Widespread dual targeting of proteins in land plants: When, where, how and why

Plant Signaling and Behavior

Volumn 8, Issue 8, 2013, Pages

  Carrie, Chris ^a   Whelan, James ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Chloroplasts; Dual targeting; Evolution; Mitochondria; Peroxisomes

Indexed keywords

EMBRYOPHYTA;

VEGETABLE PROTEIN;

ARTICLE; EMBRYOPHYTA; METABOLISM; PROTEIN TRANSPORT;

EMBRYOPHYTA; PLANT PROTEINS; PROTEIN TRANSPORT;

EID: 84881154724     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.25034     Document Type: Article

References (42)

1. Creissen G, Reynolds H, Xue Y, Mullineaux P. Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J 1995; 8:167-75. PMID:7670502; http://dx.doi. org/10.1046/j.1365-313X.1995.08020167.x
2. Carrie C, Kühn K, Murcha MW, Duncan O, Small ID, O'Toole N, et al. Approaches to defining dual-targeted proteins in Arabidopsis. Plant J 2009; 57:1128-39. PMID:19036033; http://dx.doi. org/10.1111/j.1365-313X.2008.03745.x
3. Carrie C, Murcha MW, Kuehn K, Duncan O, Barthet M, Smith PM, et al. Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett 2008; 582:3073-9. PMID:18703057; http://dx.doi.org/10.1016/j.febslet.2008.07.061
4. Souciet G, Menand B, Ovesna J, Cosset A, Dietrich A, Wintz H. Characterization of two bifunctional Arabdopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs. Eur J Biochem 1999; 266:848-54. PMID:10583378; http://dx.doi.org/10.1046/j.1432- 1327.1999.00922.x
5. Lee J, Lee H, Kim J, Lee S, Kim DH, Kim S, et al. Both the hydrophobicity and a positively charged region flanking the C-terminal region of the transmembrane domain of signal-anchored proteins play critical roles in determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in Arabidopsis cells. Plant Cell 2011; 23:1588-607. PMID:21515817; http://dx.doi. org/10.1105/tpc.110.082230
6. Reisen D, Hanson MR. Association of six YFPmyosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol 2007; 7:6. PMID:17288617; http://dx.doi.org/10.1186/1471-2229-7-6
7. Robert N, d'Erfurth I, Marmagne A, Erhardt M, Allot M, Boivin K, et al. Voltage-dependent-anionchannels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Mol Biol 2012; 78:431-46. PMID:22294207; http://dx.doi.org/10.1007/ s11103-012-9874-5
8. Hooks KB, Turner JE, Graham IA, Runions J, Hooks MA. GFP-tagging of Arabidopsis acyl-activating enzymes raises the issue of peroxisome-chloroplast import competition versus dual localization. J Plant Physiol 2012; 169:1631-8. PMID:22920973; http:// dx.doi.org/10.1016/j.jplph.2012.05.026
9. Thatcher LF, Carrie C, Andersson CR, Sivasithamparam K, Whelan J, Singh KB. Differential gene expression and subcellular targeting of Arabidopsis glutathione S-transferase F8 is achieved through alternative transcription start sites. J Biol Chem 2007; 282:28915-28. PMID:17670748; http://dx.doi.org/10.1074/jbc.M702207200
10. Schwacke R, Fischer K, Ketelsen B, Krupinska K, Krause K. Comparative survey of plastid and mitochondrial targeting properties of transcription factors in Arabidopsis and rice. Mol Genet Genomics 2007; 277:631-46. PMID:17295027; http://dx.doi. org/10.1007/s00438-007-0214-4
11. Xu L, Carrie C, Law SR, Murcha MW, Whelan J. Acquisition, conservation, and loss of dual-targeted proteins in land plants. Plant Physiol 2013; 161:644-62. PMID:23257241; http://dx.doi.org/10.1104/ pp.112.210997
