EF-G

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Protein-synthesizing GTPase
EF-G Post State PDB 4V5F.jpg
Identifiers
EC no. 3.6.5.3
Alt. namesElongation factor G, EF-G
Databases
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BRENDA BRENDA entry
ExPASy NiceZyme view
KEGG KEGG entry
MetaCyc metabolic pathway
PRIAM profile
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PubMed articles
NCBI proteins
Translation elongation factor EFG/EF2
Identifiers
SymbolTransl_elong_EFG/EF2
InterPro IPR004540
SCOP2 1n0u / SCOPe / SUPFAM
EFG/EF2, domain IV
Identifiers
SymbolEFG_IV
Pfam PF03764
Pfam clan CL0329
SMART SM00889
CDD cd01434
Available protein structures:
Pfam   structures / ECOD  
PDB RCSB PDB; PDBe; PDBj
PDBsum structure summary

EF-G (elongation factor G, historically known as translocase) is a prokaryotic elongation factor involved in mRNA translation. As a GTPase, EF-G catalyzes the movement (translocation) of transfer RNA (tRNA) and messenger RNA (mRNA) through the ribosome. [1]

Contents

Structure

Encoded by the fusA gene on the str operon, [2] EF-G is made up of 704 amino acids that form 5 domains, labeled Domain I through Domain V. Domain I may be referred to as the G-domain or as Domain I(G), since it binds to and hydrolyzes guanosine triphosphate (GTP). Domain I also helps EF-G bind to the ribosome, and contains the N-terminal of the polypeptide chain. [3] [4] Domain IV is important for translocation, as it undergoes a significant conformational change and enters the A site on the 30S ribosomal subunit, pushing the mRNA and tRNA molecules from the A site to the P site. [5]

The five domains may be also separated into two super-domains. Super-domain I consists of Domains I and II, and super-domain II consists of Domains III - IV. Throughout translocation, super-domain I will remain relatively unchanged, as it is responsible for binding tightly to the ribosome. However, super-domain II will undergo a large rotational motion from the pre-translocational (PRE) state to the post-translocational (POST) state. Super-domain I is similar to the corresponding sections of EF-Tu. [6] [7] [8] Super-domain II in the POST state mimics the tRNA molecule of the EF-Tu • GTP • aa-tRNA ternary complex. [9]

Crystal structure of EF-G in the POST state with Domains I - V labeled. PDB ID: 4V5F EF-G Post State PDB 4V5F (labeled).jpg
Crystal structure of EF-G in the POST state with Domains I - V labeled. PDB ID: 4V5F

EF-G on the ribosome

Binding to L7/L12

L7/L12 is only a multicopy protein on the large ribosomal subunit of the bacterial ribosome that binds to certain GTPases, like Initiation Factor 2, Elongation factor-Tu, Release Factor 3, and EF-G. [10] Specifically, the C-terminal of L7/L12 will bind to EF-G and is necessary for GTP hydrolysis. [4]

Interaction with the GTPase Associated Center

The GTPase Associated Center (GAC) is a region on the large ribosomal subunit that consists of two smaller regions of 23S ribosomal RNA called the L11 stalk and the sarcin-ricin loop (SRL). [11] As a highly conserved rRNA loop in evolution, the SRL is critical in helping GTPases bind to the ribosome, but is not essential for GTP hydrolysis. There is some evidence to support that a phosphate oxygen in the A2662 residue of the SRL may help hydrolyze GTP. [12]

Animation of the 70S ribosome with the P site tRNA (orange), E site tRNA (green), mRNA (yellow), and elongation factor G (red) in the POST state. PDB ID: 4W29 EF-G, mRNA, and tRNAs in POST state PDB 4W29.gif
Animation of the 70S ribosome with the P site tRNA (orange), E site tRNA (green), mRNA (yellow), and elongation factor G (red) in the POST state. PDB ID: 4W29

Function in protein elongation

EF-G catalyzes the translocation of the tRNA and mRNA down the ribosome at the end of each round of polypeptide elongation. [1] In this process, the peptidyl transferase center (PTC) has catalyzed the formation of a peptide bond between amino acids, moving the polypeptide chain from the P site tRNA to the A site tRNA. The 50S and 30S ribosomal subunits are now allowed to rotate relative to each other by approximately 7°. [13] [14] The subunit rotation is coupled with the movement of the 3' ends of both tRNA molecules on the large subunit from the A and P sites to the P and E sites, respectively, while the anticodon loops remain unshifted. This rotated ribosomal intermediate, in which the first tRNA occupies a hybrid A/P position and the second tRNA occupies a hybrid P/E position is a substrate for EF-G-GTP. [1] [13]

