Dynamics of peroxisome abundance: a tale of division and proliferation

Current Opinion in Plant Biology

Volumn 12, Issue 6, 2009, Pages 781-788

  Kaur, Navneet ^a   Hu, Jianping ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CARRIER PROTEIN; DYNAMIN; HYH PROTEIN, ARABIDOPSIS; MEA PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; PEROXIN 11 PROTEIN, ARABIDOPSIS; PHYA PROTEIN, ARABIDOPSIS; PHYTOCHROME A;

ARABIDOPSIS; CELL CYCLE; CYTOLOGY; GENE EXPRESSION REGULATION; LIGHT; METABOLISM; PEROXISOME; PROTEIN PROCESSING; REVIEW;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CELL CYCLE; DYNAMINS; GENE EXPRESSION REGULATION, PLANT; LIGHT; MEMBRANE PROTEINS; PEROXISOMES; PHYTOCHROME A; PROTEIN PROCESSING, POST-TRANSLATIONAL;

ARABIDOPSIS;

EID: 70450188176     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2009.08.001     Document Type: Review

References (80)

1. Hayashi M., and Nishimura M. Entering a new era of research on plant peroxisomes. Curr Opin Plant Biol 6 (2003) 577-582
2. Nyathi Y., and Baker A. Plant peroxisomes as a source of signalling molecules. Biochim Biophys Acta 1763 (2006) 1478-1495
3. Olsen L.J., and Harada J. Peroxisomes and their assembly in higher plants. Annu Rev Plant Biol 46 (1995) 123-146
4. Reumann S., and Weber A.P. Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled-others remain. Biochim Biophys Acta 1763 (2006) 1496-1510
5. Fan J., Quan S., Orth T., Awai C., Chory J., and Hu J. The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol 139 (2005) 231-239
6. Hu J., Aguirre M., Peto C., Alonso J., Ecker J., and Chory J. A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297 (2002) 405-409
7. Lin Y., Sun L., Nguyen L.V., Rachubinski R.A., and Goodman H.M. The Pex16p homolog SSE1 and storage organelle formation in Arabidopsis seeds. Science 284 (1999) 328-330
8. Rylott E.L., Rogers C.A., Gilday A.D., Edgell T., Larson T.R., and Graham I.A. Arabidopsis mutants in short- and medium-chain acyl-CoA oxidase activities accumulate acyl-CoAs and reveal that fatty acid beta-oxidation is essential for embryo development. J Biol Chem 278 (2003) 21370-21377
9. Schumann U., Wanner G., Veenhuis M., Schmid M., and Gietl C. AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc Natl Acad Sci USA 100 (2003) 9626-9631
10. Sparkes I.A., Brandizzi F., Slocombe S.P., El-Shami M., Hawes C., and Baker A. An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol 133 (2003) 1809-1819
11. Steinberg S.J., Dodt G., Raymond G.V., Braverman N.E., Moser A.B., and Moser H.W. Peroxisome biogenesis disorders. Biochim Biophys Acta 1763 (2006) 1733-1748
12. Purdue P.E., and Lazarow P.B. Peroxisome biogenesis. Annu Rev Cell Dev Biol 17 (2001) 701-752
13. Yan M., Rayapuram N., and Subramani S. The control of peroxisome number and size during division and proliferation. Curr Opin Cell Biol 17 (2005) 376-383
14. Delille H.K., Alves R., and Schrader M. Biogenesis of peroxisomes and mitochondria: linked by division. Histochem Cell Biol 131 (2009) 441-446
15. Erdmann R., and Blobel G. Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J Cell Biol 128 (1995) 509-523
