A split-ubiquitin yeast two-hybrid screen to examine the substrate specificity of atToc159 and atToc132, two arabidopsis chloroplast preprotein import receptors

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Dutta, Siddhartha ^a,b   Teresinski, Howard J ^a,c   Smith, Matthew D ^a  

^a WILFRID LAURIER UNIVERSITY   (Canada)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROTEIN PRECURSOR; UBIQUITIN; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; CELL RECEPTOR; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PEPTIDE; PROTEIN BINDING; TOC132 PROTEIN, ARABIDOPSIS; TOC159 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; CHLOROPLAST; CONTROLLED STUDY; ENZYME SPECIFICITY; GENE LIBRARY; GENETIC SCREENING; IN VITRO STUDY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; RECEPTOR BINDING; SEQUENCE HOMOLOGY; TWO HYBRID SYSTEM; YEAST; CHEMISTRY; GENE EXPRESSION; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CHLOROPLASTS; GENE EXPRESSION; GENE LIBRARY; GTP PHOSPHOHYDROLASES; MEMBRANE PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84899697327     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095026     Document Type: Article

References (87)

1. Galili G (1995) Regulation of Lysine and Threonine Synthesis. Plant Cell 7: 899-906.
2. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957-970.
3. Neuhaus HE, Emes MJ (2000) Nonphotosynthetic Metabolism in Plastids. Annu Rev Plant Physiol Plant Mol Biol 51: 111-140.
4. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57: 739-759. (Pubitemid 44061043)
5. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5: 123-135. (Pubitemid 38160279)
6. Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49: 557-577. (Pubitemid 41615610)
7. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, et al. (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99: 12246-12251.
8. Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179: 257-285. (Pubitemid 351991410)
9. Kessler F, Schnell DJ (2006) The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7: 248-257. (Pubitemid 43323953)
10. Smith MD (2006) Protein import into chloroplasts: an ever-evolving story. Can J Bot 84: 12.
11. Stengel A, Soll J, Bolter B (2007) Protein import into chloroplasts: new aspects of a well-known topic. Biol Chem 388: 765-772. (Pubitemid 47184848)
12. Bionda T, Tillmann B, Simm S, Beilstein K, Ruprecht M, et al. (2010) Chloroplast import signals: the length requirement for translocation in vitro and in vivo. J Mol Biol 402: 510-523.
13. Bruce BD (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10: 440-447.
14. Bruce BD (2001) The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim Biophys Acta 1541: 2-21. (Pubitemid 34024825)
15. Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J (1994) A receptor component of the chloroplast protein translocation machinery. Science 266: 1989-1992.
16. Kouranov A, Schnell DJ (1997) Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. J Cell Biol 139: 1677-1685. (Pubitemid 28079233)
17. Ma Y, Kouranov A, LaSala SE, Schnell DJ (1996) Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J Cell Biol 134: 315-327. (Pubitemid 26250701)
18. Perry SE, Keegstra K (1994) Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6: 93-105.
19. Smith MD, Rounds CM, Wang F, Chen K, Afitlhile M, et al. (2004) atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J Cell Biol 165: 323-334. (Pubitemid 38649908)
20. Sveshnikova N, Soll J, Schleiff E (2000) Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc Natl Acad Sci U S A 97: 4973-4978. (Pubitemid 30238667)
21. Bauer J, Hiltbrunner A, Weibel P, Vidi PA, Alvarez-Huerta M, et al. (2002) Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. J Cell Biol 159: 845-854. (Pubitemid 36008366)
22. Becker T, Jelic M, Vojta A, Radunz A, Soll J, et al. (2004) Preprotein recognition by the Toc complex. EMBO J 23: 520-530. (Pubitemid 38282384)
23. Kessler F, Schnell DJ (2004) Chloroplast protein import: solve the GTPase riddle for entry. Trends Cell Biol 14: 334-338. (Pubitemid 38891700)
24. Teng YS, Chan PT, Li HM (2012) Differential age-dependent import regulation by signal peptides. PLoS Biol 10: e1001416.
25. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, et al. (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403: 203-207. (Pubitemid 30050964)
26. Hiltbrunner A, Grunig K, Alvarez-Huerta M, Infanger S, Bauer J, et al. (2004) AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery. Plant Mol Biol 54: 427-440. (Pubitemid 39059567)
27. Jackson-Constan D, Keegstra K (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125: 1567-1576. (Pubitemid 32375741)
28. Kubis S, Patel R, Combe J, Bedard J, Kovacheva S, et al. (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16: 2059-2077. (Pubitemid 39059728)
29. Ivanova Y, Smith MD, Chen K, Schnell DJ (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 15: 3379-3392. (Pubitemid 38850131)
30. Richardson LG, Jelokhani-Niaraki M, Smith MD (2009) The acidic domains of the Toc159 chloroplast preprotein receptor family are intrinsically disordered protein domains. BMC Biochem 10: 35.