As a GTPase, EF-G binds to the rotated ribosome near the A site in its GTP-bound state, and hydrolyzes GTP, releasing GDP and inorganic phosphate:

The hydrolysis of GTP allows for a large conformational change within EF-G, forcing the A/P tRNA to fully occupy the P site, the P/E tRNA to fully occupy the E site (and exit the ribosome complex), and the mRNA to shift three nucleotides down relative to the ribosome. The GDP-bound EF-G molecule then dissociates from the complex, leaving another free A-site where the elongation cycle can start again. [1] [15]

Crystal structure of the ribosome with two tRNAs (orange and green) and EF-G (in cyan) after translocation. PDB ID: 4W29. EF-G and tRNAs in the POST state.jpg
Crystal structure of the ribosome with two tRNAs (orange and green) and EF-G (in cyan) after translocation. PDB ID: 4W29.

Function in protein termination

Protein elongation continues until a stop codon appears on the mRNA. A Class I release factor (RF1 or RF2) binds to the stop codon, which induces hydrolysis of the tRNA-peptide bond in the P site, allowing the newly-formed protein to exit the ribosome. The nascent peptide continues to fold and leaves the 70S ribosome, the mRNA, the deacylated tRNA (P site), and the Class I release factor (A site). [16] [17]

In a GTP-dependent manner, the subsequent recycling is catalyzed by a Class II release factor named RF3/prfC, Ribosome recycling factor (RRF), Initiation Factor 3 (IF3) and EF-G. The protein RF3 releases the Class I release factor so that it may occupy the ribosomal A site. EF-G hydrolyzes GTP and undergoes a large conformational change to push RF3 down the ribosome, which occurs alongside tRNA dissociation and promotes the ribosomal subunit rotation. This motion actively splits the B2a/B2b bridge, which connects the 30S and the 50S subunits, so that the ribosome can split. [16] IF3 then isolates the 30S subunit to prevent re-association of the large and small subunits. [18]

Clinical significance

EF-G in pathogenic bacteria can be inhibited by antibiotics that prevent EF-G from binding to the ribosome, [19] carrying out translocation [20] or dissociating from the ribosome. [21]

For example, the antibiotic thiostrepton prevents EF-G from binding stably to the ribosome, [19] while the antibiotics dityromycin and GE82832 inhibit the activity of EF-G by preventing the translocation of the A site tRNA. Dityromycin and GE82832 do not affect the binding of EF-G to the ribosome, however. [20]

The antibiotic fusidic acid is known to inhibit Staphylococcus aureus and other bacteria by binding to EF-G after one translocation event on the ribosome, preventing EF-G from dissociating. [21] [22] However, some bacterial strains have developed resistance to fusidic acid due to point mutations in the fusA gene, which prevents fusidic acid from binding to EF-G. [23] [24]

Evolution

EF-G has a complex evolutionary history, with numerous paralogous versions of the factor present in bacteria, suggesting subfunctionalization of different EF-G variants. [25]

Elongation factors exist in all three domains of life with similar function on the ribosome. The eukaryotic and archeal homologs of EF-G are eEF2 and aEF2, respectively. In bacteria (and some archaea), the fusA gene that encodes EF-G is found within the conserved str gene with the sequence 5′ - rpsL - rpsG - fusA - tufA - 3′. [2] However, two other major forms of EF-G exist in some species of Spirochaetota, Planctomycetota, and δ-Proteobacteria (which has since been split and renamed Bdellovibrionota, Myxococcota, and Thermodesulfobacteriota), which form the spd group of bacteria that have elongation factors spdEFG1 and spdEFG2. [25] [26]

From spdEFG1 and spdEFG2 evolved the mitochondrial elongation factors mtEFG1 (GFM1) and mtEFG2 (GFM2), respectively. [25] [26] The two roles of EF-G in elongation and termination of protein translation are split amongst the mitochondrial elongation factors, with mtEFG1 responsible for translocation and mtEFG2 responsible for termination and ribosomal recycling with mitochondrial RRF.