16. Marshall P.A., Krimkevich Y.I., Lark R.H., Dyer J.M., Veenhuis M., and Goodman J.M. Pmp27 promotes peroxisomal proliferation. J Cell Biol 129 (1995) 345-355
17. Rottensteiner H., Stein K., Sonnenhol E., and Erdmann R. Conserved function of pex11p and the novel pex25p and pex27p in peroxisome biogenesis. Mol Biol Cell 14 (2003) 4316-4328
18. Tam Y.Y., Torres-Guzman J.C., Vizeacoumar F.J., Smith J.J., Marelli M., Aitchison J.D., and Rachubinski R.A. Pex11-related proteins in peroxisome dynamics: a role for the novel peroxin Pex27p in controlling peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 14 (2003) 4089-4102
19. Vizeacoumar F.J., Torres-Guzman J.C., Bouard D., Aitchison J.D., and Rachubinski R.A. Pex30p, Pex31p, and Pex32p form a family of peroxisomal integral membrane proteins regulating peroxisome size and number in Saccharomyces cerevisiae. Mol Biol Cell 15 (2004) 665-677
20. Vizeacoumar F.J., Torres-Guzman J.C., Tam Y.Y., Aitchison J.D., and Rachubinski R.A. YHR150w and YDR479c encode peroxisomal integral membrane proteins involved in the regulation of peroxisome number, size, and distribution in Saccharomyces cerevisiae. J Cell Biol 161 (2003) 321-332
21. Orth T., Reumann S., Zhang X., Fan J., Wenzel D., Quan S., and Hu J. The PEROXIN11 protein family controls peroxisome proliferation in Arabidopsis. Plant Cell 19 (2007) 333-350. This is the first comprehensive study of the Arabidopsis PEX11 family conducted in planta. The authors generated PEX11 overexpression and RNAi plants and also used yeast complementation to determine the physiological roles of the PEX11 family of proteins in Arabidopsis. They concluded that all the PEX11 proteins promoted peroxisome proliferation and that individual members of the family might have discrete roles in the process.
22. Lingard M.J., and Trelease R.N. Five Arabidopsis peroxin 11 homologs individually promote peroxisome elongation, duplication or aggregation. J Cell Sci 119 (2006) 1961-1972. This is the first report on the PEX11 family, its localization and effect in plant cell cultures. The authors used immunofluorescence microscopy in Arabidopsis suspension cultured cells to demonstrate that all PEX11s target to peroxisomes and are individually responsible for elongation, duplication, or aggregation of peroxisomes in the cell. They also determined the topological orientation of the Arabidopsis PEX11 proteins.
23. Marshall P.A., Dyer J.M., Quick M.E., and Goodman J.M. Redox-sensitive homodimerization of Pex11p: a proposed mechanism to regulate peroxisomal division. J Cell Biol 135 (1996) 123-137
24. Lingard M.J., Gidda S.K., Bingham S., Rothstein S.J., Mullen R.T., and Trelease R.N. Arabidopsis PEROXIN11c-e, FISSION1b, and DYNAMIN-RELATED PROTEIN3A cooperate in cell cycle-associated replication of peroxisomes. Plant Cell 20 (2008) 1567-1585. The authors demonstrate that all the AtPEX11s homo-oligomerize and interact with FIS1B in Arabidopsis suspension cells. They also determined that the coordinate activities of PEX11c-e, FIS1B, and DRP3A are important for cell cycle associated peroxisome replication in cultured cells.