31. Inoue K (2011) Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci 16: 550-557.
32. Infanger S, Bischof S, Hiltbrunner A, Agne B, Baginsky S, et al. (2011) The chloroplast import receptor Toc90 partially restores the accumulation of Toc159 client proteins in the Arabidopsis thaliana ppi2 mutant. Mol Plant 4: 252-263.
33. Constan D, Patel R, Keegstra K, Jarvis P (2004) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J 38: 93-106. (Pubitemid 38448447)
34. 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.
35. Lee DW, Kim JK, Lee S, Choi S, Kim S, et al. (2008) Arabidopsis nuclearencoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20: 1603-1622. (Pubitemid 352844166)
36. Richly E, Leister D (2004) An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene 329: 11-16. (Pubitemid 38366490)
37. Inoue H, Rounds C, Schnell DJ (2010) The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22: 1947-1960.
38. Chotewutmontri P, Reddick LE, McWilliams DR, Campbell IM, Bruce BD (2012) Differential transit peptide recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 24: 3040-3059.
39. Bhushan S, Kuhn C, Berglund AK, Roth C, Glaser E (2006) The role of the Nterminal domain of chloroplast targeting peptides in organellar protein import and miss-sorting. FEBS Lett 580: 3966-3972. (Pubitemid 43946880)
40. vonHeijne G, Steppuhn J, Herrmann RG (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535-545. (Pubitemid 19111117)
41. Zhang XP, Glaser E (2002) Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci 7: 14-21. (Pubitemid 34108194)
42. Lee DW, Lee S, Oh YJ, Hwang I (2009) Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts. Plant Physiol 151: 129-141.
43. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208. (Pubitemid 40314921)
44. Berggard T, Linse S, James P (2007) Methods for the detection and analysis of protein-protein interactions. Proteomics 7: 2833-2842. (Pubitemid 47359924)
45. Phizicky EM, Fields S (1995) Protein-protein interactions: methods for detection and analysis. Microbiol Rev 59: 94-123.
46. Stoevesandt O, Taussig MJ, He M (2009) Protein microarrays: high-throughput tools for proteomics. Expert Rev Proteomics 6: 145-157.
47. Caliebe A, Grimm R, Kaiser G, Lubeck J, Soll J, et al. (1997) The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J 16: 7342-7350. (Pubitemid 28010494)
48. Kikuchi S, Bedard J, Hirano M, Hirabayashi Y, Oishi M, et al. (2013) Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339: 571-574.
49. Kovacs-Bogdan E, Benz JP, Soll J, Bolter B Tic20 forms a channel independent of Tic110 in chloroplasts. BMC Plant Biol 11: 133.
50. Kuchler M, Decker S, Hormann F, Soll J, Heins L (2002) Protein import into chloroplasts involves redox-regulated proteins. EMBO J 21: 6136-6145. (Pubitemid 35415330)
51. Nielsen E, Akita M, Davila-Aponte J, Keegstra K (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 16: 935-946. (Pubitemid 27113173)
52. Benz JP, Stengel A, Lintala M, Lee YH, Weber A, et al. (2009) Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 21: 3965-3983.
53. Aronsson H, Combe J, Patel R, Agne B, Martin M, et al. (2010) Nucleotide binding and dimerization at the chloroplast pre-protein import receptor, atToc33, are not essential in vivo but do increase import efficiency. Plant J 63: 297-311.
54. Bedard J, Kubis S, Bimanadham S, Jarvis P (2007) Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). J Biol Chem 282: 21404-21414. (Pubitemid 47099947)
55. Auerbach D, Thaminy S, Hottiger MO, Stagljar I (2002) The post-genomic era of interactive proteomics: facts and perspectives. Proteomics 2: 611-623. (Pubitemid 34693559)
56. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, et al. (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A 98: 4569-4574. (Pubitemid 32295017)
57. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, et al. (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403: 623-627. (Pubitemid 30103994)
58. Johnsson N, Varshavsky A (1994) Split ubiquitin as a sensor of protein interactions in vivo. Proc Natl Acad Sci U S A 91: 10340-10344. (Pubitemid 24328992)
59. Fetchko M, Stagljar I (2004) Application of the split-ubiquitin membrane yeast two-hybrid system to investigate membrane protein interactions. Methods 32: 349-362. (Pubitemid 38299326)
60. Iyer K, Burkle L, Auerbach D, Thaminy S, Dinkel M, et al. (2005) Utilizing the split-ubiquitin membrane yeast two-hybrid system to identify protein-protein interactions of integral membrane proteins. Sci STKE 2005: pl3.