See also

Related Research Articles

GTPases are a large family of hydrolase enzymes that bind to the nucleotide guanosine triphosphate (GTP) and hydrolyze it to guanosine diphosphate (GDP). The GTP binding and hydrolysis takes place in the highly conserved P-loop "G domain", a protein domain common to many GTPases.

<span class="mw-page-title-main">Translation (biology)</span> Cellular process of protein synthesis

In biology, translation is the process in living cells in which proteins are produced using RNA molecules as templates. The generated protein is a sequence of amino acids. This sequence is determined by the sequence of nucleotides in the RNA. The nucleotides are considered three at a time. Each such triple results in addition of one specific amino acid to the protein being generated. The matching from nucleotide triple to amino acid is called the genetic code. The translation is performed by a large complex of functional RNA and proteins called ribosomes. The entire process is called gene expression.

<span class="mw-page-title-main">Fusidic acid</span> Antibiotic

Fusidic acid, sold under the brand names Fucidin among others, is a steroid antibiotic that is often used topically in creams or ointments and eyedrops but may also be given systemically as tablets or injections.
As of October 2008, the global problem of advancing antimicrobial resistance has led to a renewed interest in its use.

Bacterial translation is the process by which messenger RNA is translated into proteins in bacteria.

Eukaryotic translation is the biological process by which messenger RNA is translated into proteins in eukaryotes. It consists of four phases: initiation, elongation, termination, and recapping.

Initiation factors are proteins that bind to the small subunit of the ribosome during the initiation of translation, a part of protein biosynthesis.

A release factor is a protein that allows for the termination of translation by recognizing the termination codon or stop codon in an mRNA sequence. They are named so because they release new peptides from the ribosome.

<span class="mw-page-title-main">EF-Tu</span> Prokaryotic elongation factor

EF-Tu is a prokaryotic elongation factor responsible for catalyzing the binding of an aminoacyl-tRNA (aa-tRNA) to the ribosome. It is a G-protein, and facilitates the selection and binding of an aa-tRNA to the A-site of the ribosome. As a reflection of its crucial role in translation, EF-Tu is one of the most abundant and highly conserved proteins in prokaryotes. It is found in eukaryotic mitochondria as TUFM.

Eukaryotic initiation factors (eIFs) are proteins or protein complexes involved in the initiation phase of eukaryotic translation. These proteins help stabilize the formation of ribosomal preinitiation complexes around the start codon and are an important input for post-transcription gene regulation. Several initiation factors form a complex with the small 40S ribosomal subunit and Met-tRNAiMet called the 43S preinitiation complex. Additional factors of the eIF4F complex recruit the 43S PIC to the five-prime cap structure of the mRNA, from which the 43S particle scans 5'-->3' along the mRNA to reach an AUG start codon. Recognition of the start codon by the Met-tRNAiMet promotes gated phosphate and eIF1 release to form the 48S preinitiation complex, followed by large 60S ribosomal subunit recruitment to form the 80S ribosome. There exist many more eukaryotic initiation factors than prokaryotic initiation factors, reflecting the greater biological complexity of eukaryotic translation. There are at least twelve eukaryotic initiation factors, composed of many more polypeptides, and these are described below.

A bacterial initiation factor (IF) is a protein that stabilizes the initiation complex for polypeptide translation.

<span class="mw-page-title-main">Eukaryotic translation termination factor 1</span> Protein-coding gene in the species Homo sapiens

Eukaryotic translation termination factor1 (eRF1), also referred to as TB3-1 or SUP45L1, is a protein that is encoded by the ERF1 gene. In Eukaryotes, eRF1 is an essential protein involved in stop codon recognition in translation, termination of translation, and nonsense mediated mRNA decay via the SURF complex.

Elongation factor 4 (EF-4) is an elongation factor that is thought to back-translocate on the ribosome during the translation of RNA to proteins. It is found near-universally in bacteria and in eukaryotic endosymbiotic organelles including the mitochondria and the plastid. Responsible for proofreading during protein synthesis, EF-4 is a recent addition to the nomenclature of bacterial elongation factors.

Protein-synthesizing GTPases are enzymes involved in mRNA translation into protein by the ribosome, with systematic name GTP phosphohydrolase (mRNA-translation-assisting). They usually include translation initiation factors such as IF-2 and translation elongation factors such as EF-Tu.

