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Tail-anchored membrane proteins: exploring the complex diversity of tail-anchored-protein targeting in plant cells

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Abstract

Tail-anchored (TA) proteins are special class of integral membrane proteins that in recent years have received a considerable amount of attention due to their diverse cellular functions and unique targeting and insertion mechanisms. Defined by the presence of a single, hydrophobic membrane-spanning domain at or near their C terminus, TA proteins must be inserted into membranes post-translationally and are orientated such that their larger N-terminal domain (most often the functional domain) faces the cytosol, while their shorter C-terminal domain faces the interior of the organelle. The C-terminal domain of TA proteins also usually contains the information responsible for their selective targeting to the proper subcellular membrane, a process that, based primarily on studies with yeasts and mammals, appears to be highly complex due to the presence of multiple pathways. Within this context, we discuss here the biogenesis of plant TA proteins and the potential for hundreds of new TA proteins identified via bioinformatics screens to contribute to the already remarkable number of roles that this class of membrane proteins participates in throughout plant growth and development.

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Abbreviations

AKR2A:

Ankryin repeat-containing protein 2A

APX:

Ascorbate peroxidase

Cb5:

Cytochrome b 5

DRP:

Dynamin-related protein

ER:

Endoplasmic reticulum

Fis1:

FISSION 1

Get:

Guided entry of tail-anchored proteins

MDAR:

Monodehydroascorbate reductase

OEP:

Outer envelope protein

Pex:

Peroxin

PMD1:

Peroxisomal and mitochondrial division factor 1

PMP:

Peroxisomal membrane protein

SAM:

Sorting and assembly machinery

SNARE:

Soluble NSF attachment protein receptors

SRP:

Signal recognition particle

TA:

Tail-anchored

TOC:

Chloroplast outer envelope translocase

TOM:

Mitochondrial outer membrane translocase

TMD:

Transmembrane domain

TPR:

Tetratricopeptide repeat

WIP:

(Trp-Pro-Pro)-domain-interacting protein

WIT:

(Trp-Pro-Pro)-domain interacting tail-anchored protein

References

  • Abell BM, Jung M, Oliver JD, Knight BC, Tyedmers J, Zimmermann R, High S (2003) Tail-anchored and signal-anchored proteins utilize overlapping pathways during membrane insertion. J Biol Chem 278:5669–5678

    Article  PubMed  CAS  Google Scholar 

  • Abell BM, Hahn M, Holbrook LA, Moloney MM (2004) Membrane topology and sequence requirements for oil body targeting of oleosin. Plant J 37:461–470

    Article  PubMed  CAS  Google Scholar 

  • Abell BM, Rabu C, Leznicki P, Young JC, High S (2007) Post-translational integration of tail-anchored proteins is facilitated by defined molecular chaperones. J Cell Sci 120:1743–1751

    Article  PubMed  CAS  Google Scholar 

  • Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B, Andrews DW (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 24:2096–2103

    Article  PubMed  CAS  Google Scholar 

  • Aung K, Zhang X, Hu J (2010) Peroxisome division and proliferation in plants. Biochem Soc Trans 38:817–822

    Article  PubMed  CAS  Google Scholar 

  • Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I (2008) AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol 10:220–227

    Article  PubMed  CAS  Google Scholar 

  • Bailly A, Sovero V, Geisler M (2006) The twisted dwarf’s ABC: how immunophilins regulate auxin transport. Plant Signal Behav 1:277–280

    Article  PubMed  Google Scholar 

  • Barbante A, Irons S, Hawes C, Frigerio L, Vitale A, Pedrazzini E (2008) Anchorage to the cytosolic face of the endoplasmic reticulum membrane: a new strategy to stabilize a cytosolic recombinant antigen in plants. Plant Biotechnol J 6:560–575

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling and development. Plant Physiol 147:1504–1515

    Article  PubMed  CAS  Google Scholar 

  • Beilharz T, Egan B, Silver PA, Hofmann K, Lithgow T (2003) Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J Biol Chem 278:8219–8223

    Article  PubMed  CAS  Google Scholar 

  • Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77:1496–1500

    Article  PubMed  CAS  Google Scholar 

  • Borgese N, Fasana E (2010) Targeting pathways of C-tail-anchored proteins. Biochim Biophys Acta. doi:10.1016/j.bbamem.2010.07.10

