Evidence for lateral gene transfer (LGT) in the evolution of eubacteria-derived small GTPases in plant organelles

Frontiers in Plant Science

Volumn 5, Issue DEC, 2014, Pages

  Suwastika, I Nengah ^a,b   Denawa, Masatsugu ^a   Yomogihara, Saki ^c   Im, Chak Han ^d   Bang, Woo Young ^d   Ohniwa, Ryosuke L ^e   Bahk, Jeong Dong ^d   Takeyasu, Kunio ^a   Shiina, Takashi ^c  

^a KYOTO UNIVERSITY   (Japan)

^b TADULAKO UNIVERSITY   (Indonesia)

^c KYOTO PREFECTURAL UNIVERSITY   (Japan)

^d Gyeongsang National University   (South Korea)

^e UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Endosymbiotic gene transfer; Evolution of organelle; Genomic analysis; Lateral gene transfer; Small GTPase

Indexed keywords

ALGAE; ALPHAPROTEOBACTERIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); BACTEROIDES; CHLOROFLEXI; CYANOBACTERIA; EMBRYOPHYTA; EUKARYOTA; LANGAT VIRUS; PROKARYOTA; PROTEOBACTERIA;

EID: 84917740883     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00678     Document Type: Article

References (61)

1. Abdallah, F., Salamini, F., and Leister, D. (2000). A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 5, 141-142. doi: 10.1016/S1360-1385(00)01574-0
2. Akiyama, T., Gohda, J., Shibata, S., Nomura, Y., Azuma, S., Ohmori, Y., et al. (2001). Mammalian homologue of E. coli ras-like GTPase (ERA) is a possible apoptosis regulator with RNA binding activity. Gene Cell 6, 987-1001. doi: 10.1046/j.1365-2443.2001.00480.x
3. Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 62, 1182-1197. doi: 10.1007/s00018-005-4539-z
4. Archibald, J. M., Rogers, M. B., Toop, M., Ishida, K.-I., and Keeling, P. J. (2003). Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. U.S.A. 100, 7678-7683. doi: 10.1073/pnas.1230951100
5. Arigoni, F., Talabot, F., Peitsch, M., Edgerton, M. D., Meldrum, E., Allet, E., et al. (1998). A genome-based approach for the identification of essential bacterial genes. Nat. Biotechnol. 16, 851-856. doi: 10.1038/nbt0998-851
6. Ball, S. G., Subtil, A., Bhattacharya, D., Moustafa, A., Weber, A. P., Gehre, L., et al. (2013). Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell 25, 7-21. doi: 10.1105/tpc.112.101329
7. Bang, W. Y., Chen, J., Jeong, I. S., Kim, S. W., Kim, C. W., Jung, H. S., et al. (2012). Functional characterization of ObgC in ribosome biogenesis during chloroplast development. Plant J. 71, 122-134. doi: 10.1111/j.1365-313X.2012.04976.x
8. Bang, W. Y., Hata, A., Im, C. H., Ishizaki, Y., Suwastika, I. N., Jeong, I. S., et al. (2009). Chloroplast ribosome-associated AtObgC is crucial for embryogenesis at the early stage. Plant Mol. Biol. 71, 379-390. doi: 10.1007/s11103-009-9529-3
9. Barlow, M. (2009). What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol. Biol. 532, 397-411. doi: 10.1007/978-1-60327-853-9_23
10. Baumgartner, B. J., Rapp, J. C., and Mullet, J. E. (1993). Plastid genes encoding the transcription/translation apparatus are differentially transcribed early in barley (Hordeum vulgare) chloroplast development. Plant Physiol. 101, 781-791.
11. Becker, B., Hoef-Emden, K., and Melkonian, M. (2008). Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol. Biol. 8:203. doi: 10.1186/1471-2148-8-203
12. Bharat, A., Jiang, M., Sullivan, S. M., Maddock, J. R., and Brown, E. D. (2006). Cooperative and critical roles for both G domains in the GTPase activity and cellular function of ribosome-associated Escherichia coli EngA. J. Bacteriol. 188, 7992-7996. doi: 10.1128/JB.00959-06
