REVIEW article

Front. Plant Sci., 27 December 2011

Sec. Plant Physiology

Volume 2 - 2011 | https://doi.org/10.3389/fpls.2011.00103

Defining the Plant Peroxisomal Proteome: From Arabidopsis to Rice

  • NK

    Navneet Kaur 1

  • JH

    Jianping Hu 1,2*

  • 1. MSU-DOE Plant Research Laboratory, Michigan State University East Lansing, MI, USA

  • 2. Plant Biology Department, Michigan State University East Lansing, MI, USA

Abstract

Peroxisomes are small subcellular organelles mediating a multitude of processes in plants. Proteomics studies over the last several years have yielded much needed information on the composition of plant peroxisomes. In this review, the status of peroxisome proteomics studies in Arabidopsis and other plant species and the cumulative advances made through these studies are summarized. A reference Arabidopsis peroxisome proteome is generated, and some unique aspects of Arabidopsis peroxisomes that were uncovered through proteomics studies and hint at unanticipated peroxisomal functions are also highlighted. Knowledge gained from Arabidopsis was utilized to compile a tentative list of peroxisome proteins for the model monocot plant, rice. Differences in the peroxisomal proteome between these two model plants were drawn, and novel facets in rice were expounded upon. Finally, we discuss about the current limitations of experimental proteomics in decoding the complete and dynamic makeup of peroxisomes, and complementary and integrated approaches that would be beneficial to defining the peroxisomal metabolic and regulatory roadmaps. The synteny of genomes in the grass family makes rice an ideal model to study peroxisomes in cereal crops, in which these organelles have received much less attention, with the ultimate goal to improve crop yield.

Introduction

Eukaryotic cells compartmentalize specific biochemical reactions in membrane-bound subcellular organelles. Peroxisomes are small and dynamic single membrane-delimited organelles found in nearly all eukaryotic cells and perform a wide array of functions, which differ in different organisms and even vary depending on the tissue type and prevailing environmental conditions. Although peroxisomes in different organisms exhibit significant functional heterogeneities, two peroxisomal functions, i.e., β-oxidation of fatty acids and hydrogen peroxide (H2O2) catabolism, are universal. Strong defects in peroxisome biogenesis or core peroxisome metabolic functions lead to fatal disorders in humans and embryonic lethality in plants (Schrader and Fahimi, 2008; Kaur et al., 2009).

In the absence of a genome, the entire peroxisome protein complement is comprised of proteins that are nuclear encoded and translated on cytosolic ribosomes prior to import into the organelle. Further, peroxisomes are distinguished from other organelles by their ability to import fully folded proteins into the organelle matrix. The presence of conserved peroxisome targeting signals (PTSs) in the peroxisome matrix proteins facilitates their recognition by cytosolic receptors. These PTSs comprise of two types: the C-terminal tripeptide PTS1 (SKL and derivatives thereof), and the N-terminal nonapeptide PTS2 (RLX5HL and derivatives) that is cleaved post-import in mammals and plants. Once bound by the cytosolic receptors, the PTS-containing proteins are transported to the peroxisome membrane and delivered into the matrix, aided by several peroxisome membrane-associated proteins that form the docking complex and the importomer (Rucktaschel et al., 2011).

Peroxisomes serve as essential “nodes” in a number of metabolic networks within the cell through physical and metabolic links with other cellular compartments such as mitochondria, chloroplasts, and oil bodies. Besides their roles in β-oxidation of fatty acids and degradation of H2O2, plant peroxisomes also mediate pathways such as photorespiration, jasmonic acid biosynthesis, indole 3-butyric acid (IBA) metabolism, glyoxylate cycle, purine degradation, and further contribute toward pathogen defense and essential developmental processes such as embryogenesis and photomorphogenesis (Hayashi and Nishimura, 2003; Baker et al., 2006; Reumann and Weber, 2006; Kaur et al., 2009; Palma et al., 2009). The major protein constituents of plant peroxisomes had been well characterized, yet the complete makeup of these organelles was far from being decoded. Understanding the metabolic and regulatory networks in these vital organelles in model plant systems, and furthermore, crop species, will be highly beneficial to modern agriculture.

Peroxisome Proteomics Studies in Plants

Innovations in protein identification techniques coupled with high sensitivity instrumentation facilities have fueled the increased use of mass spectrometry-based proteomics to map subcellular (organelle) proteomes (Yates et al., 2005; Au et al., 2007; Yan et al., 2009; Wiederhold et al., 2010). Likewise, peroxisome proteomics have also been undertaken by various groups in diverse organisms encompassing yeasts, mammals, plants, and trypanosomes (Colasante et al., 2006; Saleem et al., 2006). Given its completely sequenced and annotated genome and a wide suite of readily available molecular genetic resources, Arabidopsis was naturally the top choice for this approach to decipher the plant peroxisome proteome. However, early peroxisome proteome analysis in Arabidopsis was hindered by the lack of good peroxisome purification protocols. A combination of factors, such as the fragility of peroxisomes, elevated secondary metabolite levels in Arabidopsis, adherence of peroxisomes to mitochondria and chloroplasts, and the low peroxisome number in leaf mesophyll cells, made high purity isolation of Arabidopsis peroxisomes a challenging task. Thus, initial proteomic studies of Arabidopsis peroxisomes from greening and etiolated cotyledons only identified a small number of known and putative novel peroxisomal proteins (Fukao et al., 2002, 2003). The development of an isolation protocol for Arabidopsis leaf peroxisomes, which uses a two successive density gradient centrifugation method, resulted in the successful identification of 36 known peroxisome proteins and dozens of candidate novel proteins, some of which were later confirmed to be peroxisome localized (Reumann et al., 2007). A parallel large scale experiment, which used density centrifugation followed by free-flow electrophoresis, purified peroxisomes from Arabidopsis suspension cultured cells and discovered over 20 possible novel peroxisomal proteins by mass spectrometry (Eubel et al., 2008). Apart from Arabidopsis, soybean (Glycine max), and spinach (Spinacia oleracea) peroxisomes were also subjected to proteome analysis. About 30 peroxisomal proteins were identified from purified peroxisomes from etiolated cotyledons of soybean, among them is an adenine nucleotide transporter (Arai et al., 2008a,b). A few new peroxisomal proteins, including two enzymes in phylloquinone (vitamin K1) biosynthesis, were discovered by spinach leaf peroxisome proteomics (Babujee et al., 2010).

The NSF-funded Arabidopsis peroxisome 2010 project was initiated in late 2006 and is near its completion. The major goal for this project was to discover novel peroxisomal components and reveal new peroxisomal functions in Arabidopsis. Using one-dimensional gel electrophoresis (1-DE) followed by liquid chromatography and tandem mass spectrometry (LC-MS/MS), in-depth proteome analysis of three Arabidopsis peroxisomal subtypes, i.e., those from green leaves, etiolated germinating seedlings, and senescent leaves, respectively, was performed. Using fluorescence microscopy, the subcellular localization of over 100 putative novel peroxisomal proteins identified from proteomics and in silico PTS searches of the Arabidopsis genome was tested, and peroxisomal targeting for about 50 of them was confirmed (Reumann et al., 2009; Quan et al., unpublished). From leaves of 4-week-old plants, 85 known peroxisomal proteins were detected, and another 14 novel proteins were assigned to peroxisomes after subcellular targeting validations (Reumann et al., 2009; Quan et al., 2010). From peroxisomes of etiolated seedlings, another 15 novel peroxisomal proteins were discovered by proteomics combined with subcellular targeting assays (Quan et al., unpublished).

The recent proteomic studies followed by subcellular targeting verifications significantly expanded the list of bona-fide plant peroxisome proteins. Using data from published studies of plant peroxisomes, including the proteome analyses mentioned above, we have compiled a reference proteome for Arabidopsis peroxisomes (Table 1). For proteins identified by mass spectrometry-based experiments, we only included those that carry obvious PTS, unless they were later confirmed to be peroxisomal by a second approach, e.g., fluorescent protein subcellular targeting assay or genetic analysis. This list of Arabidopsis peroxisomal proteins currently stands at 163, which can be divided into the following categories: 117 PTS-containing matrix proteins, 38 membrane proteins, and eight proteins lacking recognizable PTS information. The 98 PTS1-containing proteins carry 23 diverse PTS1s, and the 19 PTS2-containing proteins harbor seven different PTS2s. Six proteins in the PTS2-containing protein category also bear C-terminal PTS1 or PTS1-like sequences.