<span class="mw-page-title-main">Protein synthesis inhibitor</span> Inhibitors of translation

A protein synthesis inhibitor is a compound that stops or slows the growth or proliferation of cells by disrupting the processes that lead directly to the generation of new proteins.

Eukaryotic Initiation Factor 2 (eIF2) is an eukaryotic initiation factor. It is required for most forms of eukaryotic translation initiation. eIF2 mediates the binding of tRNAiMet to the ribosome in a GTP-dependent manner. eIF2 is a heterotrimer consisting of an alpha, a beta, and a gamma subunit.

EF-Ts is one of the prokaryotic elongation factors. It is found in human mitochondria as TSFM. It is similar to eukaryotic EF-1B.

The P-site is the second binding site for tRNA in the ribosome. The other two sites are the A-site (aminoacyl), which is the first binding site in the ribosome, and the E-site (exit), the third. During protein translation, the P-site holds the tRNA which is linked to the growing polypeptide chain. When a stop codon is reached, the peptidyl-tRNA bond of the tRNA located in the P-site is cleaved releasing the newly synthesized protein. During the translocation step of the elongation phase, the mRNA is advanced by one codon, coupled to movement of the tRNAs from the ribosomal A to P and P to E sites, catalyzed by elongation factor EF-G.

<span class="mw-page-title-main">Elongation factor P</span>

EF-P is an essential protein that in bacteria stimulates the formation of the first peptide bonds in protein synthesis. Studies show that EF-P prevents ribosomes from stalling during the synthesis of proteins containing consecutive prolines. EF-P binds to a site located between the binding site for the peptidyl tRNA and the exiting tRNA. It spans both ribosomal subunits with its amino-terminal domain positioned adjacent to the aminoacyl acceptor stem and its carboxyl-terminal domain positioned next to the anticodon stem-loop of the P site-bound initiator tRNA. The EF-P protein shape and size is very similar to a tRNA and interacts with the ribosome via the exit “E” site on the 30S subunit and the peptidyl-transferase center (PTC) of the 50S subunit. EF-P is a translation aspect of an unknown function, therefore It probably functions indirectly by altering the affinity of the ribosome for aminoacyl-tRNA, thus increasing their reactivity as acceptors for peptidyl transferase.

In molecular biology, VAR1 protein domain, otherwise known as variant protein 1, is a ribosomal protein that forms part of the small ribosomal subunit in yeast mitochondria. Mitochondria possess their own ribosomes responsible for the synthesis of a small number of proteins encoded by the mitochondrial genome. VAR1 is the only protein in the yeast mitochondrial ribosome to be encoded in the mitochondria - the remaining approximately 80 ribosomal proteins are encoded in the nucleus. VAR1 along with 15S rRNA are necessary for the formation of mature 37S subunits.

Ribosomal L28e protein family is a family of evolutionarily related proteins. Members include 60S ribosomal protein L28.