25. Li X., Baumgart E., Morrell J.C., Jimenez-Sanchez G., Valle D., and Gould S.J. PEX11 beta deficiency is lethal and impairs neuronal migration but does not abrogate peroxisome function. Mol Cell Biol 22 (2002) 4358-4365
26. Hu J. Plant peroxisome multiplication: highly regulated and still enigmatic. J Inter Plant Biol 49 (2007) 1112-1118
27. Fagarasanu A., Fagarasanu M., and Rachubinski R.A. Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 23 (2007) 321-344
28. Thoms S., and Erdmann R. Dynamin-related proteins and Pex11 proteins in peroxisome division and proliferation. FEBS J 272 (2005) 5169-5181
29. Hoppins S., Lackner L., and Nunnari J. The machines that divide and fuse mitochondria. Annu Rev Biochem 76 (2007) 751-780
30. Koch A., Schneider G., Luers G.H., and Schrader M. Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J Cell Sci 117 (2004) 3995-4006
31. Osteryoung K.W., and Nunnari J. The division of endosymbiotic organelles. Science 302 (2003) 1698-1704
32. Praefcke G.J., and McMahon H.T. The dynamin superfamily: universal membrane tubulation and fission molecules?. Nat Rev Mol Cell Biol 5 (2004) 133-147
33. Gasper R., Meyer S., Gotthardt K., Sirajuddin M., and Wittinghofer A. It takes two to tango: regulation of G proteins by dimerization. Nat Rev Mol Cell Biol 10 (2009) 423-429
34. Hoepfner D., van den Berg M., Philippsen P., Tabak H.F., and Hettema E.H. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J Cell Biol 155 (2001) 979-990
35. Koch A., Thiemann M., Grabenbauer M., Yoon Y., McNiven M.A., and Schrader M. Dynamin-like protein 1 is involved in peroxisomal fission. J Biol Chem 278 (2003) 8597-8605
36. Kuravi K., Nagotu S., Krikken A.M., Sjollema K., Deckers M., Erdmann R., Veenhuis M., and van der Klei I.J. Dynamin-related proteins Vps1p and Dnm1p control peroxisome abundance in Saccharomyces cerevisiae. J Cell Sci 119 (2006) 3994-4001
37. Li X., and Gould S.J. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J Biol Chem 278 (2003) 17012-17020
38. Wilsbach K., and Payne G.S. Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. EMBO J 12 (1993) 3049-3059
39. Mano S., Nakamori C., Kondo M., Hayashi M., and Nishimura M. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J 38 (2004) 487-498
40. Zhang X., and Hu J. Two small protein families, DYNAMIN-RELATED PROTEIN3 and FISSION1, are required for peroxisome fission in Arabidopsis. Plant J 57 (2009) 146-159. The authors identified three additional proteins that function in peroxisome fission in plants, DRP3B, FIS1A, and FIS1B. Mutants in any of these three genes, along with that of DRP3A, were found to exhibit defects in peroxisome and mitochondrial fission. This is the first report to show that, similar to yeast and mammals, the plant peroxisome division machinery also consists of the evolutionarily conserved DRPs and FIS1 proteins.
41. Hong Z., Bednarek S.Y., Blumwald E., Hwang I., Jurgens G., Menzel D., Osteryoung K.W., Raikhel N.V., Shinozaki K., Tsutsumi N., et al. A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53 (2003) 261-265
42. Arimura S., Aida G.P., Fujimoto M., Nakazono M., and Tsutsumi N. Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division. Plant Cell Physiol 45 (2004) 236-242
43. Arimura S., and Tsutsumi N. A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci USA 99 (2002) 5727-5731
44. Logan D.C., Scott I., and Tobin A.K. ADL2a, like ADL2b, is involved in the control of higher plant mitochondrial morphology. J Exp Bot 55 (2004) 783-785
45. Fujimoto M., Arimura S., Mano S., Kondo M., Saito C., Ueda T., Nakazono M., Nakano A., Nishimura M., and Tsutsumi N. Arabidopsis dynamin-related proteins DRP3A and DRP3B are functionally redundant in mitochondrial fission, but have distinct roles in peroxisomal fission. Plant J 58 (2009) 388-400. The authors showed that both DRP3A and DRP3B are capable of homo-dimer and hetero-dimer formation. Additionally, their analysis of the DRP3 single and double mutants led them to propose that while DRP3A and DRP3B are functionally redundant in mitochondrial division, they perform distinct roles in peroxisome fission, with DRP3A having a more prominent role and DRP3B contributing to a minor extent.
