Structural, genomic, and phylogenetic analysis of Lian, a novel family of non-LTR retrotransposons in the yellow fever mosquito, Aedes aegypti

Molecular Biology and Evolution

Volumn 15, Issue 7, 1998, Pages 837-853

  Tu, Zhijian ^a   Isoe, Jun ^a   Guzova, Julia A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Aedes aegypti; Evolution; Genome; Repeats; Retrotransposon; Reverse transcriptase

Indexed keywords

AEDES AEGYPTI; AMINO ACID SEQUENCE; ARTICLE; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RETROPOSON; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

AEDES AEGYPTI; ARACHNIDA; HEXAPODA; INSECTA; LIA;

EID: 0031827506     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.molbev.a025989     Document Type: Article

References (106)

1. ABAD, P., C. VAURY, A. PELISSON, M. C. CHABOISSIER, I. BUSSEAU, and A. BUCHETON. 1989. A long interspersed repetitive element-the I factor of Drosophila teissieri - is able to transpose in different Drosophila species. Proc. Natl. Acad. Sci. USA 86:8887-8891.
2. AGARWAL, M. L., N. BENSAADI, J. C. SALVADO, K. CAMPBELL, and C. MOUCHES. 1993. Characterization and genetic organization of full-length copies of a LINE retroposon family dispersed in the genome of Culex pipiens mosquitoes. Insect Biochem. Mol. Biol. 23:621-629.
3. AKSOY, S., S. WILLIAMS, S. CHANG, and F. F. RICHARDS. 1990. SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res. 18:785-792.
4. ALTSCHUL, S. F., W. GISH, W. MILLER, E. W. MYERS, and D. J. LIPMAN. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. ARKHIPOVA, I. R., N. V. LYUBOMIRSKAYA, and Y. V. ILYIN. 1995. Drosophila retrotransposons. Springer-Verlag, New York.
6. BECERRA, S. P., G. M. CLORE, A. M. GRONENBORN, A. R. KARLSTROM, S. J. STAHL, S. H. WILSON, and P. T. WINGFIELD. 1990. Purification and characterization of the RNase H domain of HIV-1 reverse transcriptase expressed in recombinant Escherichia coli. FEBS Lett. 270:76-80.
7. BENSAADI-MERCHERMEK, N., J. C. SALVADO, and C. MOUCHES. 1994. Mosquito transposable elements. Genetica 93: 139-148.
8. BERG, D. E., and M. M. HOWE. 1989. Mobile DNA. American Society for Microbiology, Washington, D.C.
9. BESANSKY, N. J. 1990. A retrotransposable element from the mosquito Anopheles gambiae. Mol. Cell. Biol. 10:863-871.
10. BESANSKY, N. J., J. A. BEDELL, and O. MUKABAYIRE. 1994. Q: a new retrotransposon from the mosquito Anopheles gambiae. Insect Mol. Biol. 3:49-56.
11. BESANSKY, N. J., O. MUKABAYIRE, J. A. BEDELL, and H. LUSZ. 1996. Pegasus, a small terminal inverted repeat transposable element found in the white gene of Anopheles gambiae. Genetica 98:119-129.
12. BESANSKY, N. J., S. M. PASKEWITZ, D. M. HAMM, and F. H. COLLINS. 1992. Distinct families of site-specific retrotransposons occupy identical positions in the rRNA genes of Anopheles gambiae. Mol. Cell. Biol. 12:5102-5110.
13. BLINOV, A. G., Y. V. SOBANOV, S. S. BOGACHEV, A. P. DONCHENKO, and M. A. FILIPPOVA. 1993. The Chironomus thummi genome contains a non-LTR retrotransposon. Mol. Gen. Genet. 237:412-420.
14. BLINOV, A. G., Y. V. SOBANOV, S. V. SCHERBIK, and K. G. AIMANOVA. 1997. The Chironomus (Camptochironomus) tentans genome contains two non-LTR retrotransposons. Genome 40:143-150.
15. BROOKFIELD, J. F. Y. 1995. Transposable element as selfish DNA. Pp. 130-153 in D. J. SHERRATT, ed. Mobile genetic elements. Oxford University Press, Oxford.