Table 1

Gene nameAt locusAnnotationAt PTSOs locusOs PTSReference
PTS-CONTAINING MATRIX PROTEINS
ACH2At1g01710Acyl-CoA thioesteraseSKLLOC_Os04g47120PKLEubel et al. (2008), Reumann et al. (2007, 2009), Tilton et al. (2000, 2004)
sT4At1g04290Thioesterase family proteinSNLLOC_Os01g65950SKLEubel et al. (2008), Reumann et al. (2007, 2009)
KAT1At1g047103-Ketoacyl-CoA thiolase 1RQx5HLLOC_Os02g57260RQx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Germain et al. (2001)
LOC_Os10g31950RQx5HL
ACX3At1g06290Acyl-CoA oxidase 3RAx5HI/SSVLOC_Os06g24704RAx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Adham et al. (2005), Eastmond et al. (2000b), Froman et al. (2000), Rylott et al. (2003), Zolman et al. (2000)
ACX6At1g06310Acyl-CoA oxidase 6RAx5HI/SSLLOC_Os11g39220RLx5HLAdham et al. (2005)
ACD31.2At1g06460Small heat shock proteinRLx5HF/PKLno matchMa et al. (2006)
NDA1At1g07180NADPH dehydrogenase A1SRILOC_Os01g61410SRICarrie et al. (2008)
UP6At1g16730Unknown protein 6SKLLOC_Os06g06630CRLReumann et al. (2009), Quan et al. (2010)
4Cl3At1g204804-Coumarate:CoA ligase 3SKLLOC_Os03g04000SKLEubel et al. (2008), Shockey et al. (2003)
OPCL1At1g20510OPC-8:0 ligase 1SKLLOC_Os03g04000*SKLEubel et al. (2008), Reumann et al. (2007, 2009), Kienow et al. (2008), Koo et al. (2006)
AAE1At1g20560Acyl-activating enzyme 1SKLLOC_Os03g04130SKLEubel et al. (2008), Reumann et al. (2009), Shockey et al. (2003)
LOC_Os03g04120SKL
LOC_Os02g02700SKL
LOC_Os01g24030SKL
CAT3At1g20620Catalase 3QKL-10LOC_Os03g03910QKL-10Eubel et al. (2008), Reumann et al. (2007, 2009), Du et al. (2008), Frederick and Newcomb (1969), Frugoli et al. (1996), Fukao et al. (2002, 2003), Zimmermann et al. (2006)
LOC_Os06g51150QKL-10
LOC_Os02g02400VKI-10
CAT1At1g20630Catalase 1QKL-10LOC_Os03g03910*QKL-10Eubel et al. (2008), Reumann et al. (2007, 2009), Du et al. (2008), Frederick and Newcomb (1969), Frugoli et al. (1996), Zimmermann et al. (2006)
ATF1At1g21770Acetyl transferase 1SSILOC_Os04g35200SSMReumann et al. (2007, 2009)
GGT1At1g23310Glutamate-glyoxylate aminotransferase 1SKMLOC_Os07g01760SRMEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002), Igarashi et al. (2003), Liepman and Olsen (2003)
DEG15At1g28320Deg/HtrA proteaseSKLLOC_Os05g41810SKIEubel et al. (2008), Helm et al. (2007), Schuhmann et al. (2008)
AAE14At1g30520Acyl-activating enzyme 14SSLLOC_Os08g03630noneBabujee et al. (2010)
st1At1g48320Small thioesterase 1AKLLOC_Os03g48480SKLReumann et al. (2009)
LOC_Os05g04660AKL
pxPfkBAt1g49350PfkB-type carbohydrate kinase family proteinSMLLOC_Os05g09370RMx5HLEubel et al. (2008), Lingner et al. (2011)
NQRAt1g49670NADH:quinone reductaseSRLLOC_Os09g28570AKLEubel et al. (2008), Reumann et al. (2007, 2009)
IndAAt1g50510Indigoidine synthase ARIx5HLLOC_Os08g39420SALEubel et al. (2008), Reumann et al. (2009)
ICDHAt1g54340NADP-dependent isocitrate dehydrogenaseSRLLOC_Os01g14580SKLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2003)
AAE18At1g55320Acyl-activating enzyme 18SRILOC_Os03g59080SKLShockey et al. (2003), Wiszniewski et al. (2009)
NSAt1g60550Naphthoate synthaseRLx5HLLOC_Os01g47350RLx5HLReumann et al. (2007)
LOC_Os02g43720RAx5HL
ECIAt1g65520Monofunctional enoyl CoA hydratase/isomerase cSKLLOC_Os05g45300*SKLEubel et al. (2008), Reumann et al. (2007, 2009), Goepfert et al. (2008)
PAO4At1g65840Polyamine oxidase 4SRMLOC_Os04g57550CRT∧Eubel et al. (2008), Kamada-Nobusada et al. (2008), Ono et al. (2011)
LOC_Os04g57560SRL
AAE12At1g65890Acyl-activating enzyme 12SRLLOC_Os09g38350ARLShockey et al. (2003), Wiszniewski et al. (2009)
LOC_Os03g03790SRL
LOC_Os04g57850SKM
HPRAt1g68010Hydroxypyruvate reductase 1SKLLOC_Os02g01150SKLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002), Mano et al. (1997), Pracharoenwattana et al. (2010)
GGT2At1g70580Glutamate-glyoxylate aminotransferase 2SRMLOC_Os07g01760*SRMEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002), Igarashi et al. (2003), Liepman and Olsen (2003)
ECH2At1g76150Monofunctional enoyl-CoA hydratase 2SSLLOC_Os09g37280SSLEubel et al. (2008), Reumann et al. (2007, 2009), Goepfert et al. (2006), Strader et al. (2011)
ATF2At1g77540AcetyltransferaseSSILOC_Os04g35200*SSMReumann et al. (2009)
NADK3At1g78590NADH Kinase 3SRYLOC_Os09g17680noneWaller et al. (2010)
OPR3At2g0605012-Oxophytodienoate reductase 3SRLLOC_Os08g35740SRMEubel et al. (2008), Reumann et al. (2007, 2009), Sanders et al. (2000), Schaller et al. (2000), Stintzi and Browse (2000)
LOC_Os02g35310SPL
SGAT1At2g13360Serine-glyoxylate aminotransferaseSRILOC_Os08g39300SRIEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002), Liepman and Olsen (2003)
MDH1At2g22780NAD+-malate dehydrogenase 1RIx5HLLOC_Os12g43630RMx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002, 2003), Cousins et al. (2008), Pracharoenwattana et al. (2007)
LOC_Os03g56280RIx5HL
UriAt2g26230UricaseSKLLOC_Os01g64520SKLEubel et al. (2008), Reumann et al. (2007, 2009)
st5At2g29590Small thioesterase 5SKLLOC_Os02g32200SKLReumann et al. (2009)
LOC_Os04g35590SKL
LOC_Os01g12910SKL
NDA2At2g29990NADPH dehydrogenase A2SRILOC_Os01g61410SRICarrie et al. (2008)
CHYH1At2g30650ATP-dependent caseinolytic Clp protease/crotonase family proteinAKLLOC_Os12g16350PKLLingner et al. (2011)
LOC_Os10g42210PKL
CHYH2At2g30660ATP-dependent caseinolytic Clp protease/crotonase family proteinAKLLOC_Os12g16350*PKLLingner et al. (2011)
LOC_Os10g42210*PKL
UP3At2g31670Unknown proteinSSLLOC_Os07g41810ANLReumann et al. (2007, 2009)
LOC_Os07g41820ANL
KAT2At2g331503-Ketoacyl-CoA thiolase 2RQx5HLLOC_Os02g57260*RQx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Germain et al. (2001), Zolman et al. (2000), Fukao et al. (2003), Afitlhile et al. (2005), Castillo et al. (2004), Footitt et al. (2007a), Hayashi et al. (1998), Pye et al. (2010)
LOC_Os10g31950*RQx5HL
ACX5At2g35690Acyl-CoA oxidase 5AKLLOC_Os06g01390SRLSchilmiller et al. (2007)
GLHAt2g38180GDSL motif lipase/hydrolase family proteinARLLOC_Os06g36520AMLEubel et al. (2008)
PM16At2g41790Peptidase family M16PKLLOC_Os07g38260MKLEubel et al. (2008), Reumann et al. (2009)
LOC_Os07g38270MKL
LOC_Os07g38280MKL
CuAOAt2g42490Copper amine oxidaseSKLLOC_Os04g40040SKLEubel et al. (2008), Reumann et al. (2009)
CSY3At2g42790Citrate synthase 3RLx5HL/SSVLOC_Os02g13840RLx5HL/SALEubel et al. (2008), Reumann et al. (2007, 2009), Pracharoenwattana et al. (2005)
PAO2At2g43020Polyamine oxidase 2SRLLOC_Os04g53190SRLKamada-Nobusada et al. (2008), Ono et al. (2011)
SOAt3g01910Sulfite oxidaseSNLLOC_Os08g41830SKMEubel et al. (2008), Reumann et al. (2007, 2009), Eilers et al. (2001), Lang et al. (2007)
LOC_Os12g25630SLL
SDRcAt3g01980Short-chain dehydrogenase/reductase cSYMLOC_Os03g63290SFMReumann et al. (2007, 2009), Lingner et al. (2011)
6PGDHAt3g02360Phosphogluconate dehydrogenaseSKILOC_Os06g02144AKMEubel et al. (2008), Reumann et al. (2007, 2009)
LACS6At3g05970Long-chain acyl-CoA synthetase 6RIx5HLLOC_Os12g04990RLx5HL/PKLEubel et al. (2008), Reumann et al. (2007, 2009), Fulda et al. (2004)
IBR3At3g06810IBA-response 3SKLLOC_Os07g47820ARMEubel et al. (2008), Reumann et al. (2009), Zolman et al. (2007, 2008)
