Proteome analysis of peroxisomes from dark‐treated senescent Arabidopsis leaves
dc.contributor.author | Pan, Ronghui | |
dc.contributor.author | Reumann, Sigrun | |
dc.contributor.author | Lisik, Piotr | |
dc.contributor.author | Tietz, Stefanie | |
dc.contributor.author | Olsen, Laura J. | |
dc.contributor.author | Hu, Jianping | |
dc.date.accessioned | 2018-11-20T15:36:22Z | |
dc.date.available | 2020-01-06T16:40:59Z | en |
dc.date.issued | 2018-11 | |
dc.identifier.citation | Pan, Ronghui; Reumann, Sigrun; Lisik, Piotr; Tietz, Stefanie; Olsen, Laura J.; Hu, Jianping (2018). "Proteome analysis of peroxisomes from dark‐treated senescent Arabidopsis leaves." Journal of Integrative Plant Biology 60(11): 1028-1050. | |
dc.identifier.issn | 1672-9072 | |
dc.identifier.issn | 1744-7909 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/146507 | |
dc.description.abstract | Peroxisomes compartmentalize a dynamic suite of biochemical reactions and play a central role in plant metabolism, such as the degradation of hydrogen peroxide, metabolism of fatty acids, photorespiration, and the biosynthesis of plant hormones. Plant peroxisomes have been traditionally classified into three major subtypes, and in‐depth mass spectrometry (MS)‐based proteomics has been performed to explore the proteome of the two major subtypes present in green leaves and etiolated seedlings. Here, we carried out a comprehensive proteome analysis of peroxisomes from Arabidopsis leaves given a 48‐h dark treatment. Our goal was to determine the proteome of the third major subtype of plant peroxisomes from senescent leaves, and further catalog the plant peroxisomal proteome. We identified a total of 111 peroxisomal proteins and verified the peroxisomal localization for six new proteins with potential roles in fatty acid metabolism and stress response by in vivo targeting analysis. Metabolic pathways compartmentalized in the three major subtypes of peroxisomes were also compared, which revealed a higher number of proteins involved in the detoxification of reactive oxygen species in peroxisomes from senescent leaves. Our study takes an important step towards mapping the full function of plant peroxisomes.Peroxisomes are important to development and stress response. Here we report a comprehensive proteome analysis of peroxisomes from Arabidopsis leaves treated with extended darkness, which identified new proteins with potential roles in fatty acid metabolism and stress response, thus taking an important step towards defining the full function of plant peroxisomes. | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.title | Proteome analysis of peroxisomes from dark‐treated senescent Arabidopsis leaves | |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Biology | |
dc.subject.hlbtoplevel | Science | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/146507/1/jipb12670-sup-0001-SuppFigs-S1.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/146507/2/jipb12670.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/146507/3/jipb12670_am.pdf | |
dc.identifier.doi | 10.1111/jipb.12670 | |
dc.identifier.source | Journal of Integrative Plant Biology | |
dc.identifier.citedreference | Quan S, Yang P, Cassin‐Ross G, Kaur N, Switzenberg R, Aung K, Li J, Hu J ( 2013 ) Proteome analysis of peroxisomes from etiolated arabidopsis seedlings identifies a peroxisomal protease involved in ‐oxidation and development. Plant Physiol 163: 1518 – 1538 | |
