Metabolite Transporters of the Plant Peroxisomal Membrane: Known and Unknown
Abstract
Tremendous progress in plant peroxisome research has revealed unexpected metabolic functions for plant peroxisomes. Besides photorespiration and lipid metabolism, plant peroxisomes play a key role in many metabolic and signaling pathways, such as biosynthesis of phytohormones, pathogen defense, senescence-associated processes, biosynthesis of biotin and isoprenoids, and metabolism of urate, polyamines, sulfite, phylloquinone, volatile benzenoids, and branched chain amino acids. These peroxisomal pathways require an interplay with other cellular compartments, including plastids, mitochondria, and the cytosol. Consequently, a considerable number of substrates, intermediates, end products, and cofactors have to shuttle across peroxisome membranes. However, our knowledge of their membrane passage is still quite limited. This review describes the solute transport processes required to connect peroxisomes with other cell compartments. Furthermore, we discuss the known and yet-to-be-defined transport proteins that mediate these metabolic exchanges across the peroxisomal bilayer.
Keywords
Plant Peroxisomes Metabolite transport proteinsAbbreviations
- AA
Amino acid
- AAE
Acyl-activating enzyme
- ABC
ATP binding cassette
- ABI5
Abscisic acid-insensitive 5
- APX
Ascorbate peroxidase
- ASC
Ascorbate
- ATP
Adenosine triphosphate
- BA
Benzoic acid
- BCAA
Branched chain amino acid
- β-ox
β-oxidation
- BZO1
Benzoyl-CoA ligase
- CHY1/DBR5
Peroxisomal β-hydroxyisobutyryl-CoA hydrolase
- CoA
Coenzyme A
- CTS
COMATOSE (peroxisomal ABC transporter)
- 2,4-D
Dichlorophenoxyacetic acid
- DAR
Dehydroascorbate reductase
- 2,4-DB
2,4-dichlorophenoxybutyrate
- D-2-HG
D-2-hydroxyglutarate
- DHNA
1,4-dihydroxy-2-naphthoate
- DiT2
Glutamate/2-oxoglutarate translocator
- DMAPP
Dimethylallyl diphosphate
- DOXP
1-deoxy-D-xylulose-5-phosphate
- FA
Fatty acid
- FFS
Farnesyl diphosphate synthase
- GAP
Glycerinaldehyde 3-phosphate
- Glu
Glutamate
- G6PD
Glucose-6-phosphate dehydrogenase
- GR
Glutathione reductase
- GSH
Glutathione
- GSSH
Glutathione disulfide
- H2O2
Hydrogen peroxide
- IAA
Indole acetic acid (auxin)
- IBA
Indole butyric acid
- IDH
Isocitrate dehydrogenase
- IDI
Isopentenyl diphosphate isomerase
- IPP
Isopentenyl diphosphate
- JA
Jasmonic acid
- KAPA
7-keto-8-amino-pelargonic acid
- NAD
Nicotinamide adenine dinucleotide
- NADH
Nicotinamide adenine dinucleotide reduced
- NADP
Nicotinamide adenine dinucleotide phosphate
- NADPH
Nicotinamide adenine dinucleotide phosphate reduced
- NAT
Nucleobase-ascorbate transport protein
- NH4+
Ammonium
- MDAR
Monodehydroascorbate reductase
- MVA
Mevalonate
- MVD
Mevalonate diphosphate decarboxylase
- OG
2-oxoglutarate
- OPC8:0
3-oxo-2-(2′-[Z]-pentenyl)cyclopentane-1-octanoic acid
- OPDA
12-oxophytodienoic acid
- OPPP
Oxidative pentose phosphate pathway
- PA
Polyamine
- PAL
Phenylalanine ammonia lyase
- PHYLLO
Plastid multifunctional enzyme
- 6PGD
6-phosphogluconate dehydrogenase
- 6PGL
6-phosphogluconolactone
- PMK
Phosphomevalonate kinase
- PMP22
22 kDa peroxisomal membrane protein
- PNC
Peroxisomal ATP transport proteins
- Pi
Inorganic phosphate
- PPase
Pyrophosphatase
- PPi
Pyrophosphate
- PT
Plastidial phosphate translocator
- PTS
Peroxisomal targeting signal
- PUT1
Small aliphatic amine transporter
- Pxmp2
Peroxisomal membrane protein 2
- PXN
Peroxisomal NAD/CoA transport protein
- Ru1.5BP
Ribulose-1.5-bisphosphate
- RNAi
RNA interference
