Báo cáo khoa học: Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts ppt

9 520 0
  • Loading ...
    Loading ...
    Loading ...

Tài liệu liên quan

Thông tin tài liệu

Ngày đăng: 07/03/2014, 03:20

MINIREVIEWProtein transport in organelles: Dual targeting of proteinsto mitochondria and chloroplastsChris Carrie, Estelle Giraud and James WhelanAustralian Research Council Centre of Excellence in Plant Energy Biology, M316, University of Western Australia, Crawley, AustraliaThe traditional dogma of both cell and molecularbiology, one gene fi one protein fi one location, haswell passed its use-by date in postgenomic biology. Itis clear from the sequencing of several genomes thatthe complexity of the proteome exceeds that of thegenome in terms of the number of functional units(i.e. there are more proteins than genes). This proteincomplexity is achieved by a number of means, ofwhich alternative splicing of genes and protein modifi-cation are the best characterized to date [1–3].Another mechanism to increase the complexity ofproteomes is the editing of transcripts (both in nuclearand organelle genomes) [4,5]. Dual targeting ofproteins does not increase the number of proteins in acell, but can expand the function(s) of a protein, inthat a protein located in more than one location, willpresumably function with a distinct biochemicalprocess in each location. Although the number ofdual-targeted proteins is small in terms of the totalorganelle proteomes, it is unclear whether this justrepresents the tip of the iceberg. Irrespective of thetotal number of dual-targeted proteins present inmitochondria and chloroplasts (note that, for thepurpose of this minireview, dual targeted refers toproteins targeted to mitochondria and chloroplasts),the phenomenon of dual targeting raises interestingquestions for inter-organelle communication. A greaterunderstanding of the process of dual targeting mayprovide useful insights into the targeting of location-specific proteins to mitochondria or chloroplasts.Keywordschloroplast; dual targeting; inter-organellecommunication; mature protein;mitochondria; processing; receptor;regulation; sorting; targeting signalCorrespondenceJ. Whelan, Australian Research CouncilCentre of Excellence in Plant EnergyBiology, University of Western Australia, 35Stirling Highway, Crawley 6009, AustraliaFax: +61 8 6488 4401Tel: +61 8 6488 1749E-mail: seamus@cyllene.uwa.edu.auWebsite: http://www.plantenergy.uwa.edu.au(Received 13 August 2008, revised 19November 2008, accepted 27 November2008)doi:10.1111/j.1742-4658.2009.06876.xAs many as fifty proteins have now been experimentally demonstrated tobe targeted to both mitochondria and plastids, a phenomenon referred toas dual targeting. Although the first reported case of dual targeting of aprotein was reported in 1995, there is still little understanding of the mech-anism of dual targeting and any similarities or differences with respect tothe targeting of location-specific proteins. This minireview summarizes dualtargeting in terms of signals, passenger proteins, receptors, regulation, whyproteins may need to be dual targeted and the future challenges thatremain in this area.AbbreviationsGFP, green fluorescent protein; GR, glutathione reductase; MPP, mitochondrial processing peptidase; NDC1, type II alternative NAD(P)Hdehydrogenase; RPS16, 16 kDa proteins of the small ribosomal subunit of mitochondria or chloroplasts; SPP, stromal processing peptidase;Toc, translocase at the outer envelope membrane of chloroplasts; Tom, translocase at the outer mitochondrial membrane.FEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS 1187Dual targeting was first reported for Pisum sativum(pea) glutathione reductase (GR) in 1995 [6], and, todate, as many as 47 different proteins have beenreported to be dual-targeted from seven different plantspecies (see Table S1). It is notable that there are alsoreports of dual-targeted proteins to chloroplasts andthe nucleus [7], to chloroplasts and the peroxisome[8,9], and, in Chlamydomonas reinhardtii, to chloro-plasts and the endoplasmic reticulum [10]. However,by far the greatest number of dual-targeted proteinsknown are targeted to chloroplasts and mitochondria.With the advent of complete genome sequence infor-mation and the combined information emerging fromorganelle proteome studies [11], green fluorescent pro-tein (GFP) tagging studies [12], and bioinformatic pre-diction of subcellular localization [13], the number ofdual-targeted proteins has increased in the last 5 yearssuch that they can be no longer be treated as an exce-ption compared to location-specific proteins. Dualtargeting can be achieved via two basic mechanisms[14,15]: alternative transcription initiation or splicingand ambiguous targeting signals (Fig. 1). Alternativetranscriptional