12. Chew O, Whelan J, Millar AH. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 2003; 278:46869-77. PMID:12954611; http://dx.doi.org/10.1074/jbc. M307525200
13. Rokov-Plavec J, Dulic M, Duchêne AM, Weygand- Durasevic I. Dual targeting of organellar seryl-tRNA synthetase to maize mitochondria and chloroplasts. Plant Cell Rep 2008; 27:1157-68. PMID:18392626; http://dx.doi.org/10.1007/s00299-008-0542-9
14. Duchêne AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, et al. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc Natl Acad Sci USA 2005; 102:16484-9. PMID:16251277; http://dx.doi. org/10.1073/pnas.0504682102
15. Hirakawa Y, Burki F, Keeling PJ. Dual targeting of aminoacyl-tRNA synthetases to the mitochondrion and complex plastid in chlorarachniophytes. J Cell Sci 2012; 125:6176-84. PMID:23038770; http:// dx.doi.org/10.1242/jcs.116533
16. Nilsson A, Olsson T, Ulfstedt M, Thelander M, Ronne H. Two novel types of hexokinases in the moss Physcomitrella patens. BMC Plant Biol 2011; 11:32. PMID:21320325; http://dx.doi.org/10.1186/1471- 2229-11-32
17. Burak E, Yogev O, Sheffer S, Schueler-Furman O, Pines O. Evolving dual targeting of a prokaryotic protein in yeast. Mol Biol Evol 2013. PMID:23462316; http://dx.doi.org/10.1093/molbev/mst039
18. Bahaji A, Muñoz FJ, Ovecka M, Baroja-Fernández E, Montero M, Li J, et al. Specific delivery of AtBT1 to mitochondria complements the aberrant growth and sterility phenotype of homozygous Atbt1 Arabidopsis mutants. Plant J 2011; 68:1115-21. PMID:21883554; http://dx.doi.org/10.1111/j.1365-313X.2011.04767.x
19. Kühn K, Richter U, Meyer EH, Delannoy E, de Longevialle AF, O'Toole N, et al. Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell 2009; 21:2762-79. PMID:19783760; http://dx.doi.org/10.1105/tpc.109.068536
20. Xu YZ, Arrieta-Montiel MP, Virdi KS, de Paula WB, Widhalm JR, Basset GJ, et al. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 2011; 23:3428-41. PMID:21934144; http:// dx.doi.org/10.1105/tpc.111.089136
21. Carrie C, Small I. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochim Biophys Acta 2013; 1833:253-9. PMID:22683762; http://dx.doi.org/10.1016/j.bbamcr.2012.05.029
22. Carrie C, Giraud E, Whelan J. Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts. FEBS J 2009; 276:1187-95. PMID:19187233; http://dx.doi.org/10.1111/j.1742- 4658.2009.06876.x
23. Law SR, Narsai R, Taylor NL, Delannoy E, Carrie C, Giraud E, et al. Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol 2012; 158:1610-27. PMID:22345507; http://dx.doi.org/10.1104/ pp.111.192351
24. Leister D, Wang X, Haberer G, Mayer KF, Kleine T. Intracompartmental and intercompartmental transcriptional networks coordinate the expression of genes for organellar functions. Plant Physiol 2011; 157:386-404. PMID:21775496; http://dx.doi. org/10.1104/pp.111.177691
25. Elo A, Lyznik A, Gonzalez DO, Kachman SD, Mackenzie SA. Nuclear genes that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Plant Cell 2003; 15:1619-31. PMID:12837951; http://dx.doi. org/10.1105/tpc.010009
26. Alexeyenko A, Millar AH, Whelan J, Sonnhammer EL. Chromosomal clustering of nuclear genes encoding mitochondrial and chloroplast proteins in Arabidopsis. Trends Genet 2006; 22:589-93. PMID:16979780; http://dx.doi.org/10.1016/j. tig.2006.09.002
27. Martin W. Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 2010; 365:847-55. PMID:20124349; http://dx.doi.org/10.1098/rstb.2009.0252