dc.identifier.citedreference | Reumann S ( 2011 ) Toward a definition of the complete proteome of plant peroxisomes: Where experimental proteomics must be complemented by bioinformatics. Proteomics 11: 1764 – 1779 | |
dc.identifier.citedreference | Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O ( 2007 ) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19: 3170 – 3193 | |
dc.identifier.citedreference | Reumann S, Chowdhary G, Lingner T ( 2016 ) Characterization, prediction and evolution of plant peroxisomal targeting signals type 1 (PTS1s). Biochim Biophys Acta ‐ Mol Cell Res 1863: 790 – 803 | |
dc.identifier.citedreference | Reumann S, Ma C, Lemke S, Babujee L ( 2004 ) AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol 136: 2587 – 2608 | |
dc.identifier.citedreference | Reumann S, Quan S, Aung K, Yang P, Manandhar‐Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber APM, Olsen LJ, Hu J ( 2009 ) In‐depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiol 150: 125 – 143 | |
dc.identifier.citedreference | Ribeiro CW, Korbes AP, Garighan JA, Jardim‐Messeder D, Carvalho FEL, Sousa RHV, Caverzan A, Teixeira FK, Silveira JAG, Margis‐Pinheiro M ( 2017 ) Rice peroxisomal ascorbate peroxidase knockdown affects ROS signaling and triggers early leaf senescence. Plant Sci 263: 55 – 65 | |
dc.identifier.citedreference | Rodríguez‐Serrano M, Romero‐Puertas MC, Sanz‐Fernández M, Hu J, Sandalio LM ( 2016 ) Peroxisomes extend peroxules in a fast response to stress via a reactive oxygen species‐mediated induction of the peroxin PEX11a. Plant Physiol 171: 1665 – 1674 | |
dc.identifier.citedreference | Sheehan D, Meade G, Foley VM, Dowd CA ( 2001 ) Structure, function and evolution of glutathione transferases: Implications for classification of non‐mammalian members of an ancient enzyme superfamily. Biochem J 360: 1 – 16 | |
dc.identifier.citedreference | Song Y, Yang C, Gao S, Zhang W, Li L, Kuai B ( 2014 ) Age‐triggered and dark‐induced leaf senescence require the bHLH transcription factors PIF3, 4, and 5. Mol Plant 7: 1776 – 1787 | |
dc.identifier.citedreference | Sparkes IA, Baker A ( 2002 ) Peroxisome biogenesis and protein import in plants, animals and yeasts: Enigma and variations? (review). Mol Membr Biol 19: 171 – 185 | |
dc.identifier.citedreference | Suzuki T, Nakajima S, Morikami A, Nakamura K ( 2005 ) An Arabidopsis protein with a novel calcium‐binding repeat sequence interacts with TONSOKU/MGOUN3/BRUSHY1 involved in meristem maintenance. Plant Cell Physiol 46: 1452 – 1461 | |
dc.identifier.citedreference | Tolbert NE, Oeser A, Yamazaki RK, Hageman RH, Kisaki T ( 1969 ) A survey of plants for leaf peroxisomes. Plant Physiol 44: 135 – 147 | |
dc.identifier.citedreference | Vicentini F, Matile PM ( 1993 ) Gerontosomes, a multifunctional type of peroxisome in senescent leaves. J Plant Physiol 142: 50 – 56 | |
dc.identifier.citedreference | Weaver LM, Amasino RM ( 2001 ) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127: 876 – 886 | |
dc.identifier.citedreference | Weaver LM, Gan S, Quirino B, Amasino RM ( 1998 ) A comparison of the expression patterns of several senescence‐associated genes in response to stress and hormone treatment. Plant Mol Biol 37: 455 – 469 | |
dc.identifier.citedreference | Wiederhold E, Veenhoff LM, Poolman B, Slotboom DJ ( 2010 ) Proteomics of Saccharomyces cerevisiae organelles. Mol Cell Proteomics 9: 431 – 445 | |
dc.identifier.citedreference | Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ ( 2007 ) An “electronic fluorescent pictograph” Browser for exploring and analyzing large‐scale biological data sets. PLoS ONE 2: e718 | |