initiation or splicing represents tran-scriptional or post-transcriptional events that producelocation-specific targeted proteins [16]. This mechanismof dual targeting will not be discussed further here[17,18]. Instead, we provide an overview the signals,proteins, receptors, sorting of dual-targeted proteinsand why dual targeting may occur. Finally, an outlineof the future challenges in this field is provided, andthe insights that may be gained from a greater under-standing of the mechanism of dual targeting for thetargeting of location-specific proteins is discussed.Targeting signals and mature proteinsTargeting signalsAnalysis of dual targeting signals indicates that theyare rather similar to plastidic and mitochondrial tar-geting signals, in that they are enriched in positivelycharged residues, and significantly deficient in acidicresidues and glycine [19]. However, there are no fea-tures detectable to date that could distinguish them asa group from location-specific targeted proteins. Theyappear to fall between mitochondrial and chloroplastictargeting signals in terms of arginine and serine con-tent (i.e. not as high as in mitochondrial targetingsignals) and may be slightly enriched in hydrophobicresidues. In yeast, proteins targeted to mitochondriaFig. 1. Overview of dual targeting of proteins to mitochondria and chloroplasts in plant cells. A gene encoding a dual-targeted protein may:(1) produce two different mRNA molecules via alternative start site for transcription initiation or alternative splicing (blue arrows), where thetwo mRNA molecules encode location-specific proteins [16], or (2) produce a single mRNA molecule that gives rise to a protein that is dualtargeted via an ambiguous targeting signal (black arrows).Dual targeting of proteins C. Carrie et al.1188 FEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBSand one other location have been reported to have alower mitochondrial targeting score using mitoprotcompared to exclusive mitochondrial proteins [20].This is not observed with proteins dual targeted tomitochondria and plastids, where the mitoprot scorefor many is quite high.Experimental analyses of dual targeting signals havealso failed to define clear facets that define dual target-ing ability. The best studied dual targeting signal isfrom pea GR [21–23]. Deletion and site-directed muta-genesis studies reveal that although some regions maybe more important for targeting to one organelle, thedual targeting signal is overlapping. This is consistentwith studies that have used tandem arrangements ofmitochondrial and chloroplastidic targeting signals andshown that the passenger protein was targeted to thelocation defined by the most N-terminal sequence [24].In the case of GR, it was concluded that positive resi-dues throughout the signal and hydrophobic residuesat the N-terminus were important for mitochondrialimport, whereas hydrophobic residues alone had thegreatest affect on chloroplast import [21]. The role ofarginine residues playing a more important role formitochondrial import was also observed for threeaminoacyl-tRNA synthetases [19].It has been reported that Arabidopsis thaliana DNApolymerase c2 is dual targeted via the use of a non-AUG start codon (a CUG codon) in translation,resulting in an additional seven amino acids at theN-terminus of the protein [25]. Thus, translation fromthe standard AUG produces a protein that is targetedto chloroplasts alone but, by alternative translation siteinitiation, the addition of seven amino acids to theN-terminus results in targeting to mitochondria andchloroplasts. This would represent an elegant mecha-nism of dual targeting. However, experimentally, it isdifficult to demonstrate that alternative translation istaking place in vivo. Analysis of the targeting ability ofDNA polymerase c2 in another study revealed that itwas dual targeted, but from a protein produced fromthe standard AUG [26], and thus via an ambiguoustargeting signal rather than alternative translation initi-ation site. Analysis of targeting of DNA polymerasec2 in different tissues or cell types indicated that theamount of GFP fluorescence from chloroplasts wasgreater than GFP fluorescence from mitochondriausing the AUG start construct [26]. However, theamount of GFP fluorescence from mitochondria usingthe CUG start construct was greater in terms of itbeing equal in intensity to GFP fluorescence fromplastids. Thus, the dual targeting ability of proteinstarting at the standard AUG codon may be over-looked due to differential targeting to both organelles.In tobacco, both DNA polymerases are reported tobe dual targeted from a standard AUG codon [27], eventhough they also contain the same upstream ‘inframe’CUG. Thus, the addition of the seven amino acids mayalter partitioning to allow