References

  1. 1 2 3 4 Shoji, S; Walker, SE; Fredrick, K (2009). "Ribosomal translocation: one step closer to the molecular mechanism". ACS Chem Biol. 4 (2): 93–107. doi:10.1021/cb8002946. PMC   3010847 . PMID   19173642.
  2. 1 2 Post, L. E.; Nomura, M. (1980-05-25). "DNA sequences from the str operon of Escherichia coli". The Journal of Biological Chemistry. 255 (10): 4660–4666. doi: 10.1016/S0021-9258(19)85545-X . ISSN   0021-9258. PMID   6989816.
  3. ↑ Liu, Kaixian; Rehfus, Joseph E.; Mattson, Elliot; Kaiser, Christian M. (2017-07-01). "The ribosome destabilizes native and non-native structures in a nascent multidomain protein". Protein Science. 26 (7): 1439–1451. doi:10.1002/pro.3189. ISSN   1469-896X. PMC   5477528 . PMID   28474852.
  4. 1 2 Carlson, Markus A.; Haddad, Bassam G.; Weis, Amanda J.; Blackwood, Colby S.; Shelton, Catherine D.; Wuerth, Michelle E.; Walter, Justin D.; Spiegel, Paul Clint (2017-06-01). "Ribosomal protein L7/L12 is required for GTPase translation factors EF-G, RF3, and IF2 to bind in their GTP state to 70S ribosomes". The FEBS Journal. 284 (11): 1631–1643. doi:10.1111/febs.14067. ISSN   1742-4658. PMC   5568246 . PMID   28342293.
  5. ↑ Salsi, Enea; Farah, Elie; Dann, Jillian; Ermolenko, Dmitri N. (2014). "Following movement of domain IV of elongation factor G during ribosomal translocation". Proceedings of the National Academy of Sciences. 111 (42): 15060–15065. Bibcode:2014PNAS..11115060S. doi: 10.1073/pnas.1410873111 . PMC   4210333 . PMID   25288752.
  6. ↑ Lin, Jinzhong; Gagnon, Matthieu G.; Bulkley, David; Steitz, Thomas A. (2015). "Conformational Changes of Elongation Factor G on the Ribosome during tRNA Translocation". Cell. 160 (1–2): 219–227. doi:10.1016/j.cell.2014.11.049. PMC   4297320 . PMID   25594181.
  7. ↑ Li, Wen; Trabuco, Leonardo G.; Schulten, Klaus; Frank, Joachim (2011-05-01). "Molecular dynamics of EF-G during translocation". Proteins: Structure, Function, and Bioinformatics. 79 (5): 1478–1486. doi:10.1002/prot.22976. ISSN   1097-0134. PMC   3132869 . PMID   21365677.
  8. ↑ Zhang, Dejiu; Yan, Kaige; Zhang, Yiwei; Liu, Guangqiao; Cao, Xintao; Song, Guangtao; Xie, Qiang; Gao, Ning; Qin, Yan (2015). "New insights into the enzymatic role of EF-G in ribosome recycling". Nucleic Acids Research. 43 (21): 10525–33. doi:10.1093/nar/gkv995. PMC   4666400 . PMID   26432831.
  9. ↑ Nyborg, J.; Nissen, P.; Kjeldgaard, M.; Thirup, S.; Polekhina, G.; Clark, B. F. (March 1996). "Structure of the ternary complex of EF-Tu: macromolecular mimicry in translation". Trends in Biochemical Sciences. 21 (3): 81–82. doi:10.1016/S0968-0004(96)30008-X. ISSN   0968-0004. PMID   8882578.
  10. ↑ Mandava, C. S.; Peisker, K.; Ederth, J.; Kumar, R.; Ge, X.; Szaflarski, W.; Sanyal, S. (2011-11-18). "Bacterial ribosome requires multiple L12 dimers for efficient initiation and elongation of protein synthesis involving IF2 and EF-G". Nucleic Acids Research. 40 (5): 2054–2064. doi:10.1093/nar/gkr1031. ISSN   0305-1048. PMC   3299993 . PMID   22102582.
  11. ↑ Maklan, E. J. (2012). Genetic and Biochemical Analysis of the GTPase Associated Center of the Ribosome. UC Santa Cruz. Merritt ID: ark:/13030/m5js9t4d. Retrieved from https://escholarship.org/uc/item/7gh9v43h
  12. ↑ Shi, Xinying; Khade, Prashant K.; Sanbonmatsu, Karissa Y.; Joseph, Simpson (2012). "Functional Role of the Sarcin–Ricin Loop of the 23S rRNA in the Elongation Cycle of Protein Synthesis". Journal of Molecular Biology. 419 (3–4): 125–138. doi:10.1016/j.jmb.2012.03.016. PMC   3348345 . PMID   22459262.
  13. 1 2 Choi, Junhong; Puglisi, Joseph D. (2017). "Three tRNAs on the ribosome slow translation elongation". Proceedings of the National Academy of Sciences. 114 (52): 13691–13696. doi: 10.1073/pnas.1719592115 . PMC   5748233 . PMID   29229848.
