Towards understanding peroxisomal phosphoregulation in Arabidopsis thaliana
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- 作者：Amr. R. A. Kataya ; Edit Schei ; Cathrine Lillo
- 关键词：Peroxisomes ; POL like phosphatases (PLL2 ; PLL3) ; Protein phosphatase 2C (PP2C) ; Protein phosphatases ; Peroxisome targeting signal type 1 (PTS1) ; Purple acid phosphatase 7 ; Signaling ; β ; Oxidation
- 刊名：Planta
- 出版年：2016
- 出版时间：March 2016
- 年：2016
- 卷：243
- 期：3
- 页码：699-717
- 全文大小：9,604 KB
- 参考文献：Ahn CS, Han JA, Lee HS, Lee S, Pai HS (2011) The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell 23:185–209. doi:10.1105/tpc.110.074005 PubMedCentral CrossRef PubMed
Ahn CS, Ahn HK, Pai HS (2015) Overexpression of the PP2A regulatory subunit Tap46 leads to enhanced plant growth through stimulation of the TOR signalling pathway. J Exp Bot 66:827–840. doi:10.1093/jxb/eru438 PubMedCentral CrossRef PubMed
Arai Y, Hayashi M, Nishimura M (2008a) Proteomic analysis of highly purified peroxisomes from etiolated soybean cotyledons. Plant Cell Physiol 49:526–539. doi:10.1093/pcp/pcn027 CrossRef PubMed
Arai Y, Hayashi M, Nishimura M (2008b) Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid beta-oxidation in soybean and Arabidopsis. Plant Cell 20:3227–3240. doi:10.1105/tpc.108.062877 PubMedCentral CrossRef PubMed
Benschop JJ, Mohammed S, O’Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214. doi:10.1074/mcp.M600429-MCP200 CrossRef PubMed
Bernhardt K, Wilkinson S, Weber AP, Linka N (2012) A peroxisomal carrier delivers NAD(+) and contributes to optimal fatty acid degradation during storage oil mobilization. Plant J 69:1–13. doi:10.1111/j.1365-313X.2011.04775.x CrossRef PubMed
Cassin-Ross G, Hu J (2014) A simple assay to identify peroxisomal proteins involved in 12-oxo-phytodienoic acid metabolism. Plant Signal Behav 9:e29464. doi:10.4161/psb.29464 PubMedCentral CrossRef
Coca M, San Segundo B (2010) AtCPK1 calcium-dependent protein kinase mediates pathogen resistance in Arabidopsis. Plant J 63:526–540. doi:10.1111/j.1365-313X.2010.04255.x CrossRef PubMed
Dammann C, Ichida A, Hong BM, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132:1840–1848PubMedCentral CrossRef PubMed
De Duve C, Baudhuin P (1966) Peroxisomes (microbodies and related particles). Physiol Rev 46:323–357PubMed
del Pozo JC, Allona I, Rubio V, Leyva A, de la Pena A, Aragoncillo C, Paz-Ares J (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J 19:579–589CrossRef PubMed
Del Vecchio HA, Ying S, Park J, Knowles VL, Kanno S, Tanoi K, She YM, Plaxton WC (2014) The cell wall-targeted purple acid phosphatase AtPAP25 is critical for acclimation of Arabidopsis thaliana to nutritional phosphorus deprivation. Plant J 80:569–581. doi:10.1111/tpj.12663 CrossRef PubMed
Engholm-Keller K, Larsen MR (2011) Titanium dioxide as chemo-affinity chromatographic sorbent of biomolecular compounds—applications in acidic modification-specific proteomics. J Proteomics 75:317–328. doi:10.1016/j.jprot.2011.07.024 CrossRef PubMed
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. doi:10.1104/pp.108.129999 PubMedCentral CrossRef PubMed
Frank J, Kaulfurst-Soboll H, Rips S, Koiwa H, von Schaewen A (2008) Comparative analyses of Arabidopsis complex glycan1 mutants and genetic interaction with staurosporin and temperature sensitive3a. Plant Physiol 148:1354–1367. doi:10.1104/pp.108.127027 PubMedCentral CrossRef PubMed
Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43:689–696CrossRef PubMed
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 44:1002–1012CrossRef PubMed
Fulda M, Shockey J, Werber M, Wolter FP, Heinz E (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. Plant J 32:93–103CrossRef PubMed
Gagne JM, Clark SE (2010) The Arabidopsis stem cell factor POLTERGEIST is membrane localized and phospholipid stimulated. Plant Cell 22:729–743. doi:10.1105/tpc.109.068734 PubMedCentral CrossRef PubMed
Gould SJ, Keller GA, Subramani S (1987) Identification of a peroxisomal targeting signal at the carboxy terminus of firefly luciferase. J Cell Biol 105:2923–2931CrossRef PubMed
Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36:D1015–D1021. doi:10.1093/nar/gkm812 PubMedCentral CrossRef PubMed
Hooper CM, Tanz SK, Castleden IR, Vacher MA, Small ID, Millar AH (2014) SUBAcon: a consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome. Bioinformatics 30:3356–3364. doi:10.1093/bioinformatics/btu550 CrossRef PubMed
Jung S, Marelli M, Rachubinski RA, Goodlett DR, Aitchison JD (2010) Dynamic changes in the subcellular distribution of Gpd1p in response to cell stress. J Biol Chem 285:6739–6749. doi:10.1074/jbc.M109.058552 PubMedCentral CrossRef PubMed
Kataya ARA (2011) Identification of peroxisome-targeted proteins implicated in plant innate immunity in Arabidopsis thaliana. PhD, Department of mathematics and Natural Science, Faculty of Science and Technology, University of Stavanger, Stavanger, Norway
Kataya AR, Heidari B, Hagen L, Kommedal R, Slupphaug G, Lillo C (2015a) Protein phosphatase 2A holoenzyme is targeted to peroxisomes by piggybacking and positively affects peroxisomal beta-oxidation. Plant Physiol 167:493–506. doi:10.1104/pp.114.254409 PubMedCentral CrossRef PubMed
Kataya AR, Heidari B, Lillo C (2015b) Protein phosphatase 2A regulatory subunits affecting plant innate immunity, energy metabolism, and flowering time–joint functions among B’eta subfamily members. Plant Signal Behav 10:e1026024. doi:10.1080/15592324.2015.1026024 PubMedCentral CrossRef PubMed
Kataya AR, Schei E, Lillo C (2015c) MAP kinase phosphatase 1 harbors a novel PTS1 and is targeted to peroxisomes following stress treatments. J Plant Physiol 179:12–20. doi:10.1016/j.jplph.2015.03.002 CrossRef PubMed
Kaur N, Reumann S, Hu J (2009) Peroxisome biogenesis and function. Arabidopsis Book 7:e0123. doi:10.1199/tab.0123
Kerk D, Templeton G, Moorhead GB (2008) Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol 146:351–367. doi:10.1104/pp.107.111393 PubMedCentral CrossRef PubMed
Kim PK, Hettema EH (2015) Multiple pathways for protein transport to peroxisomes. J Mol Biol 427:1176–1190. doi:10.1016/j.jmb.2015.02.005 CrossRef PubMed
Kim DJ, Smith SM (1994) Expression of a single gene encoding microbody NAD-malate dehydrogenase during glyoxysome and peroxisome development in cucumber. Plant Mol Biol 26:1833–1841CrossRef PubMed
Li D, Zhu H, Liu K, Liu X, Leggewie G, Udvardi M, Wang D (2002) Purple acid phosphatases of Arabidopsis thaliana. Comparative analysis and differential regulation by phosphate deprivation. J Biol Chem 277:27772–27781. doi:10.1074/jbc.M204183200 CrossRef PubMed
Liang C, Tian J, Lam HM, Lim BL, Yan X, Liao H (2010) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152:854–865. doi:10.1104/pp.109.147918 PubMedCentral CrossRef PubMed
Lillo C, Kataya AR, Heidari B, Creighton MT, Nemie-Feyissa D, Ginbot Z, Jonassen EM (2014) Protein phosphatases PP2A, PP4 and PP6: mediators and regulators in development and responses to environmental cues. Plant Cell Environ 37:2631–2648. doi:10.1111/pce.12364 CrossRef PubMed
Lingard MJ, Monroe-Augustus M, Bartel B (2009) Peroxisome-associated matrix protein degradation in Arabidopsis. Proc Natl Acad Sci USA 106:4561–4566. doi:10.1073/pnas.0811329106 PubMedCentral CrossRef PubMed
Lingner T, Kataya AR, Antonicelli GE, Benichou A, Nilssen K, Chen XY, 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. doi:10.1105/tpc.111.084095 PubMedCentral CrossRef PubMed
Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M et al (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183. doi:10.1126/science.1119409 CrossRef PubMed
Ma C, Reumann S (2008) Improved prediction of peroxisomal PTS1 proteins from genome sequences based on experimental subcellular targeting analyses as exemplified for protein kinases from Arabidopsis. J Exp Bot 59:3767–3779. doi:10.1093/jxb/ern221 CrossRef PubMed
Ma C, Haslbeck M, Babujee L, Jahn O, Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heat-shock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141:47–60. doi:10.1104/pp.105.073841 PubMedCentral CrossRef PubMed