dual targeting to be observed.As described below in detail, the passenger protein alsohas large affect on dual targeting, and different con-structs may favour targeting to one organelle comparedto another, especially if tested in a single tissue.In terms of processing, pea GR is the best studied todate [23]. Based on mobility in gels, it was concludedthat the processing site was the same in both organelles.It has been demonstrated that purified mitochondrialprocessing peptidease (MPP) and stromal processingpeptidase (SPP) are responsible for processing GR [23].The processing requirements for MPP appear to bemore stringent in that alterations near the processingsite have a greater inhibitory affect of MPP compared toSPP. In the case of aminoacyl tRNA synthetases, Gluaminoacyl-tRNA synthetase was processed at the samesite in both mitochondria and chloroplasts but for Metand Phe aminoacyl-tRNA synthetases they have differ-ent processing sites in mitochondria and chloroplasts[19]. However, because the latter study was carried outwith GFP as a passenger protein, and processing wasnot assessed by purified peptidases, processing by chlo-roplasts may be due to a variety of processing activitiesthat have been detected in chloroplasts, or due to crypticprocessing sites that can be generated when targetingsignals are fused to reporters [28,29].Dual targeting signals do not exclusively have tocomprise cleavable N-terminal signals. A protein pro-duced from a gene encoding the small subunit of ribo-somes in mitochondria and plastids (RPS16) wasfound to be dual targeted in Medicago truncatula andPopulus alba without a cleavable N-terminal targetingsignal [30].Mature proteinsAnalysis of the role of the mature protein in dual target-ing in several studies reveals that it plays a crucial rolein this process, a facet that is often overlooked. Pea GRcan only support the targeting of GFP to plastids [31],although it can support the import of phosphinothricinacetyl transferase into both mitochondria and chloro-plasts [6]. Assessing the targeting ability of threesequences that have dual targeting ability revealed that,with the pea GR targeting signal, a native mitochondrialpassenger protein was only targeted to mitochondriaand a native chloroplast passenger protein was only tar-geted to chloroplasts [31]. By contrast, the dual target-ing signal of Arabidopsis asparaginyl-tRNA synthetaseC. Carrie et al. Dual targeting of proteinsFEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS 1189supported targeting to both locations with the same pas-sengers [31]. The properties of targeting of Arabidopsishistidyl-tRNA synthetase was intermediate betweenthese two extremes, whereas the mitochondrial passen-ger was only targeted to mitochondria and the chloro-plast passenger protein was dual-targeted [31]. Furtherevidence that the mature protein plays a role in dualtargeting properties is seen with an alternativeNAD(P)H dehydrogenase (NDC1). GFP is only tar-geted to mitochondria when the targeting signal of 83amino acids is used [32], but GFP is targeted to bothmitochondria and chloroplasts when the full protein isfused to GFP [33]. It has also been demonstrated that,for tRNA nucleotidyltransferase, the mature proteinplays a major role in determining partitioning betweenmitochondria and chloroplasts [34]. Thus, compared tolocation-specific proteins, where many studies show thatthe targeting signal is sufficient to support import [35],albeit the mature protein may affect the efficiency, theeffect of the mature protein on targeting appears to bemore pronounced in the case of dual-targeted proteins.This likely reflects the fact that dual-targeted proteinshave evolved from proteins that were targeted to aspecific location [30]. Thus, the acquisition of the dualtargeting signal would be a constraint compared to tar-geting of location-specific proteins to avoid loss of tar-geting to the ‘parental’ organelle (i.e. the ambiguousdual targeting signal is a compromise and dual targetingability is dependent on the passenger protein). Notethat, with dual targeting signals, different passengerproteins affect dual targeting ability, but do not appearto block targeting to both organelles simultaneously.Usually, targeting to one organelle is maintained. Thisis evident with GR and NDC1, when the targeting sig-nal alone is fused to GFP, dual targeting ability is lost,although targeting to either plastids only (GR) or mito-chondria only (NDC1) is maintained [31,32].Organelle receptorsUnfortunately, little is known about the organellereceptors that recognize dual-targeted proteins. How-ever, because the dual-targeted proteins identified todate would be required in various types of plastids, itsuggests that they may employ different receptors com-pared to the translocase