46. Low H.H., and Lowe J. A bacterial dynamin-like protein. Nature 444 (2006) 766-769
47. Jin J.B., Bae H., Kim S.J., Jin Y.H., Goh C.H., Kim D.H., Lee Y.J., Tse Y.C., Jiang L., and Hwang I. The Arabidopsis dynamin-like proteins ADL1C and ADL1E play a critical role in mitochondrial morphogenesis. Plant Cell 15 (2003) 2357-2369
48. Gao H., Kadirjan-Kalbach D., Froehlich J.E., and Osteryoung K.W. ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci U S A 100 (2003) 4328-4333
49. Miyagishima S., Itoh R., Toda K., Kuroiwa H., Nishimura M., and Kuriowa T. Microbody proliferation and segregation cycle in the single-microbody alga Cyanidioschyzon merolae. Planta 208 (1999) 326-336
50. Miyagishima S.Y., Nishida K., Mori T., Matsuzaki M., Higashiyama T., Kuroiwa H., and Kuroiwa T. A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15 (2003) 655-665
51. Nishida K., Takahara M., Miyagishima S.Y., Kuroiwa H., Matsuzaki M., and Kuroiwa T. Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci U S A 100 (2003) 2146-2151
52. Kobayashi S., Tanaka A., and Fujiki Y. Fis1, DLP1, and Pex11p coordinately regulate peroxisome morphogenesis. Exp Cell Res 313 (2007) 1675-1686
53. Koch A., Yoon Y., Bonekamp N.A., McNiven M.A., and Schrader M. A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 16 (2005) 5077-5086
54. Zhang X., and Hu J. FISSION1A and FISSION1B proteins mediate the fission of peroxisomes and mitochondria in Arabidopsis. Mol Plant 1 (2008) 1036-1047. The authors showed that FIS1A and FIS1B play partially redundant roles and are limiting factors in promoting peroxisome and mitochondrial fission in Arabidopsis. They also determined the role of the FIS1 C terminus in targeting the protein to the organelles.
55. Delille H.K., and Schrader M. Targeting of hFis1 to peroxisomes is mediated by Pex19p. J Biol Chem 283 (2008) 31107-31115
56. Yoon Y., Krueger E.W., Oswald B.J., and McNiven M.A. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23 (2003) 5409-5420
57. Gandre-Babbe S., and van der Bliek A.M. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 19 (2008) 2402-2412. The authors employed a siRNA screen in Drosophila cells to fish out factors causing aberrant mitochondrial phenotypes and identified a novel tail-anchored protein. Subsequent analysis of a mammalian homolog of the protein (Mff) revealed that it promotes fission of both peroxisomes and mitochondria in a Fis1-independent fashion.
58. Motley A.M., Ward G.P., and Hettema E.H. Dnm1p-dependent peroxisome fission requires Caf4p, Mdv1p and Fis1p. J Cell Sci 121 (2008) 1633-1640. The authors used in vivo fission assays to demonstrate that in yeast, the fission activity of Dnm1p is dependent on the presence of Fis1p and, additionally, either Caf4p or Mdv1p. Further, they showed that Vps1p mediates peroxisome fission independently of Dnm1p, Fis1p, Caf4p and Mdv1p.
