Protein phosphatase 2A holoenzyme is targeted to peroxisomes by piggybacking and positively affects peroxisomal b-oxidation

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 493-506

  Kataya, Amr R A ^a   Heidari, Behzad ^a   Hagen, Lars ^b   Kommedal, Roald ^a   Slupphaug, Geir ^b   Lillo, Cathrine ^a  

^a UNIVERSITY OF STAVANGER   (Norway)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

HOLOENZYME; HYBRID PROTEIN; INDOLEACETIC ACID DERIVATIVE; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN BINDING; PROTEIN SUBUNIT; SUCROSE; TRIACYLGLYCEROL;

ARABIDOPSIS; BIOLOGICAL MODEL; DRUG EFFECTS; ENZYME ACTIVE SITE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; MOLECULAR EVOLUTION; MUTATION; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PEROXISOME; PHENOTYPE; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PROTEIN SUBUNIT; SEEDLING; TRANSGENIC PLANT;

ARABIDOPSIS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HOLOENZYMES; INDOLEACETIC ACIDS; LIPID METABOLISM; MODELS, BIOLOGICAL; MUTATION; OXIDATION-REDUCTION; PEROXISOMES; PHENOTYPE; PHOSPHORYLATION; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; SEEDLINGS; STRESS, PHYSIOLOGICAL; SUCROSE; TRIGLYCERIDES;

EID: 84921968605     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.254409     Document Type: Article