61. Snider J, Kittanakom S, Damjanovic D, Curak J, Wong V, et al. (2010) Detecting interactions with membrane proteins using a membrane two-hybrid assay in yeast. Nat Protoc 5: 1281-1293.
62. Pandey S, Assmann SM (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein alpha subunit GPA1 and regulates abscisic acid signaling. Plant Cell 16: 1616-1632. (Pubitemid 38774253)
63. Lentze N, Auerbach D (2008) Membrane-based yeast two-hybrid system to detect protein interactions. Curr Prot Protein Sci Chapter 19: Unit 19 17.
64. Burke D, Dawson D, and Stearns T. (2000) Methods in yeast genetics: A Cold Spring Harbor Laboratory course manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
65. Gietz RD, Schiestl RH (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protocol 2: 31-34. (Pubitemid 47040065)
66. Smith MD, Hiltbrunner A, Kessler F, Schnell DJ (2002) The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J Cell Biol 159: 833-843. (Pubitemid 36008365)
67. Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272. (Pubitemid 18007116)
68. Fashena SJ, Serebriiskii I, Golemis EA (2000) The continued evolution of twohybrid screening approaches in yeast: how to outwit different preys with different baits. Gene 250: 1-14. (Pubitemid 30347475)
69. Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340: 245-246. (Pubitemid 19171591)
70. Serebriiskii IG, Toby GG, Golemis EA (2000) Streamlined yeast colorimetric reporter activity assays using scanners and plate readers. Biotechniques 29: 278-279, 282-274, 286-278.
71. Breeden L, Nasmyth K (1985) Regulation of the yeast HO gene. Cold Spring Harb Symp Quant Biol 50: 643-650.
72. Wallas TR, Smith MD, Sanchez-Nieto S, Schnell DJ (2003) The roles of toc34 and toc75 in targeting the toc159 preprotein receptor to chloroplasts. J Biol Chem 278: 44289-44297. (Pubitemid 37377174)
73. Overton MC, Blumer KJ (2002) The extracellular N-terminal domain and transmembrane domains 1 and 2 mediate oligomerization of a yeast G proteincoupled receptor. J Biol Chem 277: 41463-41472. (Pubitemid 35257448)
74. Sun Q, Emanuelsson O, van Wijk KJ (2004) Analysis of curated and predicted plastid subproteomes of Arabidopsis. Subcellular compartmentalization leads to distinctive proteome properties. Plant Physiol 135: 723-734.
75. Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, et al. (2010) AT-CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9: 1063-1084.
76. Ueda M, Nishikawa T, Fujimoto M, Takanashi H, Arimura S, et al. (2008) Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol Biol Evol 25: 1566-1575. (Pubitemid 352019838)
77. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, et al. (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14: 354-362. (Pubitemid 38431168)
78. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, et al. (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLOS One 3: e1994.
79. Hurt EC, Soltanifar N, Goldschmidt-Clermont M, Rochaix JD, Schatz G (1986) The cleavable pre-sequence of an imported chloroplast protein directs attached polypeptides into yeast mitochondria. EMBO J 5: 1343-1350.
80. Ulrich T, Gross LE, Sommer MS, Schleiff E, Rapaport D (2012) Chloroplast beta-barrel proteins are assembled into the mitochondrial outer membrane in a process that depends on the TOM and TOB complexes. J Biol Chem 287: 27467-27479.
81. Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, et al. (2006) Twohybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46: 890-900. (Pubitemid 43780633)
82. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, et al. (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33: 1597-1613.
83. Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150: 1050-1061.
84. Kamal AH, Cho K, Kim DE, Uozumi N, Chung KY, et al. (2012) Changes in physiology and protein abundance in salt-stressed wheat chloroplasts. Mol Biol Rep 39: 9059-9074.
85. Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics 72: 367-378.
86. Friedman AL, Keegstra K (1989) Chloroplast protein import: quantitative analysis of precursor binding. Plant Physiol 89: 993-999.
87. Bischof S, Baerenfaller K, Wildhaber T, Troesch R, Vidi PA, et al. (2011) Plastid proteome assembly without Toc159: photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins. Plant Cell 23: 3911-3928. Canada