dc.identifier.citedreference | Yokouchl Y, Ikeda M, Inuzuka Y, Yukawa T ( 2002 ) Strong emission of methyl chloride from tropical plants. Nature 416: 163 – 165 | |
dc.identifier.citedreference | Arai Y, Hayashi M, Nishimura M ( 2008 ) Proteomic analysis of highly purified peroxisomes from etiolated soybean cotyledons. Plant Cell Physiol 49: 526 – 539 | |
dc.identifier.citedreference | Babujee L, Wurtz V, Ma C, Lueder F, Soni P, Van Dorsselaer A, Reumann S ( 2010 ) The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. J Exp Bot 61: 1441 – 1453 | |
dc.identifier.citedreference | Batzenschlager M, Masoud K, Janski N, Houlné G, Herzog E, Evrard J‐L, Baumberger N, Erhardt M, Nominé Y, Kieffer B, Schmit A‐C, Chabouté M‐E ( 2013 ) The GIP gamma‐tubulin complex‐associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Front Plant Sci 4: 480 | |
dc.identifier.citedreference | Beevers H ( 1979 ) Microbodies in higher plants. Annu Rev Plant Biol 30: 159 – 193 | |
dc.identifier.citedreference | Biswal UC, Biswal B ( 1984 ) Photocontrol of leaf senescence. Photochem Photobiol 39: 875 – 879 | |
dc.identifier.citedreference | Buchanan‐Wollaston V ( 1997 ) The molecular biology of leaf senescence. J Exp Bot 48: 181 – 199 | |
dc.identifier.citedreference | Chen Z, Kastaniotis AJ, Miinalainen IJ, Rajaram V, Wierenga RK, Hiltunen JK ( 2009 ) 17‐Hydroxysteroid dehydrogenase type 8 and carbonyl reductase type 4 assemble as a ketoacyl reductase of human mitochondrial FAS. FASEB J 23: 3682 – 3691 | |
dc.identifier.citedreference | Corpas FJ, Barroso JB, Sandalio LM, Palma JM, Lupianez JA, del Río LA ( 1999 ) Peroxisomal NADP‐dependent isocitrate dehydrogenase. Characterization and activity regulation during natural senescence. Plant Physiol 121: 921 – 928 | |
dc.identifier.citedreference | Corpas FJ, Barroso JB, Carreras A, Quiros M, Leon AM, Romero‐Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gomez M, del Río LA ( 2004 ) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136: 2722 – 2733 | |
dc.identifier.citedreference | Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR ( 2000 ) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97: 3718 – 23 | |
dc.identifier.citedreference | Desai M, Hu J ( 2008 ) Light induces peroxisome proliferation in Arabidopsis seedlings through the photoreceptor phytochrome A, the transcription factor HY5 HOMOLOG, and the peroxisomal protein PEROXIN11b. Plant Physiol 146: 1117 – 1127 | |
dc.identifier.citedreference | Desai M, Pan R, Hu J ( 2017 ) Arabidopsis forkhead‐associated domain protein 3 negatively regulates peroxisome division. J Integr Plant Biol 59: 454 – 458 | |
dc.identifier.citedreference | Distefano S, Palma JM, McCarthy II, del Rio LA ( 1999 ) Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209: 308 – 13 | |
dc.identifier.citedreference | Dixon DP, Hawkins T, Hussey PJ, Edwards R ( 2009 ) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60: 1207 – 1218 | |
dc.identifier.citedreference | Duncan O, Taylor NNLN, Carrie C, Eubel H, Kubiszewski‐Jakubiak S, Zhang B, Narsai R, Millar AH, Whelan J ( 2011 ) Multiple lines of evidence localize signaling, morphology, and lipid biosynthesis machinery to the mitochondrial outer membrane of Arabidopsis. Plant Physiol 157: 1093 – 1113 | |
dc.identifier.citedreference | Engqvist MKM, Schmitz J, Gertzmann A, Florian A, Jaspert N, Arif M, Balazadeh S, Mueller‐Roeber B, Fernie AR, Maurino VG ( 2015 ) GLYCOLATE OXIDASE3, a Glycolate Oxidase Homolog of Yeast l‐Lactate Cytochrome c Oxidoreductase, supports l‐Lactate oxidation in roots of Arabidopsis. Plant Physiol 169: 1042 – 1061 | |