at the outer envelope mem-brane of chloroplasts (Toc)64 and Toc159 system usedby proteins involved in photosynthesis [36]. TheToc159 family in Arabidopsis consists of four proteins:Toc159, Toc132, Toc120 and Toc 90 [37]. It is possiblethat one of these members is specialized in the importof dual-targeted proteins. With references to the vari-ous import pathways that exist for protein import intomitochondria and plastids, no experimental studieshave been carried out to determine the import and ⁄ orsorting pathways used by dual-targeted proteins.In the case of mitochondrial receptors for dual-targeted proteins, it has been shown that a doubleknockout of the translocase at the outer mitochondrialmembrane (Tom), tom20,inArabidopsis, which stillcontained one functional Tom20 isoform, had higherrates of import for GR, whereas some mitochondrialprecursor proteins were decreased [38]. In the tripletom20 knockout mutant, which has severely reducedrates of protein import for several mitochondrial pre-cursor proteins, the import of GR was unaffected com-pared to the wild-type [38]. This indicates that GR canutilize a different receptor compared to several mito-chondrial proteins imported via the general and carrierimport pathways. The same study also assessed therole of other outer membrane proteins on GR import.Plant mitochondria contain an outer membrane pro-tein of 64 kDa (OM64) that displays more than 70%amino acid sequence identity with the chloroplastouter envelope receptor Toc64 [23]. OM64 did notappear to play any specific role in the import of GRcompared to mitochondrial precursor proteins. Oneprotein that was identified to play a role in the importof GR into mitochondria was metaxin [38]. This mito-chondrial outer membrane protein was first identifiedin mammals, and was subsequently shown to be partof the sorting and assembly machinery complex inyeast (SAM), called Sam35 (also called Tom34 orTob35) [39]. Metaxin knockouts have severe affects onthe protein import of all proteins tested in Arabidopsis,presumably acting indirectly because it plays a role inimport and ⁄ or assembly of b-barrel proteins into theouter mitochondrial membrane [38,39]. However, usingan alternative method to assess a role in import, theaddition of in vitro synthesized metaxin to import reac-tion mixtures can compete for the import of GR intomitochondria, and some but not all other mitochon-drial proteins tested, suggesting that it plays some rolein import of GR on the cytosolic surface of the outermembrane. Notably, metaxin was also up-regulated inabundance in the double and triple tom20 knockoutmutants, where import of mitochondrial precursorproteins was affected but GR was not [38].Sorting and regulationThere is no direct experimental evidence demonstratingthat dual-targeted proteins are actively sorted or thatsorting between organelles is regulated. However, thereare several observations that suggest sorting is notsimply a passive process. Most dual-targeted proteinsDual targeting of proteins C. Carrie et al.1190 FEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBScontain the sequence motif for phosphorylation by acytosolic protein kinase that acts as a guidance com-plex to the Toc complex of chloroplasts (see Table S1).Any regulation of the activity of this complex couldchange the partitioning of dual-targeted proteinsbetween mitochondria and chloroplasts [40,41]. Muta-tion of this site in GR [21], and indeed in chloroplast-specific targeted proteins [42], does not appear to affectthe amount or rate of import. However, in vitro importassays often employ animal-based translation lysates,or, even in plant-based systems, translation mixturesare prepared in advance and frozen. In such in vitroimport systems with a single purified organelle, thissystem of regulation may be by-passed or go unde-tected. Where else does the protein have to go?Dual targeting is most commonly detected usingGFP tagged proteins. Because the emphasis of manystudies has been to determine that the protein understudy is dual targeted, the reported data tend to showcells with both mitochondria and chloroplasts that areclearly visible. In a more comprehensive study, weanalysed the fluorescence intensity of several dual-tar-geted proteins and found that it differed considerably[26]. Thus, in Arabidopsis suspension cells, for somedual-targeted proteins, targeting to chloroplasts wasmost dominant, but the same constructs in onion epi-dermal cells gave approximately equal GFP labellingof both mitochondria and chloroplasts. Furthermore,one study reported that, for the dual-targeted proteinsigma factor 2B, targeting to one organelle is onlyobserved in any one cell [43]. Another study reportedthat the GFP fluorescence intensity differs betweenexperiments with dual-targeted