  • Borgese N, Righi M (2010) Remote origins of tail-anchored proteins. Traffic 11:877–885

    Article  PubMed  CAS  Google Scholar 

  • Borgese N, Colombo S, Pedrazzini E (2003) The tale of tail-anchored proteins: coming from the cytosol and looking for a membrane. J Cell Biol 161:1013–1019

    Article  PubMed  CAS  Google Scholar 

  • Borgese N, Brambillasca S, Colombo S (2007) How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 19:368–375

    Article  PubMed  CAS  Google Scholar 

  • Bozkurt G, Stjepanovic G, Vilardi F, Amlacher S, Wild K, Bange G, Favaloro V, Rippe K, Hurt E, Dobberstein B, Sinning I (2009) Structural insights into tail-anchored protein binding and membrane insertion by Get3. Proc Natl Acad Sci USA 106:21131–21136

    Article  PubMed  CAS  Google Scholar 

  • Brambillasca S, Yabal M, Soffientini P, Stefanovic S, Makarow M, Hegde RS, Borgese N (2005) Transmembrane topogenesis of a tail-anchored protein is modulated by membrane lipid composition. EMBO J 24:2533–2542

    Article  PubMed  CAS  Google Scholar 

  • Brambillasca S, Yabal M, Makarow M, Borgese N (2006) Unassisted translocation of large polypeptide domains across phospholipid bilayers. J Cell Biol 175:767–777

    Article  PubMed  CAS  Google Scholar 

  • Brkljacic J, Zhao Q, Meier I (2009) WPP-domain proteins mimic the activity of the HSC70-1 chaperone in preventing mistargeting of RanGAP1-anchoring protein WIT1. Plant Physiol 151:142–154

    Article  PubMed  CAS  Google Scholar 

  • Chang YW, Chuang YC, Ho YC, Cheng MY, Sun YJ, Hsiao CD, Wang C (2010) Crystal structure of Get4-Get5 complex and its interactions with Sgt2, Get3, and Ydj1. J Biol Chem 285:9962–9970

    Article  PubMed  CAS  Google Scholar 

  • Chartron JW, Suloway CJ, Zaslaver M, Clemons WM Jr (2010) Structural characterization of the Get4/Get5 complex and its interaction with Get3. Proc Natl Acad Sci USA 107:12127–12132

    Google Scholar 

  • Choi SB, Wang C, Muench DG, Ozawa K, Franceschi VR, Wu Y, Okita TW (2000) Messenger RNA targeting of rice seed storage proteins to specific ER subdomains. Nature 407:765–767

    Article  PubMed  CAS  Google Scholar 

  • Colombo SF, Longhi R, Borgese N (2009) The role of cytosolic proteins in the insertion of tail-anchored proteins into phospholipid bilayers. J Cell Sci 122:2383–2392

    Article  PubMed  CAS  Google Scholar 

  • de Vetten N, ter Horst J, van Schaik HP, de Boer A, Mol J, Koes R (1999) A cytochrome b 5 is required for full activity of flavonoid 3′, 5′-hydroxylase, a cytochrome P450 involved in the formation of blue flower colors. Proc Natl Acad Sci USA 96:778–783

    Article  PubMed  Google Scholar 

  • del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272

    Article  PubMed  CAS  Google Scholar 

  • Delille HK, Schrader M (2008) Targeting of hFis1 to peroxisomes is mediated by Pex19p. J Biol Chem 283:31107–31115

    Article  PubMed  CAS  Google Scholar 

  • Dhanoa PK, Richardson LG, Smith MD, Gidda SK, Henderson MP, Andrews DW, Mullen RT (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS One 5:e10098

    Article  PubMed  CAS  Google Scholar 

  • Donaldson RP (2002) Peroxisomal membrane enzymes. In: Baker A, Graham IA (eds) Plant peroxisomes: biochemistry, cell biology, and biotechnological applications. Kluwer Academic Publishers, Dordrecht, pp 259–278

  • Fagarasanu A, Fagarasanu M, Rachubinski RA (2007) Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 23:321–344