MFP2At3g06860Fatty acid multifunctional protein 2SRLLOC_Os01g24680ARLEubel et al. (2008), Reumann et al. (2007, 2009), Arent et al. (2010), Eastmond and Graham (2000), Richmond and Bleecker (1999), Rylott et al. (2006)
LOC_Os05g06300ARM
LOC_Os05g29880SRL
SDRbAt3g12800Short-chain dehydrogenase/reductase bSKLLOC_Os04g52400SKLEubel et al. (2008), Reumann et al. (2007)
HAOX1At3g14150Hydroxy-acid oxidase 1SMLLOC_Os07g42440SLLReumann et al. (2009)
LOC_Os07g05820SRL
LOC_Os03g57220PRL
LOC_Os04g53210SRL
GO1At3g14415Glycolate oxidase 1PRLLOC_Os07g05820*SRLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002)
GO2At3g14420Glycolate oxidase 2ARLLOC_Os07g05820*SRLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002)
HBCDHAt3g15290Hydroxybutyryl-CoA dehydrogenasePRLLOC_Os01g58380SSLEubel et al. (2008), Reumann et al. (2007, 2009)
AAE7At3g16910Acyl-activating enzyme 7SRLLOC_Os03g19240SRMEubel et al. (2008), Reumann et al. (2009), Shockey et al. (2003), Turner et al. (2005a)
LOC_Os03g19250SRM
GPK1At3g17420Glyoxysomal protein kinase 1AKILOC_Os01g21960SSKFukao et al. (2003), Ma and Reumann (2008)
SCO3At3g19570Snowy Cotyledon 3SRLLOC_Os03g10820noneAlbrecht et al. (2010)
ICLAt3g21720Isocitrate lyaseSRMLOC_Os07g34520SRMFukao et al. (2003), Eastmond et al. (2000a), Olsen et al. (1993)
GR1At3g24170Glutathione reductase 1TNLLOC_Os02g56850TNLEubel et al. (2008), Reumann et al. (2007), Kataya and Reumann (2010)
BADHAt3g48170Aldehyde dehydrogenaseSKLLOC_Os08g32870SKLEubel et al. (2008), Reumann et al. (2007, 2009), Mitsuya et al. (2009)
LOC_Os04g39020SKL
MIFAt3g51660Macrophage migration inhibitory factorSKLLOC_Os11g01600noneReumann et al. (2007), Reumann et al. (2009), Li et al. (2009)
ACX4At3g51840Acyl-CoA oxidase 4SRLLOC_Os01g06600ARLEubel et al. (2008), Reumann et al. (2007, 2009), Rylott et al. (2003), Zolman et al. (2000), Hayashi et al. (1999)
LOC_Os05g07090SRL
LOC_Os06g23780ARL
MDAR1At3g52880Monodehydroascorbate reductase 1AKILOC_Os09g39380SKIEubel et al. (2008), Reumann et al. (2007, 2009), Lisenbee et al. (2005)
LOC_Os08g44340AKV
SDRAt3g55290Short-chain dehydrogenase/reductaseSSLLOC_Os08g39960SSLEubel et al. (2008), Reumann et al. (2007, 2009)
ZnDHAt3g56460Zinc-binding dehydrogenaseSKLLOC_Os05g24880SRLEubel et al. (2008), Reumann et al. (2009)
HIT3At3g56490Histidine triad family protein 3RVx5HFLOC_Os01g59750RLx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Quan et al. (2010), Guranowski et al. (2010)
LOC_Os11g18990RLx5HL
CPAt3g57810Cysteine proteaseSKLLOC_Os09g31280SRLLingner et al. (2011)
CSY2At3g58750Citrate synthase 2RLx5HL/SALLOC_Os02g13840*RLx5HL/SALEubel et al. (2008), Reumann et al. (2009), Pracharoenwattana et al. (2005)
PAO3At3g59050Polyamine oxidase 3SRMLOC_Os04g53190*SRLKamada-Nobusada et al. (2008), Ono et al. (2011), Moschou et al. (2008)
st3At3g61200Small thioesterase 3SKLLOC_Os07g27960ASLEubel et al. (2008), Reumann et al. (2009), Fukao et al. (2003)
ACHAt4g00520Acyl-CoA thioesterase family proteinAKLLOC_Os04g47120*PKLEubel et al. (2008)
EH3At4g02340Epoxide hydrolase 3ASLLOC_Os05g19150AEMEubel et al. (2008), Reumann et al. (2007, 2009)
LOC_Os01g15120SKF
LOC_Os03g61340SRL
LOC_Os10g35520RQx4HL
MCDAt4g04320Malonyl-CoA decarboxylaseSRLLOC_Os09g23070noneEubel et al. (2008), Reumann et al. (2009), Carrie et al. (2009)
4CL1At4g051604-Coumarate:CoA ligase 1SKMLOC_Os03g05780SKLEubel et al. (2008), Reumann et al. (2007, 2009), Kienow et al. (2008), Schneider et al. (2005)
LOC_Os10g42800SRL
LOC_Os07g17970SRL
IBR1At4g05530Indole-3-butyric acid response 1SRLLOC_Os09g04730SRLEubel et al. (2008), Reumann et al. (2007, 2009), Wiszniewski et al. (2009), Zolman et al. (2008)
IBR10At4g14430Indole-3-butyric acid response 10PKLLOC_Os05g45300SKLReumann et al. (2007, 2009), Goepfert et al. (2008), Zolman et al. (2008)
ECHIAAt4g16210Monofunctional enoyl-CoA hydratase/isomerase aSKLLOC_Os03g19680SKLEubel et al. (2008), Reumann et al. (2007, 2009)
HIT1At4g16566Histidine triad family protein 1SKVLOC_Os01g59750*RLx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Guranowski et al. (2010)
ACX1At4g16760Acyl-CoA oxidase 1ARLLOC_Os06g01390*SRLEubel et al. (2008), Reumann et al. (2009), Adham et al. (2005), Castillo et al. (2004), Schilmiller et al. (2007), Hooks et al. (1999), Pinfield-Wells et al. (2005)
GO3At4g18360Glycolate oxidase 3AKLLOC_Os03g57220*PRLEubel et al. (2008), Reumann et al. (2007, 2009)
4Cl5At4g190104-Coumarate:CoA ligase 5SRLLOC_Os08g04770SKLShockey et al. (2003)
NDB1At4g28220NADPH dehydrogenase B1SRILOC_Os06g47000SRICarrie et al. (2008)
LOC_Os05g26660SSL
AIM1At4g29010Abnormal inflorescence meristem 1SKLLOC_Os02g17390SRMEubel et al. (2008), Reumann et al. (2009), Richmond and Bleecker (1999), Delker et al. (2007)
CAT2At4g35090Catalase 2QKL-10LOC_Os03g03910*QKL-10Eubel et al. (2008), Reumann et al. (2007, 2009), Frederick and Newcomb (1969), Frugoli et al. (1996), Fukao et al. (2002), Zimmermann et al. (2006)
AGT2At4g39660Alanine: glyoxylate aminotransferase 2SRLLOC_Os03g07570SGLLiepman and Olsen (2003)
LOC_Os03g21960SKL
LOC_Os05g39770SKL
MLSAt5g03860Malate synthaseSRLLOC_Os04g40990CKLFukao et al. (2003), Olsen et al. (1993), Cornah et al. (2004)
BIOTIN FAt5g046207-Keto-8-aminopelargonic acid synthasePKLLOC_Os01g53450SKLTanabe et al. (2011)
LOC_Os10g41150SKL
MDH2At5g09660NAD+-malate dehydrogenase 2RIx5HLLOC_Os12g43630*RMx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Cousins et al. (2008), Pracharoenwattana et al. (2007)
LOC_Os03g56280*RIx5HL
ASP3At5g11520Aspartate aminotransferaseRIx5HLLOC_Os01g55540RLx5HLEubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2002), Mettler and Beevers (1980), Schultz and Coruzzi (1995)
ELT1At5g11910Esterase/lipase/thioesterase family 1SRILOC_Os01g39790SSAReumann et al. (2009)
LOC_Os05g46210PKL
AAE5At5g16370Acyl-activating enzyme 5SRMLOC_Os04g57850*SKMEubel et al. (2008), Reumann et al. (2007, 2009), Shockey et al. (2003)
ATMS1At5g17920Cobalamin-independent methionine synthaseSAKLOC_Os12g42884SAKReumann et al. (2007), Reumann et al. (2009)
CSD3At5g18100Copper/zinc superoxide dismutase 3AKLLOC_Os03g11960SAVEubel et al. (2008), Reumann et al. (2007, 2009), Kliebenstein et al. (1998)
NUDT19At5g20070Nudix hydrolase homolog 19SSLLOC_Os06g04910SNLBabujee et al. (2010)
AAE17At5g23050Acyl-activating enzyme 17SKLLOC_Os09g21230SKIEubel et al. (2008), Reumann et al. (2009), Shockey et al. (2003)
MIA40At5g23395Mitochondrial intermembrane space assembly machinery 40SKLLOC_Os04g44550PKLCarrie et al. (2010)
6PGLAt5g244006-Phosphoglu conolactonaseSKLLOC_Os08g43370SSIReumann et al. (2007)
LACS7At5g27600Long-chain acyl-CoA synthetase 7RLx5HI/SKLLOC_Os11g04980RLx5HL/SKLEubel et al. (2008), Reumann et al. (2007, 2009), Fulda et al. (2004)
AtHsp15.7At5g37670Heat shock protein similar to 17.6 kDa class ISKLLOC_Os06g14240SKLMa et al. (2006)
GSTT1At5g41210Glutathione S-transferase θ isoform 1SKILOC_Os11g37730SKLEubel et al. (2008), Reumann et al. (2007, 2009), Dixon et al. (2009)
LOC_Os11g37750SKL
SCP2At5g42890Sterol carrier protein 2SKLLOC_Os02g52720SKLEubel et al. (2008), Reumann et al. (2007, 2009), Edqvist et al. (2004), Zheng et al. (2008)