Mano S, Nishimura M (2005) Plant peroxisomes. Vitam Horm 72:111–154. doi:10.1016/S0083-6729(05)72004-5 CrossRef PubMed
Maselli GA, Slamovits CH, Bianchi JI, Vilarrasa-Blasi J, Cano-Delgado AI, Mora-Garcia S (2014) Revisiting the evolutionary history and roles of protein phosphatases with Kelch-like domains in plants. Plant Physiol 164:1527–1541. doi:10.1104/pp.113.233627 PubMedCentral CrossRef PubMed
Matre P (2009) Protein phosphatase 2A and regulation of nitrate reductase in plants. PhD, Department of mathematics and Natural Science, Faculty of Science and Technology, University of Stavanger, Stavanger, Norway
Matre P, Meyer C, Lillo C (2009) Diversity in subcellular targeting of the PP2A B’eta subfamily members. Planta 230:935–945. doi:10.1007/s00425-009-0998-z CrossRef PubMed
Meyer T, Holscher C, Schwoppe C, von Schaewen A (2011) Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. Plant J 66:745–758. doi:10.1111/j.1365-313X.2011.04535.x CrossRef PubMed
Moorhead GB, De Wever V, Templeton G, Kerk D (2009) Evolution of protein phosphatases in plants and animals. Biochem J 417:401–409. doi:10.1042/BJ20081986 CrossRef PubMed
Mullen RT, Trelease RN (2006) The ER-peroxisome connection in plants: development of the “ER semi-autonomous peroxisome maturation and replication” model for plant peroxisome biogenesis. Biochim Biophys Acta 1763:1655–1668. doi:10.1016/j.bbamcr.2006.09.011 CrossRef PubMed
Olczak M, Morawiecka B, Watorek W (2003) Plant purple acid phosphatases—genes, structures and biological function. Acta Biochim Pol 50:1245–1256PubMed
Orth T, Reumann S, Zhang XC, Fan JL, Wenzel D, Quan S, Hu JP (2007) The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19:333–350. doi:10.1105/tpc.106.045831 PubMedCentral CrossRef PubMed
Quan S, Yang PF, Cassin-Ross G, Kaur N, Switzenberg R, Aung K, Li JY, Hu JP (2013) Proteome analysis of peroxisomes from etiolated Arabidopsis seedlings identifies a peroxisomal protease involved in beta- oxidation and development. Plant Physiol 163:1518–1538. doi:10.1104/pp.113.223453 PubMedCentral CrossRef PubMed
Rappsilber J, Ishihama Y, Mann M (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75:663–670CrossRef PubMed
Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135:783–800PubMedCentral CrossRef PubMed
Reumann S, Lavanya 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. doi:10.1105/tpc.107.050989 PubMedCentral CrossRef PubMed
Reumann S, Quan S, Aung K, Yang PF et al (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. doi:10.1104/pp.109.137703 PubMedCentral CrossRef PubMed
Reumann S, Buchwald D, Lingner T (2012) PredPlantPTS1: a web Server for the prediction of plant peroxisomal proteins. Front Plant Sci 3:194. doi:10.3389/fpls.2012.00194 PubMedCentral CrossRef PubMed
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMed
Schenk G, Mitić N, Hanson GR, Comba P (2013) Purple acid phosphatase: a journey into the function and mechanism of a colorful enzyme. Coord Chem Rev 257:473–482. doi:10.1016/j.ccr.2012.03.020 CrossRef
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRef PubMed
Sents W, Ivanova E, Lambrecht C, Haesen D, Janssens V (2013) The biogenesis of active protein phosphatase 2A holoenzymes: a tightly regulated process creating phosphatase specificity. FEBS J 280:644–661. doi:10.1111/j.1742-4658.2012.08579.x CrossRef PubMed
Song S-K, Clark SE (2005) POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis. Dev Biol 285:272–284. doi:10.1016/j.ydbio.2005.06.020 CrossRef PubMed
Sørhagen K, Laxa M, Peterhänsel C, Reumann S (2013) The emerging role of photorespiration and non-photorespiratory peroxisomal metabolism in pathogen defence. Plant Biol 15:723–736. doi:10.1111/j.1438-8677.2012.00723.x CrossRef PubMed
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197 PubMedCentral CrossRef PubMed
Theodoulou FL, Bernhardt K, Linka N, Baker A (2013) Peroxisome membrane proteins: multiple trafficking routes and multiple functions? Biochem J 451:345–352. doi:10.1042/bj20130078 CrossRef PubMed
Tian J, Liao H (2015) The role of intracellular and secreted purple acid phosphatases in plant phosphorus scavenging and recycling. Annu Plant Rev 48:265–287. doi:10.1002/9781118958841.ch10