    Article  PubMed  CAS  Google Scholar 

  • Fan RC, Peng CC, Xu YH, Wang XF, Li Y, Shang Y, Du SY, Zhao R, Zhang XY, Zhang LY, Zhang DP (2009) Apple sucrose transporter SUT1 and sorbitol transporter SOT6 interact with cytochrome b 5 to regulate their affinity for substrate sugars. Plant Physiol 150:1880–1901

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JJ, Chen JC, Miao Y, Shao Y, Lin J, Bock PE, Johnson AE (2003) Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J Biol Chem 278:18628–18637

    Article  PubMed  CAS  Google Scholar 

  • Freiin Loeffelholz von Colberg CO, Kriechbaumer V, Ewan RA, Jonczyk R, Lehmann S, Young JC, Abell BM (2010) OEP61 is a novel chaperone receptor at the chloroplast outer envelope in Arabidopsis. Manuscript in preparation

  • Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390:775–782

    Article  PubMed  CAS  Google Scholar 

  • Gutensohn M, Schulz B, Nicolay P, Flugge UI (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 23:771–783

    Article  PubMed  CAS  Google Scholar 

  • Halbach A, Landgraf C, Lorenzen S, Rosenkranz K, Volkmer-Engert R, Erdmann R, Rottensteiner H (2006) Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J Cell Sci 119:2508–2517

    Article  PubMed  CAS  Google Scholar 

  • Henderson MP, Billen LP, Kim PK, Andrews DW (2007a) Cell-free analysis of tail-anchor protein targeting to membranes. Methods 41:427–438

    Article  PubMed  CAS  Google Scholar 

  • Henderson MP, Hwang YT, Dyer JM, Mullen RT, Andrews DW (2007b) The C-terminus of cytochrome b 5 confers endoplasmic reticulum specificity by preventing spontaneous insertion into membranes. Biochem J 401:701–709

    Article  PubMed  CAS  Google Scholar 

  • High S, Abell BM (2004) Tail-anchored protein biosynthesis at the endoplasmic reticulum: the same but different. Biochem Soc Trans 32:659–662

    Article  PubMed  CAS  Google Scholar 

  • Hofmann NR, Theg SM (2005) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10:450–457

    Article  PubMed  CAS  Google Scholar 

  • Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R, Paneque M, Chen Z, Johansson I, Blatt MR (2009) A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 21:2859–2877

    Article  PubMed  CAS  Google Scholar 

  • Hwang YT, Pelitire SM, Henderson MP, Andrews DW, Dyer JM, Mullen RT (2004) Novel targeting signals mediate the sorting of different isoforms of the tail-anchored membrane protein cytochrome b 5 to either endoplasmic reticulum or mitochondria. Plant Cell 16:3002–3019

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154

    Article  PubMed  CAS  Google Scholar 

  • Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285

    Article  PubMed  CAS  Google Scholar 

  • Janiak F, Leber B, Andrews DW (1994) Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J Biol Chem 269:9842–9849

    PubMed  CAS  Google Scholar 

  • Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282:100–103

    Article  PubMed  CAS  Google Scholar 

  • Jespersen HM, Kjaersgard IV, Ostergaard L, Welinder KG (1997) From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem J 326(Pt 2):305–310

    PubMed  CAS  Google Scholar 

  • Kajander T, Sachs JN, Goldman A, Regan L (2009) Electrostatic interactions of Hsp-organizing protein tetratricopeptide domains with Hsp70 and Hsp90: computational analysis and protein engineering. J Biol Chem 284:25364–25374

    Article  PubMed  CAS  Google Scholar 

  • Kalbfleisch T, Cambon A, Wattenberg BW (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8:1687–1694

    Article  PubMed  CAS  Google Scholar 

  • Karnik SK, Trelease RN (2005) Arabidopsis peroxin 16 coexists at steady state in peroxisomes and endoplasmic reticulum. Plant Physiol 138:1967–1981

    Article  PubMed  CAS  Google Scholar 

  • Karyotou K, Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Arch Biochem Biophys 434:248–257

    Google Scholar 

  • Kaur N, Hu J (2009) Dynamics of peroxisome abundance: a tale of division and proliferation. Curr Opin Plant Biol 12:781–788

    Article  PubMed  CAS  Google Scholar 

  • Kemper C, Habib SJ, Engl G, Heckmeyer P, Dimmer KS, Rapaport D (2008) Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J Cell Sci 121:1990–1998