AtDCIAt5g43280Δ3,5-Δ2,4-Enoyl-CoA-isomeraseAKLLOC_Os01g70090SKLEubel et al. (2008), Reumann et al. (2007, 2009), Goepfert et al. (2005)
UP5At5g44250Unknown protein 5SRLLOC_Os11g40070SKLReumann et al. (2009)
LON2At5g47040Lon protease homolog 2SKLLOC_Os09g36300SKLReumann et al. (2009), Lingard and Bartel (2009)
ACAT1.3At5g47720Acetoacetyl-CoA thiolase 1.3SALLOC_Os01g02020SSLCarrie et al. (2007)
HIT2At5g48545Histidine triad family protein 2RLx5HLLOC_Os11g18990*RLx5HLReumann et al. (2009), Guranowski et al. (2010)
LOC_Os12g13120RLx5HL
KAT5At5g488803-Ketoacyl-CoA thiolase 5RQx5HLLOC_Os02g57260*RQx5HLReumann et al. (2007, 2009), Germain et al. (2001), Castillo et al. (2004)
TLPAt5g58220Transthyretin-like proteinRLx5HL#LOC_Os03g27320RMx5HL#Eubel et al. (2008), Reumann et al. (2007, 2009), Lamberto et al. (2010)
4CL2At5g633804-Coumarate:CoA ligase 2SKLLOC_Os01g67540SRLReumann et al. (2009), Kienow et al. (2008), Schneider et al. (2005)
ACX2At5g65110Acyl-CoA oxidase 2RIx5HLLOC_Os11g39220*RIx5HLEubel et al. (2008), Reumann et al. (2009), Adham et al. (2005), Hooks et al. (1999)
UP7At5g65400Unknown protein 7SLMLOC_Os04g37710noneReumann et al. (2009)
CHY1At5g659403-Hydroxyisobutyryl-CoA hydrolaseAKLLOC_Os12g16350PKLEubel et al. (2008), Reumann et al. (2009), Lange et al. (2004), Zolman et al. (2001a)
Gene nameAt locusAnnotationOs locusReference
PEROXISOME MEMBRANE PROTEINS
PEX11cAt1g01820Peroxin 11 cLOC_Os06g03660Lingard et al. (2008), Lingard and Trelease (2006), Orth et al. (2007), Nito et al. (2007)
PEX6At1g03000Peroxin 6LOC_Os04g52690Delker et al. (2007), Zolman and Bartel (2004)
PEX7At1g29260Peroxin 7LOC_Os02g14790Hayashi et al. (2005), Ramon and Bartel (2011), Singh et al. (2009), Woodward and Bartel (2005)
PEX11aAt1g47750Peroxin 11aLOC_Os03g19010Lingard et al. (2008), Lingard and Trelease (2006), Orth et al. (2007)
LOC_Os03g19000
PEX3BAt1g48635Peroxin 3 isoform BLOC_Os09g14510Nito et al. (2007), Hunt and Trelease (2004)
PEX2At1g79810Peroxin 2LOC_Os05g19480Nito et al. (2007), Hu et al. (2002), Prestele et al. (2010), Sparkes et al. (2005)
DRP3BAt2g14120Dynamin-related protein 3BLOC_Os01g69130Arimura et al. (2004), Arimura and Tsutsumi (2002), Fujimoto et al. (2009), Zhang and Hu (2009)
LOC_Os04g31190
PEX10At2g26350Peroxin 10LOC_Os07g41800Nito et al. (2007), Prestele et al. (2010), Flynn et al. (2005), Schumann et al. (2003, 2007), Sparkes et al. (2003)
PEX16At2g45690Peroxin 16LOC_Os02g03070Nito et al. (2007), Karnik and Trelease (2005, 2007), Lin et al. (1999, 2004)
PEX11dAt2g45740Peroxin 11dLOC_Os03g02590Lingard et al. (2008), Lingard and Trelease (2006), Orth et al. (2007)
PEX19AAt3g03490Peroxin 19 isoform ALOC_Os02g44220Nito et al. (2007), Hadden et al. (2006)
PEX12At3g04460Peroxin 12LOC_Os10g32960Nito et al. (2007), Prestele et al. (2010), Fan et al. (2005), Mano et al. (2006)
PEX13At3g07560Peroxin 13LOC_Os07g05810Nito et al. (2007), Mano et al. (2006), Boisson-Dernier et al. (2008)
APEM9At3g10572Aberrant peroxisome morphology 9LOC_Os06g48970Goto et al. (2011)
PEX3AAt3g18160Peroxin 3 isoform ALOC_Os09g14510*Nito et al. (2007), Hunt and Trelease (2004)
DRP5BAt3g19720Dynamin-related protein 5BLOC_Os12g07880Zhang and Hu (2010)
PEX22At3g21865Peroxin 22LOC_Os04g53690Lingard et al. (2009), Zolman et al. (2005)
LOC_Os04g57680
PEX11bAt3g47430Peroxin 11bLOC_Os04g45210Lingard and Trelease (2006), Orth et al. (2007), Desai and Hu (2008)
FIS1AAt3g57090Fission 1 isoform ALOC_Os03g24060Delker et al. (2007), Zheng et al. (2008), Lingard et al. (2008), Zhang and Hu (2009), Scott et al. (2006)
LOC_Os05g31770
LOC_Os01g72280
PEX11eAt3g61070Peroxin 11eLOC_Os06g03660*Lingard et al. (2008), Lingard and Trelease (2006), Orth et al. (2007)
DRP3AAt4g33650Dynamin-related protein 3ALOC_Os01g69130*Arimura et al. (2004), Fujimoto et al. (2009), Zhang and Hu (2009), Mano et al. (2004)
LOC_Os04g31190*
PEX1At5g08470Peroxin 1LOC_Os08g44240Nito et al. (2007), Charlton et al. (2005)
FIS1BAt5g12390Fission 1 isoform BLOC_Os05g31770*Zheng et al. (2008), Lingard et al. (2008), Zhang and Hu (2009)
LOC_Os01g72280*
LOC_Os03g24060*
PEX19BAt5g17550Peroxin 19 isoform BLOC_Os02g44220*Nito et al. (2007), Hadden et al. (2006)
PEX4At5g25760Peroxin 4LOC_Os02g42314Nito et al. (2007), Lingard et al. (2009), Zolman et al. (2005)
PEX5At5g56290Peroxin 5LOC_Os08g39080Hayashi et al. (2005), Ramon and Bartel (2011), Woodward and Bartel (2005), Brown et al. (2011); Khan and Zolman (2010)
PEX14At5g62810Peroxin 14LOC_Os05g01090Eubel et al. (2008), Reumann et al. (2007, 2009), Hayashi et al. (2000), Nito et al. (2002)
PNC1At3g05290Peroxisomal adenine nucleotide carrier 1LOC_Os05g32630Eubel et al. (2008), Arai et al. (2008a), Linka et al. (2008)
CDCAt3g55640Ca2+-dependent carrierLOC_Os03g16080Carrie et al. (2009)
LOC_Os01g04990
PMD1At3g58840Peroxisomal and Mitochondrial Division Factor 1no matchAung and Hu (2011)
PMP22At4g04470Peroxisomal membrane protein of 22 kDaLOC_Os02g13270Eubel et al. (2008), Murphy et al. (2003), Tugal et al. (1999)
LOC_Os08g45210
LOC_Os01g12800
PXA1/CTSAt4g39850Peroxisomal ABC transporter 1/ComatoseLOC_Os01g73530 LOC_Os05g01700Eubel et al. (2008), Reumann et al. (2009), Footitt et al. (2002), Hayashi et al. (2002), Hooks et al. (2007), Kunz et al. (2009), Nyathi et al. (2010), Theodoulou et al. (2005), Zhang et al. (2011), Zolman et al. (2001b)
PNC2At5g27520Peroxisomal adenine nucleotide carrier 2LOC_Os05g32630*Eubel et al. (2008), Arai et al. (2008a), Linka et al. (2008)
PXN/PMP38/PMP36At2g39970Peroxisomal membrane protein of 36 kDaLOC_Os03g15860Eubel et al. (2008), Reumann et al. (2009), Bernhardt et al. (2011), Fukao et al. (2001)
LOC_Os02g13170
LOC_Os09g33470
PEN2At2g44490Penetration 2LOC_Os06g21570Bednarek et al. (2009), Clay et al. (2009), Lipka et al. (2005), Westphal et al. (2008), Maeda et al. (2009)
LOC_Os04g39880
LOC_Os04g39900
MDAR4At3g27820Monodehydroascorbate reductase 4LOC_Os02g47800Reumann et al. (2009), Lisenbee et al. (2005), Eastmond (2007)
LOC_Os02g47790
APX3At4g35000Ascorbate peroxidase 3LOC_Os08g43560Eubel et al. (2008), Reumann et al. (2007, 2009), Fukao et al. (2003), Fukao et al. (2002), Lisenbee et al. (2003), Narendra et al. (2006)
LOC_Os04g14680
DHARAt1g19570Dehydroascorbate reductase 1LOC_Os05g02530Reumann et al. (2009)
LOC_Os06g12630
PEROXISOME PROTEINS LACKING PTS
GLX1At1g11840Glyoxylase I homologLOC_Os08g09250Reumann et al. (2009), Quan et al. (2010)
SMP2At2g02510Short membrane protein 2LOC_Os02g35610Abu-Abied et al. (2009)
SOXAt2g24580Sarcosine oxidaseLOC_Os09g32290Goyer et al. (2004)
LOC_Os12g35890
LOC_Os01g21380
CoAEAt2g27490Dephospho-CoA kinaseLOC_Os01g25880Reumann et al. (2009)
B12D1At3g48140Senescence-associated protein/B12D-related proteinLOC_Os07g17330Reumann et al. (2009)
LOC_Os07g17310
LOC_Os06g13680
NDPK1At4g09320Nucleoside diphosphate kinase type 1LOC_Os10g41410Reumann et al. (2009)
CPK1At5g04870Calcium dependent protein kinase 1LOC_Os12g30150Coca and San Segundo (2010)
LOC_Os07g06740
LOC_Os03g57450
ACAT2At5g48230Acetoacetyl-CoA thiolase 2LOC_Os09g07830Reumann et al. (2007, 2009)