- ROS
Reactive oxygen species
- SA
Salicylic acid
- SO
Sulfite oxidase
- TCA
Tricarboxylic acid cycle
- YFP
Yellow fluorescent protein
- XDH
Xanthine dehydrogenase
Notes
Acknowledgements
This work was supported by the DFG-grant 1781/1-1, 1781/2-1 and GRK 1525 (to Nicole Linka). The authors are grateful to Andreas P. M. Weber for helpful discussion. Many thanks to Kristin Bernhardt, Martin Schroers, Sarah K. Vigelius, Jan Wiese, and Thomas Wrobel for their commitments to elucidate the peroxisomal permeome in plants. Rothamsted Research receives grant-aided support from the BBSRC of the UK.
References
- Agrimi G, Russo A, Pierri CL, Palmieri F (2012) The peroxisomal NAD(+) carrier of Arabidopsis thaliana transports coenzyme A and its derivatives. J Bioenerg Biomembr 44:333–340PubMedCrossRefGoogle Scholar
- Antonenkov VD, Hiltunen JK (2011) Transfer of metabolites across the peroxisomal membrane. Biochim Biophys Acta 1822:1374–1386PubMedGoogle Scholar
- Arai Y, Hayashi M, Nishimura M (2008a) Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid beta-oxidation in soybean and Arabidopsis. Plant Cell 20:3227–3240PubMedCrossRefGoogle Scholar
- Arai YM, Hayashi M, Nishimura M (2008b) Proteomic analysis of highly purified peroxisomes from etiolated soybean cotyledons. Plant Cell Physiol 49:526–539PubMedCrossRefGoogle Scholar
- Araujo WL, Ishizaki K, Nunes-Nesi A, Tohge T, Larson TR, Krahnert I, Balbo I, Witt S, Dörmann P, Graham IA, Leaver CJ, Fernie AR (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22:1549–1563PubMedCrossRefGoogle Scholar
- 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 61:1441–1453PubMedCrossRefGoogle Scholar
- Bernhardt K, Wilkinson S, Weber APM, Linka N (2012) A peroxisomal carrier delivers NAD and contributes to optimal fatty acid degradation during storage oil mobilization. Plant J 69:1–13PubMedCrossRefGoogle Scholar
- Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415:146–154PubMedCrossRefGoogle Scholar
- Byrne RS, Hänsch R, Mendel RR, Hille R (2009) Oxidative half-reaction of Arabidopsis thaliana sulfite oxidase: generation of superoxide by a peroxisomal enzyme. J Biol Chem 284: 35479–35484PubMedCrossRefGoogle Scholar
- Clastre M, Papon N, Courdavault V, Giglioli-Guivarc’h N, St-Pierre B, Simkin AJ (2011) Subcellular evidence for the involvement of peroxisomes in plant isoprenoid biosynthesis. Plant Signal Behav 6:2044–2046PubMedCrossRefGoogle Scholar
- Corpas FJ, de la Colina C, Sánchez-Rasero F, del Río LA (1997) A role for leaf peroxisomes in the catabolism of purines. J Plant Physiol 151:246–250CrossRefGoogle Scholar
- Corpas FJ, Barroso JB, Sandalio LM, Distefano S, Palma JM, Lupiáñez JA, del Río LA (1998) A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes. Biochem J 330:777–784PubMedGoogle Scholar
- Corpas FJ, Barroso JB, Sandalio LM, Palma JM, Lupiáñez JA, del Río LA (1999) Peroxisomal NADP-dependent isocitrate dehydrogenase: characterization and activity regulation during natural senescence. Plant Physiol 121:921–928PubMedCrossRefGoogle Scholar
- Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, del Río LA (2008) Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165:1319–1330PubMedCrossRefGoogle Scholar
- Daruwala R, Song J, Koh WS, Rumsey SC, Levine M (1999) Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett 460:480–484PubMedCrossRefGoogle Scholar
- Dave A, Hernández ML, He Z, Andriotis VM, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599PubMedCrossRefGoogle Scholar