28. Carrie C, Giraud E, Duncan O, Xu L, Wang Y, Huang S, et al. Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. J Biol Chem 2010; 285:36138-48. PMID:20829360; http://dx.doi. org/10.1074/jbc.M110.121202
29. Reddehase S, Grumbt B, Neupert W, Hell K. The disulfide relay system of mitochondria is required for the biogenesis of mitochondrial Ccs1 and Sod1. J Mol Biol 2009; 385:331-8. PMID:19010334; http:// dx.doi.org/10.1016/j.jmb.2008.10.088
30. Regev-Rudzki N, Pines O. Eclipsed distribution: a phenomenon of dual targeting of protein and its significance. Bioessays 2007; 29:772-82. PMID:17621655; http://dx.doi.org/10.1002/ bies.20609
31. Regev-Rudzki N, Battat E, Goldberg I, Pines O. Dual localization of fumarase is dependent on the integrity of the glyoxylate shunt. Mol Microbiol 2009; 72:297-306. PMID:19415796; http://dx.doi. org/10.1111/j.1365-2958.2009.06659.x
32. Beardslee TA, Roy-Chowdhury S, Jaiswal P, Buhot L, Lerbs-Mache S, Stern DB, et al. A nucleusencoded maize protein with sigma factor activity accumulates in mitochondria and chloroplasts. Plant J 2002; 31:199-209. PMID:12121449; http://dx.doi. org/10.1046/j.1365-313X.2002.01344.x
33. Paul P, Simm S, Blaumeiser A, Scharf KD, Fragkostefanakis S, Mirus O, et al. The protein translocation systems in plants - composition and variability on the example of Solanum lycopersicum. BMC Genomics 2013; 14:189. PMID:23506162; http://dx.doi.org/10.1186/1471-2164-14-189
34. Lamberti G, Drurey C, Soll J, Schwenkert S. The phosphorylation state of chloroplast transit peptides regulates preprotein import. Plant Signal Behav 2011; 6:1918-20. PMID:22105029; http://dx.doi. org/10.4161/psb.6.12.18127
35. Lamberti G, Gügel IL, Meurer J, Soll J, Schwenkert S. The cytosolic kinases STY8, STY17, and STY46 are involved in chloroplast differentiation in Arabidopsis. Plant Physiol 2011; 157:70-85. PMID:21799034; http://dx.doi.org/10.1104/pp.111.182774
36. Michaud M, Maréchal-Drouard L, Duchêne AM. RNA trafficking in plant cells: targeting of cytosolic mRNAs to the mitochondrial surface. Plant Mol Biol 2010; 73:697-704. PMID:20506035; http://dx.doi. org/10.1007/s11103-010-9650-3
37. Weis BL, Schleiff E, Zerges W. Protein targeting to subcellular organelles via MRNA localization. Biochim Biophys Acta 2013; 1833:260-73. PMID:23457718; http://dx.doi.org/10.1016/j.bbamcr. 2012.04.004
38. Stengel A, Benz JP, Buchanan BB, Soll J, Bölter B. Preprotein import into chloroplasts via the Toc and Tic complexes is regulated by redox signals in Pisum sativum. Mol Plant 2009; 2:1181-97. PMID:19995724; http://dx.doi.org/10.1093/mp/ ssp043
39. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA. SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 2013; 41:D1185-91. PMID:23180787; http://dx.doi. org/10.1093/nar/gks1151
40. Cabantous S, Terwilliger TC, Waldo GS. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat Biotechnol 2005; 23:102-7. PMID:15580262; http://dx.doi.org/10.1038/nbt1044
41. Karniely S, Rayzner A, Sass E, Pines O. Alphacomplementation as a probe for dual localization of mitochondrial proteins. Exp Cell Res 2006; 312:3835-46. PMID:17034789; http://dx.doi. org/10.1016/j.yexcr.2006.08.021
42. Romanini DW, Cornish VW. Protein labelling: Playing tag with proteins. Nat Chem 2012; 4:248-50. PMID:22437705; http://dx.doi.org/10.1038/ nchem.1325