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21:494–500

    Article  PubMed  CAS  Google Scholar 

  • Kim SG, Park CM (2007a) Membrane-mediated salt stress signaling in flowering time control. Plant Signal Behav 2:517–518

    Article  PubMed  Google Scholar 

  • Kim YS, Park CM (2007b) Membrane regulation of cytokinin-mediated cell division in Arabidopsis. Plant Signal Behav 2:15–16

    Article  PubMed  Google Scholar 

  • Kim PK, Janiak-Spens F, Trimble WS, Leber B, Andrews DW (1997) Evidence for multiple mechanisms for membrane binding and integration via carboxyl-terminal insertion sequences. Biochemistry 36:8873–8882

    Article  PubMed  CAS  Google Scholar 

  • Kim PK, Hollerbach C, Trimble WS, Leber B, Andrews DW (1999) Identification of the endoplasmic reticulum targeting signal in vesicle-associated membrane proteins. J Biol Chem 274:36876–36882

    Article  PubMed  CAS  Google Scholar 

  • Kim PK, Annis MG, Dlugosz PJ, Leber B, Andrews DW (2004) During apoptosis bcl-2 changes membrane topology at both the endoplasmic reticulum and mitochondria. Mol Cell 14:523–529

    Article  PubMed  CAS  Google Scholar 

  • Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144

    Article  PubMed  CAS  Google Scholar 

  • Kriechbaumer V, Shaw R, Mukherjee J, Bowsher CG, Harrison AM, Abell BM (2009) Subcellular distribution of tail-anchored proteins in Arabidopsis. Traffic 10:1753–1764

    Article  PubMed  CAS  Google Scholar 

  • Kutay U, Hartmann E, Rapoport TA (1993) A class of membrane proteins with a C-terminal anchor. Trends Cell Biol 3:72–75

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Wang F, Schnell DJ (2009) Toc receptor dimerization participates in the initiation of membrane translocation during protein import into chloroplasts. J Biol Chem 284:31130–31141

    Article  PubMed  CAS  Google Scholar 

  • Leznicki P, Clancy A, Schwappach B, High S (2010) Bat3 promotes the membrane integration of tail-anchored proteins. J Cell Sci 123:2170–2178

    Article  PubMed  CAS  Google Scholar 

  • Li H, Chen LJ (1997) A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides. J Biol Chem 272:10968–10974

    Article  PubMed  CAS  Google Scholar 

  • Li J, Qian X, Hu J, Sha B (2009) Molecular chaperone Hsp70/Hsp90 prepares the mitochondrial outer membrane translocon receptor Tom71 for preprotein loading. J Biol Chem 284:23852–23859

    Article  PubMed  CAS  Google Scholar 

  • Lindner R, Naim HY (2009) Domains in biological membranes. Exp Cell Res 315:2871–2878

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–1183

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174

    Article  PubMed  CAS  Google Scholar 

  • Lisenbee CS, Heinze M, Trelease RN (2003) Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells. Plant Physiol 132:870–882

    Article  PubMed  CAS  Google Scholar 

  • Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–914

    Article  PubMed  CAS  Google Scholar 

  • Lister R, Carrie C, Duncan O, Ho LH, Howell KA, Murcha MW, Whelan J (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19:3739–3759

    Article  PubMed  CAS  Google Scholar 

  • Macasev D, Newbigin E, Whelan J, Lithgow T (2000) How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol 123:811–816

    Article  PubMed  CAS  Google Scholar 

  • Macasev D, Whelan J, Newbigin E, Silva-Filho MC, Mulhern TD, Lithgow T (2004) Tom22’, an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes. Mol Biol Evol 21:1557–1564

    Article  PubMed  CAS  Google Scholar 

  • Maggio C, Barbante A, Ferro F, Frigerio L, Pedrazzini E (2007) Intracellular sorting of the tail-anchored protein cytochrome b 5 in plants: a comparative study using different isoforms from rabbit and Arabidopsis. J Exp Bot 58:1365–1379

    Article  PubMed  CAS  Google Scholar 

  • Mateja A, Szlachcic A, Downing ME, Dobosz M, Mariappan M, Hegde RS, Keenan RJ (2009) The structural basis of tail-anchored membrane protein recognition by Get3. Nature 461:361–366