- De Marcos Lousa C, van Roermund CWT, Postis VLG, Dietrich D, Kerr ID, Wanders RJA, Baldwin SA, Baker A, Theodoulou F (2013) Intrinsic acyl-CoA thioesterase activity of a peroxisomal ATP binding cassette transporters is required for transport and metabolism of fatty acids. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1218034110 PubMedGoogle Scholar
- del Río LA, Fernández VM, Rupérez FL, Sandalio LM, Palma JM (1989) NADH induces the generation of superoxide radicals in leaf peroxisomes. Plant Physiol 89:728–731PubMedCrossRefGoogle Scholar
- del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272PubMedCrossRefGoogle Scholar
- del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335PubMedCrossRefGoogle Scholar
- Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156PubMedGoogle Scholar
- Desimone M, Catoni E, Ludewig U, Hilpert M, Schneider A, Kunze R, Tegeder M, Frommer WB, Schumacher K (2002) A novel superfamily of transporters for allantoin and other oxo derivatives of nitrogen heterocyclic compounds in Arabidopsis. Plant Cell 14:847–856PubMedCrossRefGoogle Scholar
- Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376–1387PubMedCrossRefGoogle Scholar
- Engqvist MKM, Kuhn A, Wienstroer J, Weber K, Jansen EEW, Jakobs C, Weber APM, Maurino VG (2011) Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. J Biol Chem 286:11382–11390PubMedCrossRefGoogle Scholar
- 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 148:1809–1829PubMedCrossRefGoogle Scholar
- Flügge UI, Gao W (2005) Transport of isoprenoid intermediates across chloroplast envelope membranes. Plant Biol (Stuttg) 7:91–97CrossRefGoogle Scholar
- Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M (2002) Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO J 21:2912–2922PubMedCrossRefGoogle Scholar
- Fukao Y, Hayashi M, Nishimura M (2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant Cell Physiol 43:689–696PubMedCrossRefGoogle Scholar
- 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 16:394–405PubMedCrossRefGoogle Scholar
- Gillissen B, Bürkle L, André B, Kuhn C, Rentsch D, Brandl B, Frommer WB (2000) A new family of high-affinity transporters for adenine, cytosine, and purine derivatives in Arabidopsis. Plant Cell 12:291–300PubMedGoogle Scholar
- Gross J, Cho WK, Lezhneva L, Falk J, Krupinska K, Shinozaki K, Seki M, Herrmann RG, Meurer J (2006) A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J Biol Chem 281:17189–17196PubMedCrossRefGoogle Scholar
- Haferkamp I, Fernie AR, Neuhaus HE (2011) Adenine nucleotide transport in plants: much more than a mitochondrial issue. Trends Plant Sci 16:507–515PubMedCrossRefGoogle Scholar
- Hashida S-N, Itami T, Takahashi H, Takahara K, Nagano M, Kawai-Yamada M, Shoji K, Goto F, Yoshihara T, Uchimiya H (2010) Nicotinate/nicotinamide mononucleotide adenyltransferase-mediated regulation of NAD biosynthesis protects guard cells from reactive oxygen species in ABA-mediated stomatal movement in Arabidopsis. J Exp Bot 61:3813–3825PubMedCrossRefGoogle Scholar
- Hayashi M, Nito K, Takei-Hoshi R, Yagi M, Kondo M, Suenaga A, Yamaya T, Nishimura M (2002) Ped3p is a peroxisomal ATP-binding cassette transporter that might supply substrates for fatty acid beta-oxidation. Plant Cell Physiol 43:1–11PubMedCrossRefGoogle Scholar
- Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Prog Lipid Res 51:95–148PubMedCrossRefGoogle Scholar
- Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5:263–267PubMedCrossRefGoogle Scholar
- Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303PubMedCrossRefGoogle Scholar
- Ibdah M, Pichersky E (2009) Arabidopsis chy1 null mutants are deficient in benzoic acid-containing glucosinolates in the seeds. Plant Biol (Stuttg) 11:574–581CrossRefGoogle Scholar
- Igarashi K, Kashiwagi K (2010) Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol Biochem 48:506–512PubMedCrossRefGoogle Scholar
- Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107PubMedGoogle Scholar
- Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284PubMedGoogle Scholar
- Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M (2008) A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol 49:1272–1282PubMedCrossRefGoogle Scholar
- Kanai M, Nishimura M, Hayashi M (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J 62:936–947PubMedGoogle Scholar
- Kienow L, Schneider K, Bartsch M, Stuible HP, Weng H, Miersch O, Wasternack C, Kombrink E (2008) Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana. J Exp Bot 59:403–419PubMedCrossRefGoogle Scholar
- Klempien A, Kaminaga Y, Qualley A, Nagegowda DA, Widhalm JR, Orlova I, Shasany AK, Taguchi G, Kish CM, Cooper BR, D’Auria JC, Rhodes D, Pichersky E, Dudareva N (2012) Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers. Plant Cell 24: 2015–2030PubMedCrossRefGoogle Scholar
- Kliebenstein DJ, D’Auria JC, Behere AS, Kim JH, Gunderson KL, Breen JN, Lee G, Gershenzon J, Last RL, Jander G (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J 51:1062–1076PubMedCrossRefGoogle Scholar
- Kunz HH, Scharnewski M, Feussner K, Feussner I, Flügge UI, Fulda M, Gierth M (2009) The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell 21:2733–2749PubMedCrossRefGoogle Scholar
- Lamberto I, Percudani R, Gatti R, Folli C, Petrucco S (2010) Conserved alternative splicing of Arabidopsis transthyretin-like determines protein localization and S-allantoin synthesis in peroxisomes. Plant Cell 22:1564–1574PubMedCrossRefGoogle Scholar
- Lange PR, Eastmond PJ, Madagan K, Graham IA (2004) An Arabidopsis mutant disrupted in valine catabolism is also compromised in peroxisomal fatty acid beta-oxidation. FEBS Lett 571:147–153PubMedCrossRefGoogle Scholar
- Lee S, Kaminaga Y, Cooper B, Pichersky E, Dudareva N, Chapple C (2012) Benzoylation and sinapoylation of glucosinolate R-groups in Arabidopsis. Plant J 72:411–422PubMedCrossRefGoogle Scholar
- Linka N, Esser C (2012) Transport proteins regulate the flux of metabolites and cofactors across the membrane of plant peroxisomes. Front Plant Sci 3:3PubMedCrossRefGoogle Scholar
- Linka N, Weber APM (2010) Intracellular metabolite transporters in plants. Mol Plant 3:21–53PubMedCrossRefGoogle Scholar
- Linka N, Theodoulou FL, Haslam RP, Linka M, Napier JA, Neuhaus HE, Weber APM (2008) Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20:3241–3257PubMedCrossRefGoogle Scholar
- López-Huertas E, Sandalio LM, del Río LA (1995) Integral membrane polypeptides of pea leaf peroxisomes – characterisation and response to plant stress. Plant Physiol Biochem 33: 295–302Google Scholar
- López-Huertas E, Sandalio LM, Gomez M, del Río LA (1997) Superoxide radical generation in peroxisomal membranes: evidence for the participation of the 18 kDa integral membrane polypeptide. Free Radical Res 26:497–506CrossRefGoogle Scholar
- López-Huertas E, Corpas FJ, Sandalio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536PubMedCrossRefGoogle Scholar
