Navneet Kaur1 Jianping Hu1,2*- 1 MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, USA
- 2 Plant Biology Department, Michigan State University, East Lansing, MI, USA
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. Peroxisomal proteins in Arabidopsis and rice.
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.
Conflict of Interest Statement
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.
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.
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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; Paper pending published: 30 November 2011;
Accepted: 08 December 2011; Published online: 27 December 2011.
Edited by:
Andreas P. M. Weber, University of Duesseldorf, GermanyReviewed by:
Roland Krause, Max Planck Institute of Molecular Cell Biology and Genetics, GermanyRobert 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: huji@msu.edu