References (63)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
3. Browse J, McCourt PJ, Somerville CR (1986) Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Anal Biochem 152: 141-145
4. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
5. Coca M, San Segundo B (2010) AtCPK1 calcium-dependent protein kinase mediates pathogen resistance in Arabidopsis. Plant J 63: 526-540
6. Dammann C, Ichida A, Hong B, Romanowsky SM, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calciumdependent protein kinase isoforms from Arabidopsis. Plant Physiol 132: 1840-1848
7. De Duve C, Baudhuin P (1966) Peroxisomes (microbodies and related particles). Physiol Rev 46: 323-357
8. Eichhorn PJ, Creyghton MP, Bernards R (2009) Protein phosphatase 2A regulatory subunits and cancer. Biochim Biophys Acta 1795: 1-15
9. 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
10. 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
11. Farkas I, Dombrádi V, Miskei M, Szabados L, Koncz C (2007) Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci 12: 169-176
12. 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
13. Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J (2004) Peroxisomal Acyl- CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16: 394-405
14. 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: 93-103
15. Germain V, Rylott EL, Larson TR, Sherson SM, Bechtold N, Carde JP, Bryce JH, Graham IA, Smith SM (2001) Requirement for 3-ketoacyl-CoA thiolase-2 in peroxisome development, fatty acid beta-oxidation and breakdown of triacylglycerol in lipid bodies of Arabidopsis seedlings. Plant J 28: 1-12
16. Heidari B, Matre P, Nemie-Feyissa D, Meyer C, Rognli OA, Møller SG, Lillo C (2011) Protein phosphatase 2A B55 and A regulatory subunits interact with nitrate reductase and are essential for nitrate reductase activation. Plant Physiol 156: 165-172
17. Heidari B, Nemie-Feyissa D, Kangasjärvi S, Lillo C (2013) Antagonistic regulation of flowering time through distinct regulatory subunits of protein phosphatase 2A. PLoS ONE 8: e67987
18. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439
19. Jen CH, Manfield IW, Michalopoulos I, Pinney JW, Willats WGT, Gilmartin PM, Westhead DR (2006) The Arabidopsis co-expression tool (ACT): a WWW-based tool and database for microarray-based gene expression analysis. Plant J 46: 336-348
20. Karp PD, Ouzounis CA, Moore-Kochlacs C, Goldovsky L, Kaipa P, Ahrén D, Tsoka S, Darzentas N, Kunin V, López-Bigas N (2005) Expansion of the BioCyc collection of pathway/genome databases to 160 genomes. Nucleic Acids Res 33: 6083-6089
21. Kaur N, Reumann S, Hu J (2009) Peroxisome Biogenesis and Function. The Arabidopsis Book 7: e0123, doi/10.1199/tab.0123
22. 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: 1833-1841
23. Koroleva OA, Tomlinson ML, Leader D, Shaw P, Doonan JH (2005) Highthroughput protein localization in Arabidopsis using Agrobacteriummediated transient expression of GFP-ORF fusions. Plant J 41: 162-174
24. Kragler F, Lametschwandtner G, Christmann J, Hartig A, Harada JJ (1998) Identification and analysis of the plant peroxisomal targeting signal 1 receptor NtPEX5. Proc Natl Acad Sci USA 95: 13336-13341
25. Lee MS, Mullen RT, Trelease RN (1997) Oilseed isocitrate lyases lacking their essential type 1 peroxisomal targeting signal are piggybacked to glyoxysomes. Plant Cell 9: 185-197
26. Leivar P, Antolín-Llovera M, Ferrero S, Closa M, Arró M, Ferrer A, Boronat A, Campos N (2011) Multilevel control of Arabidopsis 3-hydroxy-3- methylglutaryl coenzyme A reductase by protein phosphatase 2A. Plant Cell 23: 1494-1511
27. Lemieux B, Miquel M, Somerville C, Browse J (1990) Mutants of Arabidopsis with alterations in seed lipid fatty acid composition. Theor Appl Genet 80: 234-240
28. 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
29. 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
30. Mano S, Nishimura M (2005) Plant peroxisomes. Vitam Horm 72: 111-154
31. Matre P, Meyer C, Lillo C (2009) Diversity in subcellular targeting of the PP2A B'eta subfamily members. Planta 230: 935-945
32. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, HeislerMG, Ohno C, Zhang J, Huang F, et al (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130: 1044-1056
33. Orth T, Reumann S, Zhang X, Fan J, Wenzel D, Quan S, Hu J (2007) The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19: 333-350
34. 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 β-oxidation and development. Plant Physiol 163: 1518-1538
35. 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: 663-670
36. Rehling P, Albertini M, Kunau WH (1996) Protein import into peroxisomes: new developments. Ann N Y Acad Sci 804: 34-46
37. Reumann S (2004) Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol 135: 783-800
38. 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
39. 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
40. Reumann S, Quan S, Aung K, Yang P, Manandhar-Shrestha K, Holbrook D, Linka N, Switzenberg R, Wilkerson CG, Weber AP, et al (2009) Indepth 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
41. Reumann S, Singhal R (2014) Isolation of Leaf Peroxisomes from Arabidopsis for Organelle Proteome Analyses. In JV Jorrin-Novo, S Komatsu, W Weckwerth, S Wienkoop, eds, Plant Proteomics, Ed 2, Vol 1072. Humana Press, pp 541-552
42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425
43. Samson F, Brunaud V, Balzergue S, Dubreucq B, Lepiniec L, Pelletier G, Caboche M, Lecharny A (2002) FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res 30: 94-97
44. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675
45. Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994
46. Sørhagen K, Laxa M, Peterhänsel C, Reumann S (2013) The emerging role of photorespiration and non-photorespiratory peroxisomal metabolism in pathogen defence. Plant Biol (Stuttg) 15: 723-736
47. 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
48. Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, et al (2011) PP2A activates brassinosteroidresponsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13: 124-131
49. Terol J, Bargues M, Carrasco P, Pérez-Alonso M, Paricio N (2002) Molecular characterization and evolution of the protein phosphatase 2A B' regulatory subunit family in plants. Plant Physiol 129: 808-822
50. Tran HT, Nimick M, Uhrig RG, Templeton G, Morrice N, Gourlay R, DeLong A, Moorhead GB (2012) Arabidopsis thaliana histone deacetylase 14 (HDA14) is an α-tubulin deacetylase that associates with PP2A and enriches in the microtubule fraction with the putative histone acetyltransferase ELP3. Plant J 71: 263-272
51. Trotta A, Konert G, Rahikainen M, Aro EM, Kangasjärvi S (2011b) Knockdown of protein phosphatase 2A subunit B'γ promotes phosphorylation of CALRETICULIN 1 in Arabidopsis thaliana. Plant Signal Behav 6: 1665-1668
52. Trotta A, Wrzaczek M, Scharte J, Tikkanen M, Konert G, Rahikainen M, Holmström M, Hiltunen HM, Rips S, Sipari N, et al (2011a) Regulatory subunit B'gamma of protein phosphatase 2A prevents unnecessary defense reactions under low light in Arabidopsis. Plant Physiol 156: 1464-1480
53. Uhrig RG, Labandera AM, Moorhead GB (2013) Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci 18: 505-513
54. van den Bosch H, Schutgens RB, Wanders RJ, Tager JM (1992) Biochemistry of peroxisomes. Annu Rev Biochem 61: 157-197
55. Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56: 505-516
56. Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143
57. 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
58. Woodward AW, Bartel B (2005) The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol Biol Cell 16: 573-583
59. Yang R, Jarvis DE, Chen H, Beilstein MA, Grimwood J, Jenkins J, Shu S, Prochnik S, Xin M, Ma C, et al (2013) The reference genome of the halophytic plant Eutrema salsugineum. Front Plant Sci 4: 46
60. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
61. Zhang X, Hu J (2010) The Arabidopsis chloroplast division protein DYNAMIN-RELATED PROTEIN5B also mediates peroxisome division. Plant Cell 22: 431-442
62. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632
63. 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