- Lucas KA, Filley JR, Erb JM, Graybill ER, Hawes JW (2007) Peroxisomal metabolism of propionic acid and isobutyric acid in plants. J Biol Chem 282:24980–24989PubMedCrossRefGoogle Scholar
- Mateos RM, León AM, Sandalio LM, Gómez M, del Río LA, Palma JM (2003) Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterisation and antioxidant activity. J Plant Physiol 160:1507–1516PubMedCrossRefGoogle Scholar
- Maurino VG, Grube E, Zielinski J, Schild A, Fischer K, Flügge UI (2006) Identification and expression analysis of twelve members of the nucleobase-ascorbate transporter (NAT) gene family in Arabidopsis thaliana. Plant Cell Physiol 47:1381–1393PubMedCrossRefGoogle Scholar
- Meyer T, Holscher C, Schwöppe C, von Schaewen A (2011) Alternative targeting of Arabidopsis plastidic glucose 6-phosphate dehydogenase 1 (G6PD1) involves cysteine-dependent interaction with G6PD4 in the cytosol. Plant J 66:745–758PubMedCrossRefGoogle Scholar
- Moschou PN, Sanmartin M, Andriopoulou AH, Rojo E, Sanchez-Serrano JJ, Roubelakis-Angelakis KA (2008) Bridging the gap between plant and mammalian polyamine catabolism: a novel peroxisomal polyamine oxidase responsible for a full back-conversion pathway in Arabidopsis. Plant Physiol 147:1845–1857PubMedCrossRefGoogle Scholar
- Mulangi V, Phuntumart V, Aouida M, Ramotar D, Morris P (2012) Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235:1–11PubMedCrossRefGoogle Scholar
- Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. Arabidopsis Book 9:e0142PubMedGoogle Scholar
- Nowak K, Luniak N, Witt C, Wüstefeld Y, Wachter A, Mendel RR, Hänsch R (2004) Peroxisomal localization of sulfite oxidase separates it from chloroplast-based sulfur assimilation. Plant Cell Physiol 45:1889–1894PubMedCrossRefGoogle Scholar
- Nyathi Y, De Marcos LC, van Roermund CW, Wanders RJ, Johnson B, Baldwin SA, Theodoulou FL, Baker A (2010) The Arabidopsis peroxisomal ABC transporter, comatose, complements the Saccharomyces cerevisiae pxa1 pxa2 delta mutant for metabolism of long chain fatty acids and exhibits fatty acyl-Coa stimulated ATPase activity. J Biol Chem 2010:21Google Scholar
- Palmieri F, Rieder B, Ventrella A, Bianco E, Do PT, Nunes-Nesi A, Trauth AU, Fiermonte G, Tjdaen J, Agrimi S, Kirchberger S, Paradies E, Fernie AR, Neuhaus HE (2009) Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD carrier proteins. J Biol Chem 284:31249–31259PubMedCrossRefGoogle Scholar
- Pinon V, Ravanel S, Douce R, Alban C (2005) Biotin synthesis in plants. The first committed step of the pathway is catalyzed by a cytosolic 7-keto-8-aminopelargonic acid synthase. Plant Physiol 139:1666–1676PubMedCrossRefGoogle Scholar
- Pracharoenwattana I, Cornah JE, Smith SM (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell 17:2037–2048PubMedCrossRefGoogle Scholar
- Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in β-oxidation, but not in the glyoxylate cycle. Plant J 50:381–390PubMedCrossRefGoogle Scholar
- Pracharoenwattana I, Zhou W, Smith SM (2010) Fatty acid beta-oxidation in germinating Arabidopsis seeds is supported by peroxisomal hydroxypyruvate reductase when malate dehydrogenase is absent. Plant Mol Biol 72:101–109PubMedCrossRefGoogle Scholar
- Qualley AV, Widhalm JR, Adebesin F, Kish CM, Dudareva N (2012) Completion of the core β-oxidative pathway of benzoic acid biosynthesis in plants. Proc Natl Acad Sci USA 109: 16383–16388PubMedCrossRefGoogle Scholar
- Reumann S (2000) The structural properties of plant peroxisomes and their metabolic significance. Biol Chem 381:639–648PubMedCrossRefGoogle Scholar