proteins [19]. Suchreports are likely to increase in the future.One interesting opportunity for regulation of parti-tioning dual-targeted proteins is the possibility thatmRNA for dual-targeted proteins is targeted to theorganelle surface [23]. Regulation of targeting ofmRNA could result in changes in partitioning. As yet,there is no evidence for mRNA targeting to mitochon-dria or plastids, even for mRNA encoding location-specific proteins.Why dual target proteins?Mitochondria and chloroplasts share many commonenzymatic steps that are catalysed by location-specificproteins [44]. Thus, it is unclear why some and, at thisstage, a relatively small number of activities are carriedout by dual-targeted proteins. Furthermore, in manycases where a dual-targeted protein exists, location-specific isoforms also exist. Thus, dual targeting doesnot appear to be a strategy of limiting gene number inthe nuclear genome. As outlined previously, dual tar-geting of proteins appears to have arose before themonocot ⁄ dicot split [30], and is present in several plantspecies (see Table S1). The RPS16 protein gives aninteresting insight into the evolutionarily history ofdual targeting. In both Arabidopsis and Oryza sativa(rice), the chloroplast genome contains a functionalgene encoding this protein; however, the nuclearlocated gene that encodes the mitochondrial proteinhas dual targeting ability. Thus, acquisition of dualtargeting ability may be a pre-requisite or at least facil-itate the loss of organelle genes. Therefore, dual target-ing of proteins may have been more widespread,occurring early in the evolutionarily history of plants.Characterization of organelle RNA polymerases inPhyscomitrella patens concluded that there is no dual-targeted isoform [45], in contrast to previous studies[46]. Thus, it is unclear how widespread and conserveddual targeting is in plant evolution.An examination of proteins that are dual targetedreveals that they differ substantially in functional cate-gorization compared to a genome wide classification(Fig. 2; see also Table S1). Dual-targeted proteinsappear to be particularly enriched in the categories ofcell cycle and DNA synthesis, and protein synthesis(Fig. 2; see also Table S1). This may simply be due tothe fact that a limited number of dual-targeted pro-teins are known because dual-targeted proteins alsohave significantly less proteins of uncharacterized fun-ction compared to the whole genome (Fig. 2). Exami-nation of the expression patterns of dual-targetedproteins across several tissue types and developmentalstages reveals that they are relatively static, displayingsimilar levels of expression across green and not greentissues and across developmental stages ranging fromembryonic to senescence (see Fig. S1). This suggeststhat they encode basic but essential functions requiredin mitochondria and plastids. An examination of thelist of dual-targeted proteins also reveals that severalsteps in a biochemical process may be dual targeted(e.g. the process of organelle gene expression, proteinsinvolved in DNA replication, transcription and trans-lation are dual targeted, and for the ascorbate glutathi-one cycle, several enzymes are dual targeted) [47]. Forboth these processes, location-specific isoforms alsoexist for many steps.The reason for dual targeting a protein may com-prise a means of inter-organelle communication. Send-ing the same proteins to both organelles at the sametime ensures that they are both at least capable ofcarrying out these functions in a co-ordinated manner.Organelle genome replication and number mayhave also have roles beyond their immediate codingC. Carrie et al. Dual targeting of proteinsFEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS 1191capacity. In human cancers, the depletion of mitochon-drial DNA is associated with altered methylation pat-terns in the nucleus, and restoration of mitochondrialDNA reverses these changes [48]. Given that epigeneticregulation can have widespread affects beyond specificorganelle functions [49], in plant cells that contain twoorganelles with their own genomes, it may be necessaryat times to co-ordinate the replication and ⁄ or expres-sion of both organelle genomes.At the level of the individual functions encoded bydual-targeted proteins, it is likely that the activitiesencoded are required in both organelles at the sametime. Thus, dual-targeted glutamine synthetase plays arole in assimilating ammonia that is produced in themitochondria during photorespiration, which com-prises the best known biochemical process that linksmitochondrial and chloroplast function [50]. The factthat GR and the associated enzymes in the ascorbateglutathione cycle are dual targeted is not surprisinggiven that mitochondria are the site of ascorbate syn-thesis, and that this cycle plays an important role inboth organelles in maintaining cellular redox balance[51]. Thus, taking the current list of dual-targeted pro-teins as a whole or at an individual level, the activitiesprovide a direct link between organelle functions,which is not achieved by other communication path-ways, such as retrograde regulation [52,53].Future challengesThe understanding of the mechanism of dual targetingis at a very early stage compared to that of location-specific proteins. Defining the plastidic and mitochon-drial receptor(s) for dual-targeted proteins wouldrepresent a major landmark, in that a comparison withthe binding of location-specific proteins to theirFig. 