Phylogenetic Relationships Among Group II Intron ORFs

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2001 Feb 27

PMID 11222775

Citations 97

Authors

S Zimmerly

G Hausner

Wu Xc

Affiliations

Soon will be listed here.

Abstract

Group II introns are widely believed to have been ancestors of spliceosomal introns, yet little is known about their own evolutionary history. In order to address the evolution of mobile group II introns, we have compiled 71 open reading frames (ORFs) related to group II intron reverse transcriptases and subjected their derived amino acid sequences to phylogenetic analysis. The phylogenetic tree was rooted with reverse transcriptases (RTs) of non-long terminal repeat retroelements, and the inferred phylogeny reveals two major clusters which we term the mitochondrial and chloroplast-like lineages. Bacterial ORFs are mainly positioned at the bases of the two lineages but with weak bootstrap support. The data give an overview of an apparently high degree of horizontal transfer of group II intron ORFs, mostly among related organisms but also between organelles and bacteria. The Zn domain (nuclease) and YADD motif (RT active site) were lost multiple times during evolution. Differences in domain structures suggest that the oldest ORFs were concise, while the ORF in the mitochondrial lineage subsequently expanded in three locations. The data are consistent with a bacterial origin for mobile group II introns.

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References

Romine M, Stillwell L, Wong K, Thurston S, Sisk E, Sensen C . Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol. 1999; 181(5):1585-602. PMC: 93550. DOI: 10.1128/JB.181.5.1585-1602.1999. View

Malik H, BURKE W, Eickbush T . The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol. 1999; 16(6):793-805. DOI: 10.1093/oxfordjournals.molbev.a026164. View

Huang C, Narita M, Yamagata T, Itoh Y, Endo G . Structure analysis of a class II transposon encoding the mercury resistance of the Gram-positive Bacterium bacillus megaterium MB1, a strain isolated from minamata bay, Japan. Gene. 1999; 234(2):361-9. DOI: 10.1016/s0378-1119(99)00184-5. View

Saldanha R, Chen B, Wank H, Matsuura M, Edwards J, Lambowitz A . RNA and protein catalysis in group II intron splicing and mobility reactions using purified components. Biochemistry. 1999; 38(28):9069-83. DOI: 10.1021/bi982799l. View

Schafer B, Wolf K . A novel group-II intron in the cox1 gene of the fission yeast Schizosaccharomyces pombe is inserted in the same codon as the mobile group-II intron aI2 in the Saccharomyces cerevisiae cox1 homologue. Curr Genet. 1999; 35(6):602-8. DOI: 10.1007/s002940050458. View

Vogel J, Borner T, Hess W . Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants. Nucleic Acids Res. 1999; 27(19):3866-74. PMC: 148650. DOI: 10.1093/nar/27.19.3866. View

Burger G, Gray M, Lang B . Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell. 1999; 11(9):1675-94. PMC: 144311. DOI: 10.1105/tpc.11.9.1675. View

Wank H, Sanfilippo J, Singh R, Matsuura M, Lambowitz A . A reverse transcriptase/maturase promotes splicing by binding at its own coding segment in a group II intron RNA. Mol Cell. 1999; 4(2):239-50. DOI: 10.1016/s1097-2765(00)80371-8. View

Qiu Y, Lee J, Soltis D, Soltis P, Zanis M, ZIMMER E . The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature. 1999; 402(6760):404-7. DOI: 10.1038/46536. View

10.

Mohr G, Smith D, Belfort M, Lambowitz A . Rules for DNA target-site recognition by a lactococcal group II intron enable retargeting of the intron to specific DNA sequences. Genes Dev. 2000; 14(5):559-73. PMC: 316424. View

11.

Martinez-Abarca F, Toro N . Homing of a bacterial group II intron with an intron-encoded protein lacking a recognizable endonuclease domain. Mol Microbiol. 2000; 35(6):1405-12. DOI: 10.1046/j.1365-2958.2000.01804.x. View

12.

Guo H, Karberg M, Long M, Jones 3rd J, Sullenger B, Lambowitz A . Group II introns designed to insert into therapeutically relevant DNA target sites in human cells. Science. 2000; 289(5478):452-7. DOI: 10.1126/science.289.5478.452. View

13.

Martinez-Abarca F, Toro N . RecA-independent ectopic transposition in vivo of a bacterial group II intron. Nucleic Acids Res. 2000; 28(21):4397-402. PMC: 113133. DOI: 10.1093/nar/28.21.4397. View

14.

Baldauf S, Roger A, Doolittle W . A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000; 290(5493):972-7. DOI: 10.1126/science.290.5493.972. View

15.

Kohlstaedt L, Wang J, Friedman J, Rice P, Steitz T . Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science. 1992; 256(5065):1783-90. DOI: 10.1126/science.1377403. View

16.

Hardy C, Clark-Walker G . Nucleotide sequence of the COX1 gene in Kluyveromyces lactis mitochondrial DNA: evidence for recent horizontal transfer of a group II intron. Curr Genet. 1991; 20(1-2):99-114. DOI: 10.1007/BF00312772. View

17.

Xiong Y, Eickbush T . Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990; 9(10):3353-62. PMC: 552073. DOI: 10.1002/j.1460-2075.1990.tb07536.x. View

18.

Hilu K, Liang H . The matK gene: sequence variation and application in plant systematics. Am J Bot. 2011; 84(6):830. View

19.

Altschul S, Gish W, Miller W, Myers E, Lipman D . Basic local alignment search tool. J Mol Biol. 1990; 215(3):403-10. DOI: 10.1016/S0022-2836(05)80360-2. View

20.

Kuck U . The intron of a plastid gene from a green alga contains an open reading frame for a reverse transcriptase-like enzyme. Mol Gen Genet. 1989; 218(2):257-65. DOI: 10.1007/BF00331276. View