  14. ↑ Guo, Z.; Noller, H. F. (2012). "Rotation of the head of the 30S ribosomal subunit during mRNA translocation". Proceedings of the National Academy of Sciences. 109 (50): 20391–20394. Bibcode:2012PNAS..10920391G. doi: 10.1073/pnas.1218999109 . PMC   3528506 . PMID   23188795.
  15. ↑ da Cunha, CE; Belardinelli, R; Peske, F; Holtkamp, W; Wintermeyer, W; Rodnina, MV (2013). "Dual use of GTP hydrolysis by elongation factor G on the ribosome". Translation. 1 (1): e24315. doi:10.4161/trla.24315. PMC   4718068 . PMID   26824016.
  16. 1 2 Das, Debasis; Samanta, Dibyendu; Bhattacharya, Arpita; Basu, Arunima; Das, Anindita; Ghosh, Jaydip; Chakrabarti, Abhijit; Gupta, Chanchal Das (2017-01-18). "A Possible Role of the Full-Length Nascent Protein in Post-Translational Ribosome Recycling". PLOS ONE. 12 (1): e0170333. Bibcode:2017PLoSO..1270333D. doi: 10.1371/journal.pone.0170333 . ISSN   1932-6203. PMC   5242463 . PMID   28099529.
  17. ↑ Zavialov AV, Hauryliuk VV, Ehrenberg M (2005). "Splitting of the posttermination ribosome into subunits by the concerted action of RRF and EF-G". Molecular Cell. 18 (6): 675–686. doi: 10.1016/j.molcel.2005.05.016 . PMID   15949442.
  18. ↑ Hirokawa, Go; Nijman, Romana M.; Raj, V. Samuel; Kaji, Hideko; Igarashi, Kazuei; Kaji, Akira (2005-08-01). "The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits". RNA. 11 (8): 1317–1328. doi:10.1261/rna.2520405. ISSN   1355-8382. PMC   1370814 . PMID   16043510.
  19. 1 2 Walter, Justin D.; Hunter, Margaret; Cobb, Melanie; Traeger, Geoff; Spiegel, P. Clint (2012-01-01). "Thiostrepton inhibits stable 70S ribosome binding and ribosome-dependent GTPase activation of elongation factor G and elongation factor 4". Nucleic Acids Research. 40 (1): 360–370. doi:10.1093/nar/gkr623. ISSN   0305-1048. PMC   3245911 . PMID   21908407.
  20. 1 2 Bulkley, David; Brandi, Letizia; Polikanov, Yury S.; Fabbretti, Attilio; O’Connor, Michael; Gualerzi, Claudio O.; Steitz, Thomas A. (2014). "The Antibiotics Dityromycin and GE82832 Bind Protein S12 and Block EF-G-Catalyzed Translocation". Cell Reports. 6 (2): 357–365. doi:10.1016/j.celrep.2013.12.024. PMC   5331365 . PMID   24412368.
  21. 1 2 Belardinelli, Riccardo; Rodnina, Marina V. (2017-09-05). "Effect of Fusidic Acid on the Kinetics of Molecular Motions During EF-G-Induced Translocation on the Ribosome". Scientific Reports. 7 (1): 10536. Bibcode:2017NatSR...710536B. doi:10.1038/s41598-017-10916-8. ISSN   2045-2322. PMC   5585275 . PMID   28874811.
  22. ↑ Koripella, Ravi Kiran; Chen, Yang; Peisker, Kristin; Koh, Cha San; Selmer, Maria; Sanyal, Suparna (2012). "Mechanism of Elongation Factor-G-mediated Fusidic Acid Resistance and Fitness Compensation inStaphylococcus aureus". Journal of Biological Chemistry. 287 (36): 30257–30267. doi: 10.1074/jbc.m112.378521 . PMC   3436278 . PMID   22767604.
  23. ↑ Macvanin M, Hughes D (June 2005). "Hyper-susceptibility of a fusidic acid-resistant mutant of Salmonella to different classes of antibiotics". FEMS Microbiology Letters. 247 (2): 215–20. doi: 10.1016/j.femsle.2005.05.007 . PMID   15935566.
  24. ↑ Macvanin M, Johanson U, Ehrenberg M, Hughes D (July 2000). "Fusidic acid-resistant EF-G perturbs the accumulation of ppGpp". Molecular Microbiology. 37 (1): 98–107. doi: 10.1046/j.1365-2958.2000.01967.x . PMID   10931308. S2CID   10307058.
  25. 1 2 3 G C Atkinson; S L Baldauf (2011). "Evolution of elongation factor G and the origins of mitochondrial and chloroplast forms". Molecular Biology and Evolution. 28 (3): 1281–92. doi: 10.1093/molbev/msq316 . PMID   21097998.
  26. 1 2 Margus, Tõnu; Remm, Maido; Tenson, Tanel (2011-08-04). "A Computational Study of Elongation Factor G (EFG) Duplicated Genes: Diverged Nature Underlying the Innovation on the Same Structural Template". PLOS ONE. 6 (8): e22789. Bibcode:2011PLoSO...622789M. doi: 10.1371/journal.pone.0022789 . ISSN   1932-6203. PMC   3150367 . PMID   21829651.

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