Peroxisomal proteins in Arabidopsis and rice.

*Loci that have already been listed once; #internal PTS2; ∧proven localization; QKL (−10) in catalases are positioned 10 amino acids from the C-terminus.

Some Novel Aspects of Plant Peroxisomes Revealed by Experimental Proteomics

Results from mass spectrometry-based proteomics studies in plants suggested novel metabolic and regulatory functions of peroxisomes in processes such as auxiliary β-oxidation, detoxification, nucleic acid metabolism, protein degradation, plant defense, and other metabolic processes (Kaur et al., 2009; Reumann, 2011). Several examples that represent plant-specific features of peroxisomes are described here. More examples can be found in a recent review (Reumann, 2011).

Histidine triad family

Histidine Triad (HIT) proteins belong to an evolutionarily conserved superfamily of nucleotide binding proteins whose defining feature is the H-φ-H-φ-H-φ−φ motif, where φ represents a hydrophobic amino acid. HIT proteins act as hydrolases or transferases on a multitude of nucleotide conjugate substrates (Brenner, 2002). The consequences of loss of HIT activity have various effects, from tumor formation in mammals, high temperature sensitive growth on galactose in yeast, to a reduction of bacterial growth in the presence of d-alanine (Bieganowski et al., 2002; Bardaweel et al., 2011; Martin et al., 2011), yet the exact roles for HIT proteins in these processes remain unclear. Animal HIT proteins have been reported to be cytosolic, nuclear, or mitochondrial (Huber and Weiske, 2008), and none was shown to be associated with peroxisomes. In contrast, three out of the five Arabidopsis HIT proteins (HIT1, 2, and 3) were detected in proteomics experiments (Reumann et al., 2007, 2009; Eubel et al., 2008) and later confirmed to be localized in peroxisomes (Reumann et al., 2009). HIT2 carries a characteristic PTS2, and the PTS1-like sequence on HIT1 (SKV>) and PTS2-like sequence on HIT3 (RVx5HF) were later confirmed to be functional PTSs (Reumann et al., 2009; Quan et al., 2010). The occurrence of these proteins in peroxisomes appears to be a plant-specific phenomenon, as the Arabidopsis HIT PTSs are also conserved in their homologs in other plant species such as rice (Table 1). A recent in vitro study showed that most of the Arabidopsis HIT proteins can function as sulfohydrolases by catalyzing the conversion of adenosine 5′-phosphosulfate (APS) to AMP and sulfate (; Guranowski et al., 2010). This study also showed that, in the presence of orthophosphate (Pi), HIT1/Hint4 exhibited APS phosphorylase activity as well, resulting in the formation of ADP. Moreover, this activity was determined to be pH dependent, with HIT1 exclusively (and more efficiently) catalyzing this reaction at acidic pHs. Considering their enzymatic activity, it is possible that the three peroxisomal HIT proteins are involved in recycling the pool of adenosine nucleotides in the peroxisome. Based on the pH specific activity of HIT1, we speculate that this protein may serve to buffer peroxisomal pH. Phenotypic and functional characterization of these HIT proteins will be needed to address their role in the peroxisome and in plant physiology.

Peroxisomal NADPH production

Many peroxisomal enzymes consume NADPH during reductive reactions. For instance, several enzymes involved in JA biosynthesis (OPR3), auxiliary β-oxidation (ECRs, SDRa), and detoxification (MDAR, GR, NQR), require NADPH for their activity, underscoring the critical need for this cofactor in the peroxisome (Nyathi and Baker, 2006; Kaur et al., 2009). Several NADPH dehydrogenases are also found in the peroxisome (Carrie et al., 2008). To maintain optimal activities of these enzymes, the diminishing NADPH pool needs to be continuously replenished. In addition to providing reducing equivalents, NAPDH is also essential in oxidative damage response and peroxisome protein import (Juhnke et al., 1996; Pool et al., 1998; Pollak et al., 2007).

In plants, the plastid localized oxidative pentose phosphate pathway (OPPP) is a primary source of NADPH. OPPP consists of a three-enzyme cascade comprising of glucose-6-phosphate dehydrogenase (G6PD), 6-phosphogluconolactonase (6PGL), and 6-phosphogluconate dehydrogenase (6PGDH). These enzymes act sequentially to convert glucose-6-phosphate to ribose-5-phosphate with the concomitant production of NADPH (Kruger and von Schaewen, 2003). Besides the OPPP, NADPH is also generated by NADP-dependent isocitrate dehydrogenase (ICDH), malic enzyme (ME), aldehyde dehydrogenase (ALDH), and NAD kinase (NADK; Pollak et al., 2007). Some earlier studies indicated that the NADPH generating enzymes in OPPP and ICDH are compartmentalized in plant peroxisomes (Donaldson, 1982; Corpas et al., 1998; del Rio et al., 2002; Mateos et al., 2003). In yeasts, the presence of peroxisomal ICDH is also necessary for β-oxidation of unsaturated fatty acids and NADPH is critical to dissipate H2O2 (Henke et al., 1998; van Roermund et al., 1998; Minard and McAlister-Henn, 1999). Arabidopsis peroxisome proteomics studies detected ICDH and 6PGDH and subcellular targeting studies validated their peroxisomal localization (Fukao et al., 2002, 2003; Reumann et al., 2007, 2009; Eubel et al., 2008). Although not identified in proteomics experiments, 6PGL was shown to be a dual localized protein carrying an N-terminal transit peptide directing it to chloroplasts and a C-terminal PTS1 targeting it to peroxisomes (Reumann et al., 2007). Interestingly, although the chloroplast targeting of 6PGL is indispensable for viability, plants were unaffected in the absence of a peroxisome localized isoform (Xiong et al., 2009), strengthening the notion that plant peroxisomes have alternative sources for NADPH generation. The only enzyme missing from the set of peroxisomal OPPP was recently found to be the plastidic G6PD1, which was selectively recruited to the peroxisomes under conditions that promote transient oxidation events. This study further demonstrated the cysteine dependent heterodimer formation between the plastid targeted G6PD1 isoform and a catalytically inactive isoform G6PD4, and the import of this heterodimer into peroxisomes (Meyer et al., 2011). As such, peroxisomes seem to have a complete set of OPPP enzymes.