    Article  PubMed  CAS  Google Scholar 

  • Matsuzono Y, Fujiki Y (2006) In vitro transport of membrane proteins to peroxisomes by shuttling receptor Pex19p. J Biol Chem 281:36–42

    Article  PubMed  CAS  Google Scholar 

  • May T, Soll J (2000) 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12:53–64

    Article  PubMed  CAS  Google Scholar 

  • Michaud M, Marechal-Drouard L, Duchene AM (2010) RNA trafficking in plant cells: targeting of cytosolic mRNAs to the mitochondrial surface. Plant Mol Biol 73:697–704

    Article  PubMed  CAS  Google Scholar 

  • Motz C, Martin H, Krimmer T, Rassow J (2002) Bcl-2 and porin follow different pathways of TOM-dependent insertion into the mitochondrial outer membrane. J Mol Biol 323:729–738

    Article  PubMed  CAS  Google Scholar 

  • Mullen RT, Trelease RN (2000) The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J Biol Chem 275:16337–16344

    Article  PubMed  CAS  Google Scholar 

  • Mullen RT, Trelease RN (2006) The ER-peroxisome connection in plants: development of the “ER semi-autonomous peroxisome maturation and replication” model for plant peroxisome biogenesis. Biochim Biophys Acta 1763:1655–1668

    Article  PubMed  CAS  Google Scholar 

  • Mullen RT, Lisenbee CS, Miernyk JA, Trelease RN (1999) Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 11:2167–2185

    Article  PubMed  CAS  Google Scholar 

  • Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochim Biophys Acta 1763:1478–1495

    Article  PubMed  CAS  Google Scholar 

  • Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43:697–705

    Article  PubMed  CAS  Google Scholar 

  • Otera H, Taira Y, Horie C, Suzuki Y, Suzuki H, Setoguchi K, Kato H, Oka T, Mihara K (2007) A novel insertion pathway of mitochondrial outer membrane proteins with multiple transmembrane segments. J Cell Biol 179:1355–1363

    Article  PubMed  CAS  Google Scholar 

  • Paquette SM, Jensen K, Bak S (2009) A web-based resource for the Arabidopsis P450, cytochromes b5, NADPH-cytochrome P450 reductases, and family 1 glycosyltransferases (http://www.P450.kvl.dk). Phytochemistry 70:1940–1947

  • Paulick MG, Bertozzi CR (2008) The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47:6991–7000

    Article  PubMed  CAS  Google Scholar 

  • Pedrazzini E (2009) Tail-anchored proteins in plants. J Plant Biol 52:1226–9239

    Article  CAS  Google Scholar 

  • Qbadou S, Tien R, Soll J, Schleiff E (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J Cell Sci 116:837–846

    Article  PubMed  CAS  Google Scholar 

  • Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E (2006) The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J 25:1836–1847

    Article  PubMed  CAS  Google Scholar 

  • Rabu C, Wipf P, Brodsky JL, High S (2008) A precursor-specific role for Hsp40/Hsc70 during tail-anchored protein integration at the endoplasmic reticulum. J Biol Chem 283:27504–27513

    Article  PubMed  CAS  Google Scholar 

  • Rabu C, Schmid V, Schwappach B, High S (2009) Biogenesis of tail-anchored proteins: the beginning for the end? J Cell Sci 122:3605–3612

    Article  PubMed  CAS  Google Scholar 

  • Rosenblad MA, Larsen N, Samuelsson T, Zwieb C (2009) Kinship in the SRP RNA family. RNA Biol 6:508–516

    Article  PubMed  CAS  Google Scholar 

  • Rudhe C, Chew O, Whelan J, Glaser E (2002) A novel in vitro system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J 30:213–220

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Vallet A, Ramos B, Bednarek P, Lopez G, Pislewska-Bednarek M, Schulze-Lefert P, Molina A (2010) Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63:115–127

    Google Scholar 

  • Schrader M, Yoon Y (2007) Mitochondria and peroxisomes: are the ‘big brother’ and the ‘little sister’ closer than assumed? Bioessays 29:1105–1114

    Article  PubMed  CAS  Google Scholar 

  • Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123:507–519

    Article  PubMed  CAS  Google Scholar 

  • Schuldiner M, Metz J, Schmid V, Denic V, Rakwalska M, Schmitt HD, Schwappach B, Weissman JS (2008) The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134:634–645