2. Functional categorization of proteins dual targeted to mitochondria and chloroplasts in Arabidopsis. The number of proteins in eachclassification is expressed as a percentage of the total number of proteins in each set and compared to the functional classification of all pro-teins in Arabidopsis. An asterisk (*) indicates a significant difference at a 99% confidence interval compared to the whole genome using achi-squared test.Dual targeting of proteins C. Carrie et al.1192 FEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBScognate receptors may reveal what is required for dualtargeting, and also what is required to avoid mis-sort-ing of proteins between mitochondria and chloroplasts.The structures of binding of targeting peptides tomammalian and plant Tom20s not only revealed themolecular details of binding [54,55], but also promptedthe hypothesis of an elegant example of convergentevolution [54,56] because plant and mammalianTom20s are not orthologous. One of the most compel-ling questions concerning dual targeting is how theproteins are partitioned between both organelles?Thus, a better understanding of the role of any cyto-solic factors involved, and whether they play any regu-latory role, would explain how each organelle obtainsthe appropriate amount of protein. An understandingof why dual targeting occurs will require the evolution-arily history of dual targeting to be determined inmore detail in terms of when it arose and whether it isconserved. A complete understanding of dual targetingalso requires an understanding of why it occurs. Thisis probably best achieved by converting dual-targetedproteins to location-specific isoforms and assessingorganelle function. For dual-targeted proteins thathave location-specific isoforms, it is not clear whetherthe dual-targeted isoform has taken on new functions(neofunctionalization) or whether expression is special-ized (subfunctionalization). Promoter swapping studiesbetween dual and location-specific isoforms may alsobe informative for assessing the function of dual-targeted proteins.AcknowledgementWork on dual targeting by J.W. is supported by anAustralian Research Council grant DP0664692.References1 Kazan K (2003) Alternative splicing and proteomediversity in plants: the tip of the iceberg has justemerged. Trends Plant Sci 8, 468–471.2 Siuti N & Kelleher NL (2007) Decoding protein modifi-cations using top-down mass spectrometry. Nat Meth-ods 4, 817–821.3 Witze ES, Old WM, Resing KA & Ahn NG (2007)Mapping protein post-translational modifications withmass spectrometry. Nat Methods 4, 798–806.4 Nishikura K (2006) Editor meets silencer: crosstalkbetween RNA editing and RNA interference. Nat RevMol Cell Biol 7, 919–931.5 Takenaka M, Verbitskiy D, van der Merwe JA, Zehr-mann A & Brennicke A (2008) The process of RNAediting in plant mitochondria. Mitochondrion 8, 35–46.6 Creissen G, Reynolds H, Xue Y & Mullineaux P (1995)Simultaneous targeting of pea glutathione reductase andof a bacterial fusion protein to chloroplasts and mito-chondria in transgenic tobacco. Plant J 8, 167–175.7 Schwacke R, Fischer K, Ketelsen B, Krupinska K &Krause K (2007) Comparative survey of plastid andmitochondrial targeting properties of transcription fac-tors in Arabidopsis and rice. Mol Genet Genomics 277,631–646.8 Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S,Frydman A, Gidoni D & Eyal Y (2008) Peroxisomallocalization of Arabidopsis isopentenyl diphosphateisomerases suggests that part of the plant isoprenoidmevalonic acid pathway is compartmentalized to per-oxisomes. Plant Physiol 148, 1219–1228.9 Reumann S, Babujee L, Ma C, Wienkoop S, SiemsenT, Antonicelli GE, Rasche N, Lu¨der F, Weckwerth W& Jahn O (2007) Proteome analysis of Arabidopsis leafperoxisomes reveals novel targeting peptides, metabolicpathways, and defense mechanisms. Plant Cell 19,3170–3193.10 Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I &Danon A (2005) Dual targeting of the protein disulfideisomerase RB60 to the chloroplast and the endoplasmicreticulum. Proc Natl Acad Sci USA 102, 6225–6230.11 Heazlewood JL, Verboom RE, Tonti-Filippini