16. BRITTEN, R. J. 1996. DNA sequence insertion and evolutionary variation in gene regulation. Proc. Natl. Acad. Sci. USA 93: 9374-9377.
17. BURCH, J. B. E., D. L. DAVIS, and N. B. HAAS. 1993. Chicken repeat 1 elements contain a pol-like open reading frame and belong to the non-long terminal repeat class of retrotransposons. Proc. Natl. Acad. Sci. USA 90:8199-8203.
18. BURKE, W. D., C. C. CALALANG, and T. H. EICKBUSH. 1987. The site-specific ribosomal insertion element type II of Bombyx mon (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol. Cell. Biol. 7:2221-2230.
19. BUSSEAU, I., M.-C. CHABOISSIER, A. PELISSON, and A. BUCKETON. 1994. I factors in Drosophila melanogaster: transposition under control. Genetica 93:101-116.
20. CAMBARERI, E. B., J. HELBER, and J. A. KINSEY. 1994. Tad1, an active LINE-like element of Neurospora crassa. Mol. Gen. Genet. 242:658-665.
21. CHARLESWORTH, B., and C. H. LANGLEY. 1989. The population genetics of Drosophila transposable elements. Annu. Rev. Genet. 23:251-287.
22. CHIU, I. M., A. YANIV, J. E. DAHLBERG, A. GAZIT, S. F. SKUNTZ, S. R. TRONICK, and S. A. AARONSON. 1985. Nucleotide sequence evidence for relationship of AIDS retrovirus to lentiviruses. Nature 317:366-368.
23. CRAIGIE, R. 1992. Hotspots and warm spots: integration specificity of retroelements. Trends Genet. 8:187-190.
24. DI NOCERA, P. P., and G. CASARI. 1987. Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences. Proc. Natl. Acad. Sci. USA 84:5843-5847.
25. DOOLITTLE, W. F., and C. SAPIENZA. 1980. Selfish genes, the phenotype paradigm and genome evolution. Science 284: 601-603.
26. DREW, A. C., and P. J. BRINDLEY. 1997. A retrotransposon of the non-long terminal repeat class from the human blood fluke Schistosoma mansoni. Similarities to the chicken-repeap-1-like elements of vertebrates. Mol. Biol. Evol. 14: 602-610.
27. EICKBUSH, T. H. 1992. Transposing without ends: the non-LTR retrotransposable elements. New Biol. 4:430-440.
28. _. 1994. Origin and evolutionary relationships of retroelements. Pp. 121-157 in S. S. MORSE, ed. The evolutionary biology of viruses. Raven Press, New York.
29. _. 1997. Telomerase and retrotransposons: which came first? Science 277:911-912.
30. FAWCETT, D. H., C. K. LISTER, E. KELLETT, and D. J. FINNEGAN. 1986. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47:1007-1015.
31. FELSENSTEIN, J., and H. KISHINO. 1993. Is there something wrong with the bootstrap on phytogenies? A reply to Hillis and Bull. Syst. Biol. 42:193-200.
32. FENG, Q., J. V. MORAN, H. H. KAZAZIAN JR., and J. D. BOEKE. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905-916.
33. FINNEGAN, D. J. 1992. Transposable elements. Curr. Opin. Genet. Dev. 2:861-867.
34. GABRIEL, A., T. J. YEN, D. C. SCHWARTZ, C. L. SMITH, J. D. BOEKE, B. SOLLNER-WEBB, and D. W. CLEVELAND. 1990. A rapidly rearranging retrotransposon within the miniexon gene locus of Crithidia fasciculata. Mol. Cell. Biol. 10: 615-624.
35. GARRETT, J. E., D. S. KNUTZON, and D. CARROLL. 1989. Composite transposable elements in the Xenopus laevis genome. Mol. Cell. Biol. 9:3018-3027.
36. GRIBSKOV, M., and R. BURGESS. 1986. Sigma factors from E. coli, B. subtilis, phage SP01, and phage T4 are homologous proteins. Nucleic Acids Res. 14:6745-6763.