Titorenko VI, Rachubinski RA (1998) Mutants of the yeast Yarrowia lipolytica defective in protein exit from the endoplasmic reticulum are also defective in peroxisome biogenesis. Mol Cell Biol 18:2789–2803PubMedCentral CrossRef PubMed
Titorenko VI, Ogrydziak DM, Rachubinski RA (1997) Four distinct secretory pathways serve protein secretion, cell surface growth, and peroxisome biogenesis in the yeast Yarrowia lipolytica. Mol Cell Biol 17:5210–5226PubMedCentral CrossRef PubMed
Tran HT, Hurley BA, Plaxton WC (2010a) Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci 179:14–27. doi:10.1016/j.plantsci.2010.04.005 CrossRef
Tran HT, Qian W, Hurley BA, She YM, Wang D, Plaxton WC (2010b) Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase isozymes secreted by phosphate-starved Arabidopsis thaliana. Plant Cell Environ 33:1789–1803. doi:10.1111/j.1365-3040.2010.02184.x CrossRef PubMed
Uhrig RG, Moorhead GB (2011) Two ancient bacterial-like PPP family phosphatases from Arabidopsis are highly conserved plant proteins that possess unique properties. Plant Physiol 157:1778–1792. doi:10.1104/pp.111.182493 PubMedCentral CrossRef PubMed
Uhrig RG, Kerk D, Moorhead GB (2013a) Evolution of bacterial-like phosphoprotein phosphatases in photosynthetic eukaryotes features ancestral mitochondrial or archaeal origin and possible lateral gene transfer. Plant Physiol 163:1829–1843. doi:10.1104/pp.113.224378 PubMedCentral CrossRef PubMed
Uhrig RG, Labandera AM, Moorhead GB (2013b) Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci 18:505–513. doi:10.1016/j.tplants.2013.05.004 CrossRef PubMed
Van Bel M, Proost S, Wischnitzki E, Movahedi S, Scheerlinck C, Van de Peer Y, Vandepoele K (2012) Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol 158:590–600. doi:10.1104/pp.111.189514 PubMedCentral CrossRef PubMed
Wang L, Lu S, Zhang Y, Li Z, Du X, Liu D (2014) Comparative genetic analysis of Arabidopsis purple acid phosphatases AtPAP10, AtPAP12, and AtPAP26 provides new insights into their roles in plant adaptation to phosphate deprivation. J Integr Plant Biol 56:299–314. doi:10.1111/jipb.12184 CrossRef PubMed
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. doi:10.1371/journal.pone.0000718 PubMedCentral CrossRef PubMed
Wu G, Wang X, Li X, Kamiya Y, Otegui, Chory J (2011) Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci Signal 4:ra29. doi:10.1126/scisignal.2001258 CrossRef PubMed
Xue T et al (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genom 9:550. doi:10.1186/1471-2164-9-550 CrossRef
Yang Y-P, Randall DD, Trelease RN (1988) Phosphorylation of glyoxysomal malate synthase from castor oil seeds Ricinus communis L. FEBS Lett 234:275–279. doi:10.1016/0014-5793(88)80097-8 CrossRef
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572. doi:10.1038/nprot.2007.199 CrossRef PubMed
Yu LP, Miller AK, Clark SE (2003) POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr Biol 13:179–188CrossRef PubMed
Zhang XC, Hu JP (2010) The Arabidopsis chloroplast division protein DYNAMIN-RELATED PROTEIN5B also mediates peroxisome division. Plant Cell 22:431–442. doi:10.1105/tpc.109.071324 PubMedCentral CrossRef PubMed
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632. doi:10.1104/pp.104.046367 PubMedCentral CrossRef PubMed
Zolman BK, Silva ID, Bartel B (2001) The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid beta -oxidation. Plant Physiol 127:1266–1278. doi:10.1104/pp.010550 PubMedCentral CrossRef PubMed - 作者单位：Amr. R. A. Kataya (1)
Edit Schei (1)
Cathrine Lillo (1)
1. Faculty of Science and Technology, Centre for Organelle Research, University of Stavanger, N-4036, Stavanger, Norway - 刊物主题：Plant Sciences; Agriculture; Ecology; Forestry;
- 出版者：Springer Berlin Heidelberg
- ISSN：1432-2048
文摘
Main conclusion This work identifies new protein phosphatases and phosphatase-related proteins targeting peroxisomes, and raises the question of a novel protein import pathway from ER to peroxisomes involving peroxisomal targeting signal type 1 (PTS1)