13. Bock, R. (2010). The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci. 15, 11-22. doi: 10.1016/j.tplants.2009.10.001
14. Brinkman, F. S. L., Blanchard, J. L., Cherkasov, A., Av-Gay, Y., Brunham, R. C., Fernandez, R. C., et al. (2002). Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res. 12, 1159-1167. doi: 10.1101/gr.341802
15. Britton, R. A., Powell, B. S., Dasgupta, S., Sun, Q., Margolin, W., Lupski, J. R., et al. (1998). Cell cycle arrest in Era GTPase mutants: a potential growth rate-regulated checkpoint in Escherichia coli. Mol. Microbiol. 27, 739-750. doi: 10.1046/j.1365-2958.1998.00719.x
16. Colby, G., Wu, M., and Tzagoloff, A. (1998). MTO1 codes for a mitochondrial protein required for respiration in paromomycin-resistant mutants of Saccharomyces cerevisiae. J. Biol. Chem. 273, 27945-27952. doi: 10.1074/jbc.273.43.27945
17. Dassain, M., Leroy, A., Colosetti, L., Carolé, S., and Bouché, J. P. (1999). A new essential gene of the 'minimal genome' affecting cell division. Biochimie 81, 889-895. doi: 10.1016/S0300-9084(99)00207-2
18. Datta, K., Fuentes, J. L., and Maddock, J. R. (2005). The Yeast GTPase Mtg2p is required for mitochondrial translation and partially suppresses an rRNA methyltransferase mutant, mm2. Mol. Biol. Cell 16, 954-963. doi: 10.1091/mbc.E04-07-0622
19. Datta, K., Skidmore, J. M., Pu, K., and Maddock, J. R. (2004). The Caulobacter crescentus GTPase CgtAC is required for progression through the cell cycle and for maintaining 50S ribosomal sublevels. Mol. Microbiol. 54, 1379-1392. doi: 10.1111/j.1365-2958.2004.04354.x
20. Decoster, E., Vassal, A., and Faye, G. (1993). MSS1, a nuclear-encoded mitochondrial GTPase involved in the expression of COX1 subunit of cytochrome c oxidase. J. Mol. Biol. 232, 79-88. doi: 10.1006/jmbi.1993.1371
21. Deusch, E. W., Lam, H., and Aebersold, R. (2008). PeptideAtlas: a resource for target selection for emerging targeted proteomics workflows. EMBO Rep. 9, 429-434. doi: 10.1038/embor.2008.56
22. Grauvogela, C., and Petersen, J. (2007). Isoprenoid biosynthesis authenticates the classification of the green algaMesostigma viride as an ancient streptophyte. Gene 396, 125-133. doi: 10.1016/j.gene.2007.02.020
23. Hang, J. Q., and Zhao, G. (2003). Characterization of the 16S rRNA- and membrane-binding domains ofStreptococcus pneumoniae Era GTPase structural and functional implications. Eur. J. Biochem. 270, 4164-4172. doi: 10.1046/j.1432-1033.2003.03813.x
24. Hirano, Y., Ohniwa, R. L., Wada, C., Yoshimura, S., and Takeyasu, K. (2006). Human small G proteins, Obg H1 and Obg H2 participate in the maintenance of mitochondria and nucleolar architectures. Genes Cells 11, 1295-1304. doi: 10.1111/j.1365-2443.2006.01017.x
25. Huang, J., and Gogarten, J. P. (2007). Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 8:R99. doi: 10.1186/gb-2007-8-6-r99
26. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G., and Gibson, T. J. (1998). Multiple sequence alignment with CLUSTAL X. Trends Biochem. Sci. 23, 403-405. doi: 10.1016/S0968-0004(98)01285-7
27. Jensen, B. C., Wang, Q., Kifer, C. T., and Parsons, M. (2003). The NOG1 GTP-binding protein is required for biogenesis of the 60 s ribosomal subunit. J. Biol. Chem. 278, 32204-32211. doi: 10.1074/jbc.M304198200