- Reumann S, Weber AP (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled – others remain. Biochim Biophys Acta 1763:1496–1510PubMedCrossRefGoogle Scholar
- Reumann S (2010) Toward a definition of the complete proteome of plant peroxisomes: where experimental proteomics must be complemented by bioinformatics. Proteomics 11:1764–1779CrossRefGoogle Scholar
- Reumann S, Maier E, Heldt HW, Benz R (1998) Permeability properties of the porin of spinach leaf peroxisomes. Eur J Biochem 251:359–366PubMedCrossRefGoogle Scholar
- Reumann S, Ma C, Lemke S, Babujee L (2004) AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiol 136:2587–2608PubMedCrossRefGoogle Scholar
- Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Luder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19:3170–3193PubMedCrossRefGoogle Scholar
- Reumann S, Quan S, Aung K, Yang P, Manandhar-Shresta 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 150:125–143PubMedCrossRefGoogle Scholar
- Rokka A, Antonenkov VD, Soininen R, Immonen HL, Pirilä PL, Bergmann U, Sormunen RT, Weckström M, Benz R, Hiltunen JK (2009) Pxmp2 is a channel-forming protein in mammalian peroxisomal membrane. PLoS One 4:e5090PubMedCrossRefGoogle Scholar
- Rottensteiner H, Theodoulou FL (2006) The ins and outs of peroxisomes: co-ordination of membrane transport and peroxisomal metabolism. Biochim Biophys Acta 1763:1527–1540PubMedCrossRefGoogle Scholar
- Russell L, Larner V, Kurup S, Bougourd S, Holdsworth M (2000) The Arabidopsis COMATOSE locus regulates germination potential. Development 127:3759–3767PubMedGoogle Scholar
- Sandalio LM, Fernández VM, Rupérez FL, del Río LA (1988) Superoxide free radicals are produced in glyoxysomes. Plant Physiol 87:1–4PubMedCrossRefGoogle Scholar
- Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, Gidoni D, Eyal Y (2008) Peroxisomal localization of Arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol 148:1219–1228PubMedCrossRefGoogle Scholar
- Simkin AJ, Guirimand G, Papon N, Courdavault V, Thabet I, Ginis O, Bouzid S, Giglioli-Guivarc’h N, Clastre M (2011) Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234:903–914PubMedCrossRefGoogle Scholar
- Slocombe SP, Cornah J, Pinfield-Wells H, Soady K, Zhang Q, Gilday A, Dyer JM, Graham IA (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol J 7:694–703PubMedCrossRefGoogle Scholar
- Tanabe Y, Maruyama J-I, Yamaoka S, Yahagi D, Matsuo I, Tsutsumi N, Kitamoto K (2011) Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis. J Biol Chem 286:30455–30461PubMedCrossRefGoogle Scholar
- Thabet I, Guirimand G, Courdavault V, Papon N, Godet S, Dutilleul C, Bouzid S, Giglioli-Guivarc’h N, Clastre M, Simkin AJ (2011) The subcellular localization of periwinkle farnesyl diphosphate synthase provides insight into the role of peroxisome in isoprenoid biosynthesis. J Plant Physiol 168:2110–2116PubMedCrossRefGoogle Scholar
- Theodoulou FL, Eastmond PJ (2012) Seed storage oil catabolism: a story of give and take. Curr Opin Plant Biol 15:322–328PubMedCrossRefGoogle Scholar
- Theodoulou FL, Job K, Slocombe SP, Footitt S, Holdsworth M, Baker A, Larson TR, Graham IA (2005) Jasmonic acid levels are reduced in COMATOSE ATP-binding cassette transporter mutants. Implications for transport of jasmonate precursors into peroxisomes. Plant Physiol 137:835–840PubMedCrossRefGoogle Scholar
- Theodoulou FL, Zhang X, De Marcos LC, Nyathi Y, Baker A (2011) Peroxisomal transport systems: roles in signaling and metabolism. In: Geissler M, Venema K (eds) Signaling and comunications in plants, 1st edn. Springer, BerlinGoogle Scholar