37. HAAS, N. B., J. M. GRABOWSKI, A. B. SIVITZ, and J. B. E. BURCH. 1997. Chicken repeat 1 (CR1) elements, which define an ancient family of vertebrate non-LTR retrotransposons, contain two closely spaced open reading frames. Gene 197:305-309.
38. HAGEDORN, H. H., D. R. MADDISON, and Z. TU. 1998. Evolution of vitellogenins, cyclorrhaphan yolk proteins, and other related molecules. Adv. Insect Physiol. 27:235-284.
39. HARTL, D. L., E. R. LOZOVSKAYA, D. I. NURMINSKY, and A. R. LOHE. 1997. What restricts the activity of mariner-like transposable elements? Trends Genet. 13:197-201.
40. HATTORI, M., S. KUHARA, O. TAKENAKA, and Y. SAKAKI. 1986. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein. Nature 321:625-628.
41. HE, C., J. P. NOURSE, S. KELEMU, J. A. G. IRWIN, and J. M. MANNERS. 1996. CgT1: a non-LTR retrotransposon with restricted distribution in the fungal phytopathogen Colletotrichum gloeosporioides. Mol. Gen. Genet. 252:320-331.
42. HUGHES, M. A., A. M. WARREN, and J. M. CRAMPTON. 1996. JAM1: a novel LINE transposable element in the genome of the medically important mosquito, Aedes aegypti. P. 276 in Proceedings of the XXth International Congress of Entomology, Florence, Italy.
43. HUTCHISON, C. A., S. C. HARIES, D. D. LOEB, W. R. SHEHEE, and M. H. EDGELL. 1989. LINEs and related retroposons: long interspersed repeated sequences in the eucaryotic genome. Pp. 593-617 in D. E. BERG and M. M. HOME, eds. Mobile DNA. American Society for Microbiology, Washington, D.C.
44. ITAYA, M., and K. KONDO. 1991. Molecular cloning of a ribonuclease H (RNase HI) gene from an extreme thermophile Thermus thermophilus HB8: a thermostable RNase H can functionally replace the Escherichia coli enzyme in vivo. Nucleic Acids Res. 19:4443-4449.
45. ITAYA, M., D. MCKELVIN, S. K. CHATTERJIE, and R. J. CROUCH. 1991. Selective cloning of genes encoding RNase H from Salmonella typhimurium, Saccharomyces cerevisiae and Escherichia coli rnh mutant. Mol. Gen. Genet. 227: 438-445.
46. JAKUBCZAK, J. L., Y. XIONG, and T. H. EICKBUSH. 1990. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J. Mol. Biol. 212:37-52.
47. JI, H., D. P. MOORE, M. A. BLOMBERG, L.T. BRAITERMAN, D. F. VOYTAS, G. NATSOULIS, and J. D. BOEKE. 1993. Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell 73: 1007-1018.
48. KAJIKAWA, M., K. OHSHIMA, and N. OKADA. 1997. Determination of the entire sequence of turtle CR1: the first open reading frame of the turtle CR1 element encodes a protein with a novel zinc finger motif. Mol. Biol. Evol. 14:1206-1217.
49. KANAYA, S., and R. J. CROUCH. 1983. DNA sequence of the gene coding for Escherichia coli ribonuclease H. J. Biol. Chem. 258:1276-1281.
50. KANAYA, S., A. KOHARA, Y. MIURA, A. SEKIGUCHI, S. IWAI, H. INOUE, E. OHTSUKA, and M. IKEHARA. 1990. Identincation of the amino acid residues involved in an active site of Escherichia coli ribonuclease H by site-directed mutagenesis. J. Biol. Chem. 265:4615-4621.
51. KE, Z., G. L. GROSSMAN, A. J. CORNEL, and F. H. COLLINS. 1996. Quetzal: a transposon of the Tc1 family in the mosquito Anopheles albimanus. Genetica 98:141-147.
52. KIDWELL, M. G., and D. LISCH. 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94:7704-7711.
53. KNIGHT, M., A. MILLER, N. RAGHAVAN, C. RICHARDS, and F. LEWIS. 1992. Identification of a repetitive element in the snail Biomphalaria glabrata: relationship to the reverse transcriptase-encoding sequence in LINE-1 transposons. Gene 118:181-187.