J, SmallI & Millar AH (2007) SUBA: the Arabidopsis subcellu-lar database. Nucleic Acids Res 35, D213–D218.12 Koroleva OA, Tomlinson ML, Leader D, Shaw P &Doonan JH (2005) High-throughput protein localizationin Arabidopsis using Agrobacterium-mediated transientexpression of GFP-ORF fusions. Plant J 41, 162–174.13 Cho SH, Chung YS, Cho SK, Rim YW & Shin JS(1999) Particle bombardment mediated transformationand GFP expression in the moss Physcomitrella patens.Mol Cells 9, 14–19.14 Karniely S & Pines O (2005) Single translation–dualdestination: mechanisms of dual protein targeting ineukaryotes. EMBO Rep 6, 420–425.15 Peeters N & Small I (2001) Dual targeting to mitochon-dria and chloroplasts. Biochim Biophys Acta 1541, 54–63.16 Dinkins RD, Majee SM, Nayak NR, Martin D, Xu Q,Belcastro MP, Houtz RL, Beach CM & Downie AB(2008) Changing transcriptional initiation sites andalternative 5¢- and 3¢-splice site selection of the firstintron deploys Arabidopsis protein isoaspartyl methyl-transferase2 variants to different subcellular compart-ments. Plant J 55, 1–13.17 Millar AH, Whelan J & Small I (2006) Recent surprisesin protein targeting to mitochondria and plastids. CurrOpin Plant Biol 9, 610–615.18 Silva-Filho MC (2003) One ticket for multiple destina-tions: dual targeting of proteins to distinct subcellularlocations. Curr Opin Plant Biol 6, 589–595.C. Carrie et al. Dual targeting of proteinsFEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS 119319 Pujol C, Marechal-Drouard L & Duchene AM (2007)How can organellar protein N-terminal sequences bedual targeting signals? In silico analysis and mutagenesisapproach. J Mol Biol 369, 356–367.20 Dinur-Mills M, Tal M & Pines O (2008) Dual targetedmitochondrial proteins are characterized by lowerMTS parameters and total net charge. PLoS ONE 3,e2161.21 Chew O, Rudhe C, Glaser E & Whelan J (2003) Char-acterization of the targeting signal of dual-targeted peaglutathione reductase. Plant Mol Biol 53, 341–356.22 Rudhe C, Chew O, Whelan J & Glaser E (2002) Anovel in vitro system for simultaneous import of pre-cursor proteins into mitochondria and chloroplasts.Plant J 30, 213–220.23 Rudhe C, Clifton R, Chew O, Zemam K, Richter S,Lamppa G, Whelan J & Glaser E (2004) Processing ofthe dual targeted precursor protein of glutathionereductase in mitochondria and chloroplasts. J Mol Biol343, 639–647.24 de Castro Silva Filho M, Chaumont F, Leterme S &Boutry M (1996) Mitochondrial and chloroplast target-ing sequences in tandem modify protein import specific-ity in plant organelles. Plant Mol Biol 30, 769–780.25 Christensen AC, Lyznik A, Mohammed S, ElowskyCG, Elo A, Yule R & Mackenzie SA (2005) Dual-domain, dual-targeting organellar protein presequencesin Arabidopsis can use non-AUG start codons. PlantCell 17, 2805–2816.26 Carrie C, Kuhn K, Murch M, Duncan O, Small I,O’Toole N & Whelan J (2008) Approaches to definingdual targeted protein in Arabidopsis. Plant J, doi:10.1111/j.1365-313X.2008.03745.x.27 Ono Y, Sakai A, Takechi K, Takio S, Takusagawa M& Takano H (2007) NtPolI-like1 and NtPolI-like2, bac-terial DNA polymerase I homologs isolated from BY-2cultured tobacco cells, encode DNA polymerasesengaged in DNA replication in both plastids and mito-chondria. Plant Cell Physiol 48, 1679–1692.28 Duby G, Oufattole M & Boutry M (2001) Hydrophobicresidues within the predicted N-terminal amphiphilicalpha-helix of a plant mitochondrial targeting prese-quence play a major role in in vivo import. Plant J 27,539–549.29 Musgrove BT & Malden NJ (1989) Mediastinitis andpericarditis caused by dental infection. Br J Oral Max-illofac Surg 27, 423–428.30 Ueda M, Nishikawa T, Fujimoto M, Takanashi H,Arimura SI, Tsutsumi N & Kadowaki KI (2008)Substitution of the gene for chloroplast RPS16 wasassisted by generation of a dual targeting signal.Mol Biol Evol 25, 1566–1575.31 Chew O & Whelan J (2003) Dual targeting ability oftargeting signals is dependent on the nature of themature protein. Funct Plant Biol 30, 805–812.32 Michalecka AM, Svensson AS, Johansson FI, AgiusSC, Johanson U, Brennicke A, Binder S & RasmussonAG (2003) Arabidopsis genes encoding mitochondrialtype II NAD(P)H dehydrogenases have different evolu-tionary origin and show distinct responses to light.Plant Physiol 133, 642–652.33 Carrie C, Murcha MW, Kuehn K, Duncan O, BarthetM, Smith PM, Eubel H, Meyer E, Day DA, Millar AHet al. (2008) Type II NAD(P)H dehydrogenases aretargeted to mitochondria and chloroplasts orperoxisomes in Arabidopsis thaliana. FEBS Lett 582,3073–3079.34 von Braun SS, Sabetti A, Hanic-Joyce PJ, Gu J, SchleiffE & Joyce PB (2007) Dual targeting of the tRNAnucleotidyltransferase in plants: not just the signal.J Exp Bot 58, 4083–4093.35 Glaser E, Sjoling S, Tanudji M & Whelan J (1998)Mitochondrial protein import in plants. Signals, sorting,targeting, processing