dc.identifier.citedreference | Esser C, Kuhn A, Groth G, Lercher MJ, Maurino VG ( 2014 ) Plant and animal glycolate oxidases have a common eukaryotic ancestor and convergently duplicated to evolve long‐chain 2‐hydroxy acid oxidases. Mol Biol Evol 31: 1089 – 1101 | |
dc.identifier.citedreference | Eubel H, Meyer EH, Taylor NL, Bussell JD, O’Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH ( 2008 ) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol 148: 1809 – 1829 | |
dc.identifier.citedreference | Fahy D, Sanad MNME, Duscha K, Lyons M, Liu F, Bozhkov P, Kunz H‐H, Hu J, Neuhaus HE, Steel PG, Smertenko A ( 2017 ) Impact of salt stress, cell death, and autophagy on peroxisomes: Quantitative and morphological analyses using small fluorescent probe N‐BODIPY. Sci Rep 7: 39069 | |
dc.identifier.citedreference | Fukao Y, Hayashi M, Hara‐Nishimura I, Nishimura M ( 2003 ) Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant Cell Physiol 44: 1002 – 1012 | |
dc.identifier.citedreference | Fukao Y, Hayashi M, Nishimura M ( 2002 ) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43: 689 – 696 | |
dc.identifier.citedreference | Gloerich J, Ruiter JPN, van den Brink DM, Ofman R, Ferdinandusse S, Wanders RJA ( 2006 ) Peroxisomal trans ‐2‐enoyl‐CoA reductase is involved in phytol degradation. FEBS Lett 580: 2092 – 2096 | |
dc.identifier.citedreference | Gronemeyer T, Wiese S, Ofman R, Bunse C, Pawlas M, Hayen H, Eisenacher M, Stephan C, Meyer HE, Waterham HR, Erdmann R, Wanders RJ, Warscheid B ( 2013 ) The proteome of human liver peroxisomes: Identification of five new peroxisomal constituents by a label‐free quantitative proteomics survey. PLoS ONE 8: e57395 | |
dc.identifier.citedreference | Hooper CM, Castleden IR, Tanz SK, Aryamanesh N, Millar AH ( 2017 ) SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Res 45: D1064 – D1074 | |
dc.identifier.citedreference | Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK ( 2012 ) Plant peroxisomes: Biogenesis and function. Plant Cell 24: 2279 – 2303 | |
dc.identifier.citedreference | Jiménez A, Hernández JA, Pastori G, del Rı́o LA, Sevilla F ( 1998 ) Role of the ascorbate‐glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118: 1327 – 1335 | |
dc.identifier.citedreference | Kaur N, Hu J ( 2011 ) Defining the plant peroxisomal proteome: From Arabidopsis to rice. Front Plant Sci 2: 1 – 41 | |
dc.identifier.citedreference | Kaur N, Hu J ( 2009 ) Dynamics of peroxisome abundance: A tale of division and proliferation. Curr Opin Plant Biol 12: 781 – 788 | |
dc.identifier.citedreference | Kaur N, Reumann S, Hu J ( 2009 ) Peroxisome biogenesis and function. In: The Arabidopsis Book 7: p e0123 | |
dc.identifier.citedreference | Koh S, André A, Edwards H, Ehrhardt D, Somerville S ( 2005 ) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44: 516 – 529 | |
dc.identifier.citedreference | Li W, Zang B, Liu C, Lu L, Wei N, Cao K, Deng XW, Wang X ( 2011 ) TSA1 interacts with CSN1/CSN and may be functionally involved in Arabidopsis seedling development in darkness. J Genet Genomics 38: 539 – 546 | |
dc.identifier.citedreference | Liebsch D, Keech O ( 2016 ) Dark‐induced leaf senescence: New insights into a complex light‐dependent regulatory pathway. New Phytol 212: 563 – 570 | |
dc.identifier.citedreference | Lingner T, Kataya AR, Antonicelli GE, Benichou A, Nilssen K, Chen X‐Y, Siemsen T, Morgenstern B, Meinicke P, Reumann S ( 2011 ) Identification of novel plant peroxisomal targeting signals by a combination of machine learning methods and in vivo subcellular targeting analyses. Plant Cell 23: 1556 – 1572 | |