59. Gurvitz A., and Rottensteiner H. The biochemistry of oleate induction: transcriptional upregulation and peroxisome proliferation. Biochim Biophys Acta 1763 (2006) 1392-1402
60. Desvergne B., and Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20 (1999) 649-688
61. Kersten S., Desvergne B., and Wahli W. Roles of PPARs in health and disease. Nature 405 (2000) 421-424
62. Castillo M.C., Sandalio L.M., Del Rio L.A., and Leon J. Peroxisome proliferation, wound-activated responses and expression of peroxisome-associated genes are cross-regulated but uncoupled in Arabidopsis thaliana. Plant Cell Environ 31 (2008) 492-505
63. de Felipe M.R., Lucas M.M., and Pozuelo J.M. Cytochemical study of catalase and peroxidase in the mesophyll of Lolium rigidum plants treated with isoproturon. J Plant Physiol 132 (1988) 67-73
64. Ferreira M.B., Bird B., and Davies D.D. The effect of light on the structure and organization of Lemna peroxisomes. J Exp Bot 40 (1989) 1029-1035
65. 2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytol 161 (2003) 791-799
66. Sinclair A.M., Trobacher C.P., Mathur N., Greenwood J.S., and Mathur J. Peroxule extension over ER defined paths constitutes a rapid subcellular response to hydroxyl stress. Plant J 59 (2009) 231-242
67. Ulloa R.M., Raices M., MacIntosh G.C., Maldonado S., and Tellez-Inon M.T. Jasmonic acid affects plant morphology and calcium-dependent protein kinase expression and activity in Solanum tuberosum. Physiol Plant 115 (2002) 417-427
68. Palma J.M., Garrido M., Rodriguez-Garcia M.I., and del Rio L.A. Peroxisome proliferation and oxidative stress mediated by activated oxygen species in plant peroxisomes. Arch Biochem Biophys 287 (1991) 68-74
69. Nila A.G., Sandalio L.M., Lopez M.G., Gomez M., del Rio L.A., and Gomez-Lim M.A. Expression of a peroxisome proliferator-activated receptor gene (xPPARalpha) from Xenopus laevis in tobacco (Nicotiana tabacum) plants. Planta 224 (2006) 569-581
70. Escriva H., Bertrand S., and Laudet V. The evolution of the nuclear receptor superfamily. Essays Biochem 40 (2004) 11-26
71. Naar A.M., and Thakur J.K. Nuclear receptor-like transcription factors in fungi. Genes Dev 23 (2009) 419-432
72. Phelps C., Gburcik V., Suslova E., Dudek P., Forafonov F., Bot N., MacLean M., Fagan R.J., and Picard D. Fungi and animals may share a common ancestor to nuclear receptors. Proc Natl Acad Sci U S A 103 (2006) 7077-7081
73. Thakur J.K., Arthanari H., Yang F., Chau K.H., Wagner G., and Naar A.M. Mediator subunit Gal11p/MED15 is required for fatty acid-dependent gene activation by yeast transcription factor Oaf1p. J Biol Chem 284 (2009) 4422-4428
74. Riechmann J.L., Heard J., Martin G., Reuber L., Jiang C., Keddie J., Adam L., Pineda O., Ratcliffe O.J., Samaha R.R., et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290 (2000) 2105-2110
75. Desai M., and Hu J. 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 (2008) 1117-1127. This is the first report of plant nuclear factors being involved in peroxisome proliferation. The authors screened for changes in light-induced PEX11b expression and peroxisome abundance in various light response mutants and identified phyA and HYH as important regulators of peroxisome proliferation during dark-light transition in Arabidopsis seedlings.
76. Guo T., Kit Y.Y., Nicaud J.M., Le Dall M.T., Sears S.K., Vali H., Chan H., Rachubinski R.A., and Titorenko V.I. Peroxisome division in the yeast Yarrowia lipolytica is regulated by a signal from inside the peroxisome. J Cell Biol 162 (2003) 1255-1266
77. Baker A., Graham I.A., Holdsworth M., Smith S.M., and Theodoulou F.L. Chewing the fat: beta-oxidation in signalling and development. Trends Plant Sci 11 (2006) 124-132
78. Cereghetti G.M., Stangherlin A., Martins de Brito O., Chang C.R., Blackstone C., Bernardi P., and Scorrano L. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci U S A 105 (2008) 15803-15808
79. Taguchi N., Ishihara N., Jofuku A., Oka T., and Mihara K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282 (2007) 11521-11529
80. Harder Z., Zunino R., and McBride H. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr Biol 14 (2004) 340-345