    Article  PubMed  CAS  Google Scholar 

  • Seedorf M, Waegemann K, Soll J (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J 7:401–411

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Kim SG, Park CM (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13:550–556

    Article  PubMed  CAS  Google Scholar 

  • Setoguchi K, Otera H, Mihara K (2006) Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J 25:5635–5647

    Article  PubMed  CAS  Google Scholar 

  • Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H (2010) ANKYRIN REPEAT-CONTAINING PROTEIN 2A is an essential molecular chaperone for peroxisomal membrane-bound ASCORBATE PEROXIDASE3 in Arabidopsis. Plant Cell 22:811–831

    Article  PubMed  CAS  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  PubMed  CAS  Google Scholar 

  • Stefanovic S, Hegde RS (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128:1147–1159

    Article  PubMed  CAS  Google Scholar 

  • Stojanovski D, Guiard B, Kozjak-Pavlovic V, Pfanner N, Meisinger C (2007) Alternative function for the mitochondrial SAM complex in biogenesis of alpha-helical TOM proteins. J Cell Biol 179:881–893

    Article  PubMed  CAS  Google Scholar 

  • Tabak HF, van der Zand A, Braakman I (2008) Peroxisomes: minted by the ER. Curr Opin Cell Biol 20:393–400

    Article  PubMed  CAS  Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Galvao VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224:300–314

    Article  PubMed  CAS  Google Scholar 

  • Titorenko VI, Rachubinski RA (2009) Spatiotemporal dynamics of the ER-derived peroxisomal endomembrane system. Int Rev Cell Mol Biol 272:191–244

    Article  PubMed  CAS  Google Scholar 

  • Tsai LY, Tu SL, Li HM (1999) Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J Biol Chem 274:18735–18740

    Article  PubMed  CAS  Google Scholar 

  • Van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a protein-conducting channel. Nature 427:36–44

    Article  PubMed  CAS  Google Scholar 

  • van der Zand A, Braakman I, Tabak HF (2010) Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol Biol Cell 21:2057–2065

    Article  PubMed  CAS  Google Scholar 

  • Vergeres G, Waskell L (1995) Cytochrome b 5, its functions, structure and membrane topology. Biochimie 77:604–620

    Article  PubMed  CAS  Google Scholar 

  • Wattenberg B, Lithgow T (2001) Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes. Traffic 2:66–71

    Article  PubMed  CAS  Google Scholar 

  • Werhahn W, Niemeyer A, Jansch L, Kruft V, Schmitz UK, Braun H (2001) Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20. Plant Physiol 125:943–954

    Article  PubMed  CAS  Google Scholar 

  • Xu XM, Meulia T, Meier I (2007) Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-pore-associated proteins. Curr Biol 17:1157–1163

    Article  PubMed  CAS  Google Scholar 

  • Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59

    Article  PubMed  CAS  Google Scholar 

  • Zhao Q, Brkljacic J, Meier I (2008) Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell 20:1639–1651

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Ian Smith for assistance with figure constructions and Verena Kriechbaumer for assistance with manuscript preparation. We apologize to colleagues whose work we have been unable to cite because of space constraints. This work was supported by a Biotechnology and Biological Sciences Research Council Research Grant awarded to BMA and a University of Guelph Research Chair and grant from the Natural Sciences and Engineering Research Council of Canada to RTM.

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Authors and Affiliations

  1. Biomedical Research Centre, Sheffield Hallam University, Howard Street, Sheffield, UK

    Ben M. Abell

  2. Department of Molecular and Cellular Biology, University of Guelph, 50 Stone Road, Science Complex, Room 4470, Guelph, ON, N1G 2W1, Canada

    Robert T. Mullen

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  1. Ben M. Abell
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  2. Robert T. Mullen
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Correspondence to Ben M. Abell or Robert T. Mullen.

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Communicated by R. Reski.

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Abell, B.M., Mullen, R.T. Tail-anchored membrane proteins: exploring the complex diversity of tail-anchored-protein targeting in plant cells. Plant Cell Rep 30, 137–151 (2011). https://doi.org/10.1007/s00299-010-0925-6

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  • DOI: https://doi.org/10.1007/s00299-010-0925-6

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