and regulation. Plant Mol Biol 38,311–338.36 Soll J & Schleiff E (2004) Protein import into chlorop-lasts. Nat Rev Mol Cell Biol 5, 198–208.37 Jarvis P (2008) Targeting of nucleus-encoded proteinsto chloroplasts in plants. New Phytol 179, 257–285.38 Lister R, Carrie C, Duncan O, Ho LH, Howell KA,Murcha MW & Whelan J (2007) Functional definitionof outer membrane proteins involved in preproteinimport into mitochondria. Plant Cell 19, 3739–3759.39 Neupert W & Herrmann JM (2007) Translocation ofproteins into mitochondria. Annu Rev Biochem 76,723–749.40 Martin T, Sharma R, Sippel C, Waegemann K, Soll J& Vothknecht UC (2006) A protein kinase family inArabidopsis phosphorylates chloroplast precursorproteins. J Biol Chem 281, 40216–40223.41 Waegemann K & Soll J (1996) Phosphorylation of thetransit sequence of chloroplast precursor proteins.J Biol Chem 271, 6545–6554.42 Nakrieko KA, Mould RM & Smith AG (2004) Fidelityof targeting to chloroplasts is not affected by removalof the phosphorylation site from the transit peptide.Eur J Biochem 271, 509–516.43 Beardslee TA, Roy-Chowdhury S, Jaiswal P, Buhot L,Lerbs-Mache S, Stern DB & Allison LA (2002) Anucleus-encoded maize protein with sigma factor activ-ity accumulates in mitochondria and chloroplasts. PlantJ 31, 199–209.44 Buchanan B, Gruissem W & Jones RL (2002) Biochem-istry and Molecular Biology of Plants. American Societyof Plant Physiologists, Rockville, MD.45 Kabeya Y & Sato N (2005) Unique translation initia-tion at the second AUG codon determines mitochon-drial localization of the phage-type RNA polymerasesin the moss Physcomitrella patens. Plant Physiol 138,369–382.Dual targeting of proteins C. Carrie et al.1194 FEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS46 Richter U, Kiessling J, Hedtke B, Decker E, Reski R,Borner T & Weihe A (2002) Two RpoT genes ofPhyscomitrella patens encode phage-type RNA polyme-rases with dual targeting to mitochondria and plastids.Gene 290, 95–105.47 Chew O, Whelan J & Millar AH (2003) Molecular defi-nition of the ascorbate-glutathione cycle in Arabidopsismitochondria reveals dual targeting of antioxidantdefenses in plants. J Biol Chem 278, 46869–46877.48 Smiraglia DJ, Kulawiec M, Bistulfi GL, Ghoshal S &Singh KK (2008) A novel role for mitochondria in regu-lating epigenetic modification in the nucleus. CancerBiol Ther 7, 1182–1190.49 Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD,Berry CC, Millar AH & Ecker JR (2008) Highly inte-grated single-base resolution maps of the epigenome inArabidopsis. Cell 133, 523–536.50 Linka M & Weber AP (2005) Shuffling ammoniabetween mitochondria and plastids during photorespira-tion. Trends Plant Sci 10, 461–465.51 Noctor G, De Paepe R & Foyer CH (2007) Mitochon-drial redox biology and homeostasis in plants. TrendsPlant Sci 12, 125–134.52 Rhoads DM & Subbaiah CC (2007) Mitochondrial ret-rograde regulation in plants. Mitochondrion 7, 177–194.53 Woodson JD & Chory J (2008) Coordination of geneexpression between organellar and nuclear genomes.Nat Rev Genet 9, 383–395.54 Perry AJ, Hulett JM, Likic VA, Lithgow T & GooleyPR (2006) Convergent evolution of receptors for proteinimport into mitochondria. Curr Biol 16, 221–229.55 Saitoh T, Igura M, Obita T, Ose T, Kojima R, Mae-naka K, Endo T & Kohda D (2007) Tom20 recognizesmitochondrial presequences through dynamic equilib-rium among multiple bound states. EMBO J 26, 4777–4787.56 Lister R & Whelan J (2006) Mitochondrial proteinimport: convergent solutions for receptor structure.Curr Biol 16, R197–R199.Supporting informationThe following supplementary material is available:Fig. S1. Relative transcript abundance of genes encod-ing proteins dual targeted to mitochondria and plastidsin Arabidopsis.Table S1. Overview of proteins dual targeted to mito-chondria and plastids in plants.This supplementary material can be found in theonline version of this article.Please note: Wiley-Blackwell is not responsible forthe content or functionality of any supplementarymaterials supplied by the authors. Any queries (otherthan missing material) should be directed to the corre-sponding author for the article.C. Carrie et al. Dual targeting of proteinsFEBS Journal 276 (2009) 1187–1195 ª 2009 The Authors Journal compilation ª 2009 FEBS 1195 . under-standing of the mechanism of dual targeting for the targeting of location-specific proteins is discussed. Targeting signals and mature proteins Targeting. MINIREVIEW Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts Chris Carrie, Estelle Giraud and James
- Xem thêm -

Xem thêm: Báo cáo khoa học: Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts ppt, Báo cáo khoa học: Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts ppt, Báo cáo khoa học: Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts ppt