dc.identifier.citedreference | Lopez‐Huertas E, Charlton WL, Johnson B, Graham IA, Baker A ( 2000 ) Stress induces peroxisome biogenesis genes. EMBO J 19: 6770 – 6777 | |
dc.identifier.citedreference | Mi J, Kirchner E, Cristobal S ( 2007 ) Quantitative proteomic comparison of mouse peroxisomes from liver and kidney. Proteomics 7: 1916 – 1928 | |
dc.identifier.citedreference | Nagatoshi Y, Nakamura T ( 2007 ) Characterization of three halide methyltransferases in Arabidopsis thaliana. Plant Biotechnol 24: 503 – 506 | |
dc.identifier.citedreference | Nagatoshi Y, Nakamura T ( 2009 ) Arabidopsis HARMLESS TO OZONE LAYER protein methylates a glucosinolate breakdown product and functions in resistance to Pseudomonas syringae pv. maculicola. J Biol Chem 284: 19301 – 19309 | |
dc.identifier.citedreference | Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H ( 2006 ) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane‐bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57: 3033 – 3042 | |
dc.identifier.citedreference | Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG ( 1997 ) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12: 527 – 535 | |
dc.identifier.citedreference | Ohno S, Nishikawa K, Honda Y, Nakajin S ( 2008 ) Expression in E. coli and tissue distribution of the human homologue of the mouse Ke 6 gene, 17β‐hydroxysteroid dehydrogenase type 8. Mol Cell Biochem 309: 209 – 215 | |
dc.identifier.citedreference | Palma JA, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río LA ( 2006 ) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plant. J Exp Bot 57: 1747 – 1758 | |
dc.identifier.citedreference | Pan R, Hu J ( 2018 ) The Proteome of Plant Peroxisomes. In: del Río LA, Schrader M, eds. Proteomics of Peroxisomes: Identifying Novel Functions and Regulatory Networks. Springer, in press | |
dc.identifier.citedreference | Pan R, Kaur N, Hu J ( 2014 ) The Arabidopsis mitochondrial membrane‐bound ubiquitin protease UBP27 contributes to mitochondrial morphogenesis. Plant J 78: 1047 – 1059 | |
dc.identifier.citedreference | Pan R, Satkovich J, Hu J ( 2016 ) E3 ubiquitin ligase SP1 regulates peroxisome biogenesis in Arabidopsis. Proc Natl Acad Sci USA 113: 201613530 | |
dc.identifier.citedreference | Panchuk II, Volkov RA, Schöffl F ( 2002 ) Heat stress‐ and heat shock transcription factor‐dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129: 838 – 853 | |
dc.identifier.citedreference | Paoletti AC, Parmely TJ, Tomomori‐Sato C, Sato S, Zhu D, Conaway RC, Conaway JW, Florens L, Washburn MP ( 2006 ) Quantitative proteomic analysis of distinct mammalian mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci USA 103: 18928 – 18933 | |
dc.identifier.citedreference | Pastori GM, del Rio LA ( 1997 ) Natural senescence of pea leaves (an activated oxygen‐mediated function for peroxisomes). Plant Physiol 113: 411 – 418 | |
dc.identifier.citedreference | Peterhansel C, Horst I, Niessen M, Blume C, Kebeish R, Kürkcüoglu S, Kreuzaler F ( 2010 ) Photorespiration. In: The Arabidopsis Book 8: p e0130 | |
dc.identifier.citedreference | Quan S, Switzenberg R, Reumann S, Hu J ( 2010 ) In vivo subcellular targeting analysis validates a novel peroxisome targeting signal type 2 and the peroxisomal localization of two proteins with putative functions in defense in Arabidopsis. Plant Signal Behav 5: 151 – 153 | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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