De novo biosynthesis of NADPH also occurs in peroxisomes by the preferential phosphorylation of NADH by NADK3 (Turner et al., 2005a,b). Though not found in proteomics studies, NADK3 has been localized to peroxisomes via a novel PTS1, SRY> (Waller et al., 2010). Lastly, ALDHs are classified as NADP-dependent enzymes that detoxify aldehyde substrates (Kirch et al., 2004). Mammals possess multiple isoforms of ALDHs, which were found to be induced by oxidative stress; one particular isoform was linked to the prevention of oxidative damage (Pappa et al., 2003; Vasiliou and Nebert, 2005). Peroxisome proteomic analysis in Arabidopsis has repeatedly identified an ALDH, BADH, which has a putative role in polyamine degradation (Reumann et al., 2007, 2009; Eubel et al., 2008). Whether this protein contributes to the maintenance of peroxisomal redox homeostasis/NADP turnover needs to be ascertained. Thus, plant peroxisomes seem to have several routes to maintain a supply of NADPH within the organelle, possibly as a countermeasure for the dangers posed by oxidative stress emanating from unchecked/continuous H2O2 generated within the peroxisome.

Metabolite transporters

Proteomic analysis of the soybean peroxisomal membrane proteins led to the identification of a soybean peroxisomal adenine nucleotide transporter and later on two homologous proteins (PNC1, PNC2) from Arabidopsis (Arai et al., 2008b). An independent study of peroxisome membrane proteins isolated from Arabidopsis suspension cultured cells also identified PNC2 as a novel constituent of the peroxisome membrane (Eubel et al., 2008). A bioinformatics based approach followed by cell biological and biochemical validations found PNC1 and PNC2 as adenine nucleotide transporters in Arabidopsis as well (Linka et al., 2008). Consistent with the ATP transporter activity of the PNCs, their RNAi lines were sucrose dependent for seedling establishment and impaired in post-germinative lipid mobilization. Functional analysis of the PNCs highlights the critical need for ATP within peroxisomes and reinforces the notion that these proteins are the sole purveyors of ATP transport into peroxisomes (Arai et al., 2008b; Linka et al., 2008).

PMP38/PXN, like the PNCs, is also a member of the mitochondrial carrier family. It was initially identified as an integral peroxisome membrane protein in pumpkin cotyledons and considered to be a potential ATP/ADP transporter (Fukao et al., 2001). The presence of PMP38 in Arabidopsis peroxisomes was subsequently detected in isolated peroxisomes from proteomics works using suspension cultured cells and adult leaves (Eubel et al., 2008; Reumann et al., 2009). However, this protein failed to complement a yeast adenine nucleotide mutant (Linka et al., 2008) but instead was found to serve as an NAD+ carrier involved in peroxisomal β-oxidation (Bernhardt et al., 2011).

Peroxisome proteins lacking PTS

Dehydroascorbate reductase (DHAR) is part of the peroxisomal ascorbate-glutathione (PAG) cycle, which encompasses the enzymes MDAR1, MDAR4, APX3, and glutathione reductase (GR) and plays a key role in antioxidant metabolism (Kaur et al., 2009). DHAR was found to be peroxisomal in pea and tomato (Jimenez et al., 1997; Mittova et al., 2003), but was missing from the Arabidopsis PAG pathway until its proteomic identification and subcellular localization validation (Reumann et al., 2009). Glyoxylase I (GLXI) is another protein without obvious PTS identified from the leaf peroxisome proteome (Reumann et al., 2009). GLX system disposes of toxic byproducts such as methylglyoxal in two consecutive steps catalyzed by GLXI and GLXII (Mannervik, 2008; Yadav et al., 2008; Inoue et al., 2011). The verification of GLXI in the peroxisome expanded the suite of detoxification related proteins found in the peroxisome and indicated that half of the GLX pathway is compartmentalized in peroxisomes in Arabidopsis (Quan et al., 2010).

The plant-specific, senescence-associated B12D gene encodes for a small protein lacking any recognizable PTS. It was only detected in the proteome of leaf peroxisomes, and as a C-terminal YFP fusion was found to target to peroxisomes (Reumann et al., 2009). B12D genes in monocots such as barley and wheat are expressed during seed development but cease to be transcribed at seed maturity (Aalen et al., 1994, 2001; McIntosh et al., 2007). The germinating seed is purported to induce the expression of these genes via a putative gibberellic acid (GA) responsive promoter element. Consistent with this notion, the expression of this gene was found to be induced by GA but suppressed by abscisic acid (ABA; Steinum et al., 1998). Although no function has been attributed to B12D, the gene expression pattern suggests its role in seed germination/dormancy.

Dephospho-CoA kinase (CoAE) was identified in leaf peroxisome proteomics and localized to the periphery of the peroxisome membrane as a YFP fusion (Reumann et al., 2009). Coenzyme A (CoA) and derivatives thereof are the major currency behind many cellular metabolic pathways. CoA biosynthesis is accomplished in five successive enzymatic steps, the last of which is carried out by CoAE (Leonardi et al., 2005). Though the in planta effects of some of the enzymes catalyzing the preceding steps in CoA biosynthesis have been studied, the physiological role of CoAE in plants has not been analyzed (Rubio et al., 2006, 2008; Tilton et al., 2006). Given the number of β-oxidation reactions that require CoA, it will be necessary to determine the effect of CoAE on peroxisome metabolism.

Nucleoside diphosphate kinase type 1 (NDPK1) was another unexpected peroxisomal protein to be found through proteomics, and was seen to localize to peroxisomes as well as the cytosol and nucleus (Reumann et al., 2009). This multi-localization is perhaps not so surprising in light of the even more promiscuous localization reported for the mammalian NDPKs (Bosnar et al., 2009). NDPKs catalyze the interconversion of nucleoside diphosphates by transferring the phosphate group from a nucleoside triphosphates (NTP) to any other nucleoside diphosphates (NDP) except for ADP (Yegutkin, 2008). In view of this, NDPK1 might serve to regulate the concentration of different nucleotide phosphates within the peroxisome.

Peroxisome Proteome in Rice

The need to study peroxisomes in the monocot crop plant, rice

The pivotal roles of peroxisomes in plant development and stress responses make it highly necessary to study these organelles in crop plants, with the goal to improve the quality and yield of crop species. Rice (Oryza sativa) is one the three major staple food crops in the world and a model system for basic research in monocot plants. Traditionally, plant peroxisome studies have mainly focused on dicot species such as cucumber, pumpkin, watermelon, and pea (Beevers, 1979), and lately, Arabidopsis (Kaur et al., 2009); however, very little research has been carried out with these organelles in monocots, which differ significantly from dicots in architecture and physiology. Having a completely sequenced and well annotated genome, well developed transformation methods, and rich genetic and mutant resources, rice is deemed to be the logical choice for a model system to study peroxisome functions in monocot plants.

Despite the fact that rice has a larger genome than Arabidopsis, the advantages of studying rice orthologs of Arabidopsis genes have been exemplified by a number of cases, in which mutant phenotypes were revealed in rice but not in Arabidopsis mutant due to functional redundancy among gene family members in the latter. The best example is the identification of the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1 (GID1) from rice, in which the gid1 mutant shows a strong GA insensitive dwarf phenotype (Ueguchi-Tanaka et al., 2005). In contrast, three GID1 homologs exist in Arabidopsis and as a result, phenotypes could only be shown in higher order mutants whereas single mutant is indistinguishable from the wild-type plants (Griffiths et al., 2006). T-DNA insertion mutants for many of the new peroxisome genes we recently identified have no apparent phenotypes (Cassin and Hu, unpublished). Studying mutants of their orthologs in rice may be an easier way to decipher the functions of some of these proteins.