28. Kobayashi, G., Moriya, S., and Wada, C. (2001). Deficiency of essential GTP binding protein ObgE in Escherichia coliinhibits chromosome partition. Mol. Microbiol. 41, 1037-1051. doi: 10.1046/j.1365-2958.2001.02574.x
29. Leipe, D. D., Wolf, Y. I., Koonin, E. V., and Aravind, L. (2002). Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317, 41-72. doi: 10.1006/jmbi.2001.5378
30. Li, B., and Trueb, B. (2000). DRG represents a family of two closely related GTP-binding proteins. Biochim. Biophys. Acta 149, 196-204. doi: 10.1016/S0167-4781(00)00025-7
31. Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., 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. doi: 10.1073/pnas.182432999
32. Martin, W., and Schnarrenberger, C. (1997). The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Gen. 32, 1-18. doi: 10.1007/s002940050241
33. McFaddan, G. I. (2001). Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37, 951-959. doi: 10.1046/j.1529-8817.2001.01126.x
34. Mittenhuber, G. (2001). Comparative genomics of prokaryotic GTP-binding proteins (the Era, Obg, EngA, ThdF (TrmE), YchF and YihA families) and their relationship to eukaryotic GTP-binding proteins (the DRG, ARF, RAB, RAN, RAS and RHO families). J. Mol. Microbiol. Biotechnol. 3, 21-35.
35. Morimoto, T., Loh, P. C., Hirai, T., Asai, K., Kobayashi, K., Moriya, S., et al. (2002). Six GTP binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology 148, 3539-3552.
36. Moustafa, A., Reyes-Prieto, A., and Bhattacharya, D. (2008). Chlamydiae has contributed at least 55 genes to plantae with predominantly plastid functions. PLoS ONE 3:e2205. doi: 10.1371/journal.pone.0002205
37. Nosenko, T., Lidie, K. L., Van Dolah, F. M., Lindquist, E., Cheng, J. F., and Bhattacharya, D. (2006). Chimeric plastid proteome in the Florida "red tide" dinoflagellate Karenia brevis. Mol. Biol. Evol. 23, 2026-2038. doi: 10.1093/molbev/msl074
38. Page, R. D. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358.
39. Park, A. K., Kim, H., and Jin, H. J. (2009). Comprehensive phylogenetic analysis of evolutionarily conserved rRNA adenine dimethyltransferase suggests diverse bacterial contributions to the nucleus-encoded plastid proteome.Mol. Phylogenet. Evol. 50, 282-289. doi: 10.1016/j.ympev.2008.10.020
40. Park, J. H., Jensen, B. C., Kifer, C. T., and Parsons, M. (2001). A novel nucleolar G-protein conserved in eukaryotes.J. Cell Sci. 114, 173-185.
41. Polkinghorne, A., Ziegler, U., González-Hernández, Y., Pospischil, A., Timms, P., and Vaughan, L. (2008). Chlamydophila pneumoniae HflX belongs to an uncharacterized family of conserved GTPases and associates with the Escherichia coli 50S large ribosomal subunit. Microbiology 154, 3537-3546. doi: 10.1099/mic.0.2008/022137-0
42. Qiu, H., Price, D. C., Weber, A. P., Facchinelli, F., Yoon, H. S., and Bhattacharya, D. (2013). Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci. 18, 680-687. doi: 10.1016/j.tplants.2013.09.007
43. Ratief, J. D. (2000). Phylogenetic analysis using PHYLIP. Methods Mol. Biol. 132, 243-258.
44. Reyes-Prieto, A., and Bhattacharya, D. (2007). Phylogeny of Calvin cycle enzymes supports Plantae monophyly.Mol. Phylogenet. Evol. 45, 384-391. doi: 10.1016/j.ympev.2007.02.026
45. Reyes-Prieto, A., and Moustafa, A. (2012). Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci. Rep. 2, 1-12. doi: 10.1038/srep00955
46. Richards, T. A., Dacks, J. B., Campbell, S. A., Blanchard, J. L., Foster, P. G., McLeod, R., et al. (2006). Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot. Cell 5, 1517-1531. doi: 10.1128/EC.00106-06
47. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees.Mol. Biol. Evol. 4, 406-425.
48. Sato, A., Kobayashi, G., Hayashi, H., Yoshida, H., Wada, A., Maeda, M., et al. (2005). The GTP binding protein homolog ObgE is involved in ribosomal maturation. Genes Cells 10, 393-408. doi: 10.1111/j.1365-2443.2005.00851.x
49. Sayed, A., Matsuyama, S., and Inouye, M. (1999). Era, an essential Escherichia coli small G-protein, binds to the 30S ribosomal subunit. Biochem. Biophys. Res. Commun. 264, 51-54. doi: 10.1006/bbrc.1999.1471
50. Schaefer, L., Uicker, W. C., Wicker-Planquart, C., Foucher, A.-E., Jault, J.-M., and Britton, R. A. (2006). Multiple GTPases participate in the assembly of the large ribosomal subunit in Bacillus subtilis. J. Bacteriol. 188, 8252-8258. doi: 10.1128/JB.01213-06
51. Slominska, M., Konopa, G., Wegrzyn, G., and Czyz, A. (2002). Impaired chromosome partitioning and chynchronization of DNA replication initiation in an insertional mutant in the Vibrio harveyi cgtA gene coding for common GTP-binding protein. Biochem. J. 362, 579-584. doi: 10.1042/0264-6021:3620579
52. Suwastika, I. N., Ohniwa, R. L., Takeyasu, K., and Shiina, T. (2014). Plant Drg Proteins are Cytoplasmic Small GTPase-ObgHomologue. Proc. Environ. Sci. 20, 357-364. doi: 10.1016/j.proenv.2014.03.045
53. Sweetlove, L. J., Taylor, N. L., and Leaver, C. J. (2007). Isolation of intact, functional mitochondria from the model plant Arabidopsis thaliana. Methods Mol. Biol. 372, 125-136. doi: 10.1007/978-1-59745-365-3_9
54. Teicha, R., Zaunerb, S., Baurainc, D., Brinkmannc, H., and Petersena, J. (2007). Origin and distribution of Calvin cycle fructose and sedoheptulose bisphosphatases in plantae and complex algae: a single secondary origin of complex red plastids and subsequent propagation via tertiary endosymbioses. Protist 158, 263-276. doi: 10.1016/j.protis.2006.12.004
55. Tomar, S. K., Kumar, P., and Prakash, B. (2011). Deciphering the catalytic machinery in a universally conserved ribosome binding ATPase YchF. Biochem. Biophys. Res. Commun. 408, 459-464. doi: 10.1016/j.bbrc.2011.04.052
56. Uemura, T., Ueda, T., Ohniwa, R. L., Nakano, A., Takeyasu, K., and Sato, M. H. (2004). Systemic analysis of SNARE molecules in Arabidopsis: dissection of the post-golgi network in plant cells. Cell Struct. Funct. 29, 49-65. doi: 10.1247/csf.29.49
57. Verstraeten, N., Fauvart, M., Versées, W., and Michiels, J. (2011). The universally conserved prokaryotic GTPases.Microbiol. Mol. Biol. Rev. 75, 507-542. doi: 10.1128/MMBR.00009-11
58. Waller, R. F., Slamovits, C. H., and Keeling, P. J. (2006). Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellatesresulting in a novel plastid-targeted fusion protein. Mol. Biol. Evol. 23, 1437-1443. doi: 10.1093/molbev/msl008
59. Yagi, Y., and Shiina, T. (2011). Evolutionary aspects of plastid proteins involved in transcription the transcription of a tiny genome is mediated by a complicated machinery. Transcription 3, 290-294. doi: 10.4161/trns.21810
60. Yanagisawa, S., Yoo, S. D., and Sheen, J. (2003). Deferential regulation of EIN3 stability by glucose and ethylene signaling in plants. Nature 425, 521-525. doi: 10.1038/nature01984
61. Yue, J., Hu, X., Sun, H., Yang, Y., and Huang, J. (2012). Widespread impact of horizontal gene transfer on plant colonization of land. Nat. Commun. 3:1152. doi: 10.1038/ncomms2148