Jin Y, Liu W, Fu Z.. 2009. Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicology 18, 537–543. PubMed
Rutschow H, Ytterberg AJ, Friso G, Nilsson R, van Wijk KJ.. 2008. Quantitative proteomics of a chloroplast SRP54 sorting mutant and its genetic interactions with CLPC1 in Arabidopsis. Plant Physiology 148, 156–175. PubMed PMC
Sakamoto W, Zaltsman A, Adam Z, Takahashi Y.. 2003. Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. The Plant Cell 15, 2843–2855. PubMed PMC
Schneider CA, Rasband WS, Eliceiri KW.. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675. PubMed PMC
Selinski J, Scheibe R.. 2019. Malate valves: old shuttles with new perspectives. Plant Biology 21, 21–30. PubMed PMC
Sierla M, Rahikainen M, Salojärvi J, Kangasjärvi J, Kangasjärvi S.. 2013. Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxidants and Redox Signaling 18, 2220–2239. PubMed
Sirpiö S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM.. 2007. TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle. Biochemical Journal 406, 415–425. PubMed PMC
Steen CJ, Morris JM, Short AH, Niyogi KK, Fleming GR.. 2020. Complex roles of PsbS and xanthophylls in the regulation of nonphotochemical quenching in Arabidopsis thaliana under fluctuating light. Journal of Physical Chemistry B 124, 10311–10325. PubMed
Su PH, Li H.. 2010. Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. The Plant Cell 22, 1516–1531. PubMed PMC
Suzuki T, Matsushima C, Nishimura S, Higashiyama T, Sasabe M, Machida Y.. 2016. Identification of phosphoinositide-binding protein PATELLIN2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis. Plant and Cell Physiology 57, 1744–1755. PubMed PMC
Takáč T, Křenek P, Komis G, et al. . 2021. TALEN-based HvMPK3 knockout attenuates proteome and root hair phenotypic responses to flg22 in barley. Frontiers in Plant Science 12, 666229. PubMed PMC
Takáč T, Šamajová O, Pechan T, Luptovčiak I, Šamaj J.. 2017. Feedback microtubule control and microtubule-actin cross-talk in Arabidopsis revealed by integrative proteomic and cell biology analysis of KATANIN 1 mutants. Molecular and Cellular Proteomics 16, 1591–1609. PubMed PMC
Takechi K, Sodmergen null, Murata M, Motoyoshi F, Sakamoto W.. 2000. The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant and Cell Physiology 41, 1334–1346. PubMed
Taylor NL, Tan YF, Jacoby RP, Millar AH.. 2009. Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. Journal of Proteomics 72, 367–378. PubMed
Tejos R, Rodriguez-Furlán C, Adamowski M, Sauer M, Norambuena L, Friml J.. 2018. PATELLINS are regulators of auxin-mediated PIN1 relocation and plant development in Arabidopsis thaliana. Journal of Cell Science 131, jcs204198. PubMed
Torres-Romero D, Gómez-Zambrano A, Jesús Serrato A, Sahrawy M, Mérida A.. 2021. Arabidopsis fibrillin 1-2 subfamily exerts their functions via specific protein-protein interactions. Journal of Experimental Botany 73, 903–914. PubMed PMC
Wang C, Hu H, Qin X, Zeise B, Xu D, Rappel WJ, Boron WF, Schroeder JI.. 2016. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. The Plant Cell 28, 568–582. PubMed PMC
Wang D, Portis AR.. 2007. A novel nucleus-encoded chloroplast protein, PIFI, is involved in NAD(P)H dehydrogenase complex-mediated chlororespiratory electron transport in Arabidopsis. Plant Physiology 144, 1742–1752. PubMed PMC
Wei L, Guo J, Ouyang M, Sun X, Ma J, Chi W, Lu C, Zhang L.. 2010. LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. Journal of Biological Chemistry 285, 21391–21398. PubMed PMC
Xiong Y, Contento AL, Nguyen PQ, Bassham DC.. 2007. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiology 143, 291–299. PubMed PMC
Yi X, Hargett SR, Frankel LK, Bricker TM.. 2009. The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana. FEBS Letters 583, 2142–2147. PubMed
Yu J, Li Y, Qin Z, Guo S, Li Y, Miao Y, Song C, Chen S, Dai S.. 2020. Plant chloroplast stress response: insights from thiol redox proteomics. Antioxidants and Redox Signaling 33, 35–57. PubMed
Zhou H, Wang C, Tan T, Cai J, He J, Lin H.. 2018. Patellin1 negatively modulates salt tolerance by regulating PM Na+/H+ antiport activity and cellular redox homeostasis in Arabidopsis. Plant and Cell Physiology 59, 1630–1642. PubMed