Studying peroxisomes in rice may also have applications in engineering the more efficient C4 photosynthetic pathway into C3 crops for yield increase. Rice is a C3 plant growing in warm environment, which favors photorespiration and thus reduces photosynthesis. However, in rice cells chloroplasts and stromules occupy 95% of the cell periphery, whereas peroxisomes and mitochondria, players in photorespiration, are present in the interior of the cell and lined up along the chloroplast walls (Sage and Sage, 2009). This interesting anatomy of rice mesophyll cells, which is atypical for a C3 plant, was suggested to be significant in scavenging photorespiratory CO2 to enhance the carboxylation capability of Rubisco for CO2 refixation. In C3 plants, peroxisomes were found to be responsible for the vast majority of the H2O2 produced during photorespiration (Foyer and Noctor, 2003). It would be interesting to investigate whether there are any changes to the activity of rice peroxisomal photorespiratory enzymes in association with these organelle rearrangements.

In silico analysis of the rice peroxisome proteome

As a first step toward exploring the peroxisome proteome in cereal crop species, we performed an in silico analysis of the rice peroxisome proteome by searching the rice genome for proteins with sequence similarities with the Arabidopsis peroxisomal proteins (Table 1). Remarkably, with the exception of two proteins, every Arabidopsis peroxisome protein seems to have at least one homolog in rice. One exception is ACD31.2, a small heat shock protein. It is interesting that this protein as well as its PTS2 peptide are well conserved in most plant species (Ma et al., 2006) but entirely missing from rice. Another protein without an apparent homolog in rice is peroxisome and mitochondrial division factor 1 (PMD1), a plant-specific dual localized membrane protein involved in the proliferation of peroxisomes and mitochondria in Arabidopsis (Aung and Hu, 2011). Altogether, the putative rice peroxisome proteome consists of 133 matrix proteins, 47 membrane proteins, and 14 proteins with no apparent PTSs. Among the candidate peroxisome matrix proteins in rice, most proteins contain PTS1 or PTS2-like sequences just like their Arabidopsis counterparts, suggesting that these proteins are highly likely to be peroxisomal. Proteins which appear to have lost PTS1 signal include snowy cotyledon3 (SCO3), the dual localized malonyl-CoA decarboxylase (MCD; Carrie et al., 2008), a protein of unknown function (UP7), NADK3 (Waller et al., 2010), AAE14 (Babujee et al., 2010), and macrophage migration inhibitory factor, MIF (Li et al., 2009). Despite having a C-terminal PTS1, Arabidopsis SCO3 is actually localized to the periphery of peroxisomes and influences plastid development possibly through interaction with the cytoskeleton (Albrecht et al., 2010). Hence, the loss of the matrix targeting signal PTS1 in its rice homolog is not that surprising. For proteins whose homologs in Arabidopsis contain dual PTSs, CSY2 and LACS7 homologs retain the same PTSs, LACS6 gains a PTS1 (PKL>), ACX3 and ACX6 both lose their PTS1s, while ACD31.2 does not have an apparent rice homolog.

Rice appears to employ a greater diversity of PTSs, with (potentially) 37 assorted PTS1s and 5 PTS2s. Recognition of PTS1 in plants seems fairly plastic and tolerant of non-canonical substitutions (Lingner et al., 2011). These new PTS1s in rice still need to be validated in planta as genuine PTSs. An outright observation is the frequent substitution to Methionine (M) in both PTSs, i.e., at position 3 in the PTS1 in lieu of L or position 2 in PTS2 in lieu of L/I. Examples include ATF, OPR3, AAE7, AAE12, SO, 6PGDH, MFP2, and IBR3 for PTS1 and MDH and TLP for PTS2. Another interesting observation is the change of PTSs in the orthologs. For example, for the two proteins predicted to work sequentially in the pseudouridine catabolism pathway, i.e., Indigoidine synthase A (IndA) and PfkB-type carbohydrate kinase family protein (pxPfkB; Eubel et al., 2008; Reumann, 2011), IndA harbors a PTS2 (RIX5HL), and pxPfkb has a PTS1 (SML>) in Arabidopsis, whereas in rice IndA contains a PTS1 (SAL>) and pxPfkb has a PTS2 (RMX5HL). In a similar case, the Arabidopsis HIT2 and HIT3 proteins both have PTS2 (RLX5HL and RVX5HF respectively) and HIT1 has a PTS1 (SKV>), whereas in rice all three putative peroxisomal HIT proteins have PTS2s (RLX5HL). A third example is the acquisition of a minor PTS2 (RQX4HL) in one of the putative homologs of epoxide hydrolase (EH) in rice.

Expansion and contraction of peroxisomal protein families in rice

Rice is considered to be an ancient polyploid, as evidenced by remnants of duplicated blocks in its genome (Paterson et al., 2004). Its genome is predicted to have 1.5 times as many protein coding genes as those in Arabidopsis (Sasaki et al., 2008). Thus, many Arabidopsis peroxisome proteins or protein families have expanded in number in the rice genome, augmenting the number of rice peroxisome proteins.

Among the rice peroxisome proteins, PEX11a, MDAR4, polyamine oxidase (PAO), a protein of unknown function (UP3), AAE1, AAE7, and PM16 seem to have undergone tandem duplications. Duplication of genes is a recurrent evolutionary strategy that drives genetic diversity, and divergent expression of duplicated genes has shaped functional evolution of proteins and is crucial for their retention in the genome (Gu, 2003; Pal et al., 2006; Innan and Kondrashov, 2010). Consistent with this, the duplicated genes in each pair of the tandem duplicates of PAO, UP3, AAE7, and MDAR4 show highly dissimilar expressions (http://evolver.psc.riken.jp/seiken/OS/index.html).

The peroxisomal ATP-binding cassette (ABC) transporter PXA1/CTS/PED3 appears to have two homologs in rice. PXA1/CTS/PED3 has been attributed with a role in transporting β-oxidation substrates into the peroxisome, and mutant analysis in Arabidopsis uncovered a plethora of plant phenotypes associated with its malfunction (Zolman et al., 2001b; Hayashi et al., 2002; Theodoulou et al., 2006; Footitt et al., 2007b). In yeasts and mammals, the PXA1 function is executed by two proteins (each being a half transporter), which heterodimerize to form a functional complex (Hettema and Tabak, 2000; Wanders et al., 2007). However, the rice PXA1 homologs, like Arabidopsis PXA1, encode for full transporters and presumably have full activity. It will be worthwhile to explore as to whether the two rice homologs have different substrate specificities and whether this feature is unique to monocots.

Genes encoding several enzymes associated with the major peroxisomal functions, such as β-oxidation and related functions and detoxification, also increased in numbers in rice. Examples include fatty acid multifunctional protein (MFP), acyl-CoA oxidase (ACX), small thioesterase (sT), esterase/lipase/thioesterase family 1 (ELT1), OPR3 in JA biosynthesis, and napthoate synthase (NS), which has a predicted role in benzoate or phylloquinone metabolism. It will be interesting to investigate whether the acquisition of these additional copies of genes resulted in diversification of the enzymatic activities. β-oxidation activities are the primary source of H2O2 generation in peroxisomes. MDAR and APX are two major enzymes in the glutathione–ascorbate cycle, which serves to eliminate toxic H2O2. In line with the expanded core of β-oxidation enzymes, which are capable of generating H2O2, the antioxidative enzyme complement, including MDAR1, APX3, and GSTT, has also undergone concomitant expansion. EHs are involved in removal of toxic metabolites and enzymatic byproducts, thus fulfilling an important role in peroxisomal detoxification. In rice, there seems to have four peroxisome EHs, in contrast to the presence of a single EH in the Arabidopsis peroxisome. A study in Nicotiana suggests that peroxisomal EH may play a role in basal resistance during fungal infection (Wijekoon et al., 2011). It will be worthwhile to analyze if they are involved in pathogen response in rice as well.

Biotin is a vitamin and an important cofactor of enzymes in both decarboxylation and carboxylation reactions; their biosynthetic enzymes have been shown to be mostly mitochondrial (Smith et al., 2007; Asensi-Fabado and Munne-Bosch, 2010). Biotin F (7-keto-8-aminopelargonic acid synthase), an enzyme implicated in the first step of biotin biosynthesis, has been a recent and surprising addition to peroxisome localized proteins in Arabidopsis (Tanabe et al., 2011). Biotin F has two rice homologs, both of which contain the canonical PTS1, SKL. Production of vitamins is an economically important agricultural trait that is often exploited to enhance nutritional value of food crops (Potrykus, 2001; Beyer et al., 2002; Datta et al., 2003). Investigations into the impact of these proteins on the biotin content of the crops would define new functions of peroxisomes and be vital in understanding the contributions of peroxisomes in this process.