- Trentmann O, Jung B, Neuhaus HE, Haferkamp I (2008) Non-mitochondrial ATP/ADP transporters accept phosphate as third substrate. J Biol Chem 283:36486–36493PubMedCrossRefGoogle Scholar
- Tsukaguchi H, Tokui T, Mackenzie B, Berger UV, Chen XZ, Wang Y, Brubaker RF, Hediger MA (1999) A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 399: 70–75PubMedCrossRefGoogle Scholar
- Tugal HB, Pool M, Baker A (1999) Arabidopsis 22-kilodalton peroxisomal membrane protein. Nucleotide sequence analysis and biochemical characterization. Plant Physiol 120:309–320PubMedCrossRefGoogle Scholar
- Van Moerkercke A, Schauvinhold I, Pichersky E, Haring MA, Schuurink RC (2009) A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production. Plant J 60:292–302PubMedCrossRefGoogle Scholar
- Van Roermund CWT, Hettema EW, Kal AJ, van den Berg M, Tabak HF, Wanders RJA (1998) Peroxisomal β-oxidation of polyunsaturated fatty acids in Saccharomyces cerevisiae: isocitrate dehydrogenase provides NADPH for reduction of double bonds at even positions. EMBO J 17:677–687PubMedCrossRefGoogle Scholar
- Van Roermund CWT, Ijlst L, Majczak W, Waterham HR, Folkerts H, Wanders RJA, Hellingwerf KJ (2012) Peroxisomal fatty acid uptake mechanism in Saccharomyces cerevisiae. J Biol Chem 287:20144–20153PubMedCrossRefGoogle Scholar
- Visser WF, van Roermund CW, Ijlst L, Hellingwerf KJ, Wanders RJ, Waterham HR (2005) Demonstration and characterization of phosphate transport in mammalian peroxisomes. Biochem J 389:717–722PubMedCrossRefGoogle Scholar
- Wachter A, Wolf S, Steininger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15–30PubMedCrossRefGoogle Scholar
- Weber A, Menzlaff E, Arbinger B, Gutensohn M, Eckerskorn C, Flügge UI (1995) The 2-oxoglutarate/malate translocator of chloroplast envelope membranes: molecular cloning of a transporter containing a 12-helix motif and expression of the functional protein in yeast cells. Biochemistry 34:2621–2627PubMedCrossRefGoogle Scholar
- Werner AK, Witte CP (2011) The biochemistry of nitrogen mobilization: purine ring catabolism. Trends Plant Sci 2011:7Google Scholar
- Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369PubMedCrossRefGoogle Scholar
- Widhalm JR, Ducluzeau A-L, Buller NE, Elowsky CG, Olsen LJ, Basset GJC (2012) Phylloquinone (vitamin K1) biosynthesis in plants: two peroxisomal thioesterases of lactobacillales origin hydrolyze 1,4-dihydroxy-2-naphthoyl-CoA. Plant J 71:205–215PubMedCrossRefGoogle Scholar
- Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603PubMedCrossRefGoogle Scholar
- Wiszniewski AAG, Zhou WX, Smith SM, Bussell JD (2009) Identification of two Arabidopsis genes encoding a peroxisomal oxidoreductase-like protein and an acyl-CoA synthetase-like protein that are required for responses to pro-auxins. Plant Mol Biol 69:503–515PubMedCrossRefGoogle Scholar
- Woodward OM, Köttgen A, Coresh J, Boerwinkle E, Guggino WB, Köttgen M (2009) Identification of a urate transporter, ABCG2, with a common functional polymorphism causing gout. Proc Natl Acad Sci USA 106:10338–10342PubMedCrossRefGoogle Scholar
- Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36: 1157–1162PubMedGoogle Scholar
- Yang Z, Ohlrogge JB (2009) Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis β-oxidation mutants. Plant Physiol 150:1981–1989PubMedCrossRefGoogle Scholar
- 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 127:1266–1278PubMedCrossRefGoogle Scholar