Betaine aldehyde dehydrogenases (BADH) metabolize 4-aminobutyraldehyde/Δ1-pyrroline and probably function in polyamine catabolism in peroxisomes. Rice has two copies of this gene, and the genetic basis of fragrance in rice was linked to the BADH2 locus. Interestingly, the non-functional BADH2 allele causes fragrance production, because the accumulation of the substrate, 4-aminobutyraldehyde/Δ1-pyrroline, in this allele enhances the synthesis of 2-acetyl-1-pyrroline, a major volatile responsible for aroma in rice (Bradbury et al., 2008; Chen et al., 2008). BADH1, on the other hand, was reported to oxidize acetaldehyde and might be important to relieve oxidative stress related to the submergence and re-aeration of rice plants (Mitsuya et al., 2009).

Two peroxisome membrane proteins, PEX22 and FIS1, which serve as scaffolds to recruit downstream proteins (PEX4 and DRP3, respectively) in peroxisome biogenesis (Zolman et al., 2005; Scott et al., 2006; Lingard et al., 2008; Zhang and Hu, 2008, 2009), both seem to have an additional homolog in rice. However, subcellular targeting analysis needs to be done to verify this observation, as targeting signals for peroxisome membrane proteins are hard to define.

Conversely, some Arabidopsis multigene family proteins only have a single equivalent gene in rice. PEX19 and PEX3 are involved in peroxisome membrane protein import and both have two isoforms in Arabidopsis (Kaur et al., 2009); yet only one copy each is found in rice. The two peroxisomal adenosine nucleotide transporters PNC1 and PNC2 were suggested to have arisen from genomic chromosomal rearrangements (Palmieri et al., 2011), therefore the occurrence of a single-copy PNC in rice is not unreasonable. Lastly, citrate synthase (CSY), glutamate:glyoxylate aminotransferase (GGT), 3-ketoacyl-CoA thiolase (KAT), and acetyltransferase (ATF) have multiple isoforms in Arabidopsis but seem to be encoded by a single gene in rice. Mutants for these single-copy genes may be promising candidates to bypass gene redundancy problems encountered in Arabidopsis to unveil the function of their protein products in plants.

Future Perspectives

Proteomics provide a wealth of information regarding organelle protein constituents, yet there are limitations to this approach. Many membrane proteins along with low-abundance proteins and proteins peripherally associated with peroxisomes tend to escape detection. In fact, none of the plant mass spectrometry-based proteome studies were successful in identifying most known peroxisomal membrane proteins, including those involved in various aspects of peroxisome biogenesis. However, many of their counterparts were successfully discovered in previous peroxisomal proteomics experiments in yeasts and mammals (Schafer et al., 2001; Kikuchi et al., 2004; Wiese et al., 2007). As such, there is still a lot of space for technology improvement to maximize the coverage of plant peroxisomal proteins, especially those associated with the membrane. In addition, peroxisomes and other organelles are not static entities within the cell. Some proteins may be accumulated or redistributed in the peroxisome in response to varied stimuli in a tissue-, environment-, or development-specific manner, and as a result, underrepresented in the analyzed proteome. Therefore, sampling of the peroxisome proteome at various developmental stages and under different environmental conditions may uncover proteins with provisional presence in these organelles.

Since experimental proteomics has its limitations in detecting low-abundance and transient peroxisomal proteins, this approach needs to be complemented by in silico protein prediction studies in order to completely decode the peroxisome proteome. Bioinformatics approaches have been very powerful in predicting peroxisomal proteins based on the presence of PTSs on them, allowing researchers to verify the predictions by subcellular localization studies (Kamada et al., 2003; Reumann et al., 2004; Lingner et al., 2011; Reumann, 2011). Furthermore, to assign functions to each newly identified peroxisomal protein, reverse genetics analysis and biochemical characterizations need to be conducted. In the Arabidopsis peroxisome 2010 project, we have analyzed more than 90 sequence-indexed T-DNA insertion mutants of over 50 novel peroxisomal genes through a series of physiological, biochemical, and cell biological assays to assess the roles of the corresponding proteins in peroxisomes. This systematic approach revealed the involvement of more peroxisomal proteins in embryogenesis, peroxisome protein import, and defense response (Cassin and Hu, unpublished). Other physiological assays coupled with metabolic profiling will need to be employed to elucidate the novel roles of plant peroxisomes, as our current tool box for analyzing peroxisome-related functions is only limited to the well known peroxisomal functions such as β-oxidation and photorespiration.

Knowledge gained through organelle proteomics can help us build increasingly complex models regarding the functions and regulation of these compartments, and map metabolic fluxes in relation to other organelles. Cross comparison of global environmental stress proteomics data using known peroxisome proteins identified proteins with changed abundance under salt (6PGL, NDPK1), cadmium (MDAR1, ATMS1, CAT3), and cold (CAT3) stresses (Taylor et al., 2009). Post-translational modification (PTM) of plant peroxisomal proteins is a field that has been unexplored, except for the phosphorylation of PMP38/PXN reported by Eubel et al. (2008). The list of Arabidopsis peroxisomal proteins can be used to query preexisting databases that compile data of global PTM events. Information extracted from the databases can then be used to formulate hypothesis, followed by experimental testing.

A systems biology approach, which combines functional genomics, proteomics, and computational tools, may help to establish a global network of peroxisome function in plants. Studies in yeasts at the systems level defined the network dynamics that control the response of yeast cells to fatty acids at multiple levels, including signaling, transcription, chromatin dynamics, and peroxisome biogenesis (Saleem et al., 2010a,b). Three transcription factors in yeast have been demonstrated to be directly responsible for transcriptional regulation of peroxisome biogenesis genes as well as metabolic enzymes therein during response to oleic acids (Gurvitz and Rottensteiner, 2006). Likewise, the mammalian nuclear receptor, PPARα, controls the activation of peroxisomal genes in response to metabolic stimuli (Desvergne and Wahli, 1999). Plant peroxisome proteins far outnumber those found in yeasts or mammals, i.e., over 160 in Arabidopsis and (putatively) more than 190 in rice, vs. 61 in Saccharomyces cerevisiae and 85 in humans (Schrader and Fahimi, 2008). Yet how transcriptional regulation of peroxisomal genes is accomplished in plants is largely unknown. Direct binding of two transcriptional factors to promoters of peroxisome genes in plants has been reported. The first is the bZIP transcription factor, HY5 homolog (HYH), which binds to the promoter of the peroxisome proliferator gene PEX11b and controls its light specific activation in a phytochrome A-dependent manner, resulting in light-induced peroxisome proliferation (Desai and Hu, 2008). In addition, using chromatin immunoprecipitation-on-chip analysis, PEX11b and a glyoxalase I homolog (GLX1) were found to be direct targets of the bHLH transcription factor POPEYE (PYE) under iron deplete conditions (Long et al., 2010). We can now use the inventory of Arabidopsis peroxisome proteins in combination with available global expression datasets to build transcriptional regulatory networks based on co-expression analysis. Mining such data should also enable us to connect common expression patterns to possible regulatory factors. This knowledge would be instrumental to broadening our understanding of what factors govern peroxisome protein composition in plants and how they relate to global environmental or developmental changes.

Given the agronomical importance of plant peroxisomes, extending the large scale proteome study of these organelles into crop plants will be highly beneficial to improving the quality, yield, and stress response of crop species. In addition to the in silico proteome analysis of rice peroxisomes performed in this study, experimental proteomics should be employed to understand the dynamic rice peroxisomal proteome in different tissues and developmental stages, and under various environmental cues. Comparison of the peroxisome proteomes in rice and Arabidopsis will shed light onto the evolution of peroxisomal functions in diverse plant lineages. Grass (Poaceae) genomes display extensive synteny (Devos and Gale, 1997), thus information gained from rice could be applied to other cereal crops such as maize and wheat, which are also prominent food crops worldwide.

Statements

Acknowledgments

We apologize to those colleagues whose works are not covered in this review. Work in the Hu lab was supported by grants from the National Science Foundation (MCB 0618335) and the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (DE-FG02-91ER20021) to Jianping Hu.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Summary

Keywords

peroxisome, proteomics, Arabidopsis, rice

Citation

Kaur N and Hu J (2011) Defining the Plant Peroxisomal Proteome: From Arabidopsis to Rice. Front. Plant Sci. 2:103. doi: 10.3389/fpls.2011.00103

Received

14 November 2011

Accepted

08 December 2011

Published

27 December 2011

Volume

2 - 2011

Edited by

Andreas P. M. Weber, University of Duesseldorf, Germany

Reviewed by

Roland Krause, Max Planck Institute of Molecular Cell Biology and Genetics, Germany; Robert Mullen, University of Guelph, Canada

Copyright

© 2011 Kaur and Hu.

This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

*Correspondence: Jianping Hu, MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USA. e-mail:

This article was submitted to Frontiers in Plant Physiology, a specialty of Frontiers in Plant Science.

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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