54. KOELLE, M. R., W. A. SEGRAVES, and D. S. HOGNESS. 1992. DHR3: a Drosophila steroid receptor homolog. Proc. Natl. Acad. Sci. USA 89:6167-6171.
55. LEVIN, H. L. 1997. It's prime time for reverse transcriptase. Cell 88:5-8.
56. LEVIS, R. W., R. GANESAN, K. HOUTCHENS, L. A. TOLAR, and F. M. SHEEN. 1993. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75:1083-1093.
57. LIN, Y., M. T. HAMBLIN, M. J. EDWARDS, C. BARILLAS-MURY, M. R. KANOST, D. G. KNIPPLE, M. F WOLFNER, and H. H. HAGEDORN. 1993. Structure, expression, and hormonal control of genes from the mosquito, Aedes aegypti, which encode proteins similar to the vitelline membrane proteins of Drosophila melanogaster. Dev. Biol. 155:558-568.
58. LUAN, D. D., M. H. KORMAN, J. L. JAKUBCZAK, and T. H. EICKBUSH. 1993. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595-605.
59. MCCLURE, M. A. 1991. Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol. Biol. Evol. 8: 835-856.
60. _. 1992. Sequence analysis of eukaryotic retroid proteins. Math. Comput. Modelling 16:121-136.
61. _. 1993. Evolutionary history of reverse transcriptase. Pp 425-444 in A. M. SKALKA and S. GOFF, eds. Reverse transcriptase. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
62. MCDONALD, J. F. 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Dev. 3:855-864.
63. _. 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10:123-126.
64. MARTIN, S. L. 1995. Characterization of a LINE-1 cDNA that originated from RNA present in ribonucleoprotein particles: implications for the structure of an active mouse LINE-1. Gene 153:261-266.
65. MASON, J. M., and H. BIESSMANN. 1995. The unusual telomeres of Drosophila. Trends Genet. 11:58-62.
66. MEINKOTH, J., and G. WAHL. 1984. Hybridization of nucleic acids immobilized on solid supports. Anal. Biochem. 138: 267-284.
67. MIZRAHI, V., P. HUBERTS, S. S. DAWES, and L. R. DUDDING. 1993. A PCR method for the sequence analysis of the gyrA, polA and rnhA gene segments from mycobacteria. Gene 136:287-290.
68. MOUCHES, C., N. BENSAADI, and J. C. SALVADO. 1992. Characterization of a LINE retroposon dispersed in the genome of three non sibling Aedes mosquito species. Gene 120:183-190.
69. MUKABAYIRE, O., and N. J. BESANSKY. 1996. Distribution of T1, Q, Pegasus and mariner transposable elements on the polytene chromosomes of PEST, a standard strain of Anopheles gambiae. Chromosoma 104:585-595.
70. MURPHY, N. B., A. PAYS, P. TEBABI, H. COQUELET, M. GUYAUX, M. STEINERT, and E. PAYS. 1987. Trypanosoma brucei repeated element with unusual structural and transcriptional properties. J. Mol. Biol. 195:855-871.
71. NAKAMURA, T. M., G. B. MORIN, K. B. CHAPMAN, S. L. WEINRICH, W. H. ANDREWS, J. LINGNER, C. B. HARLEY, and T. R. CECH. 1997. Telomerase catalytic subunit homologs from fission yeast and human. Science 277:955-959.
72. O'HARE, K., M. R. ALLEY, T. E. CULLINGFORD, A. DRIVER, and M. J. SANDERSON. 1991. DNA sequence of the Doc retroposon in the white-one mutant of Drosophila melanogaster and of secondary insertions in the phenotypically altered derivatives white-honey and white-eosin. Mol. Gen. Genet. 225:17-24.
73. OKAZAKI, S., H. ISHIKAWA, and H. FUJIWARA. 1995. Structural analysis of Tras1, a novel family of telomeric repeat-associated retrotransposons in the silkworm, Bombyx mori. Mol. Cell. Biol. 15:4545-4552.
74. ORGEL, L. E., and F. H. CRICK. 1980. Selfish DNA: the ultimate parasite. Nature 284:604-607.
75. PARDUE, M. L., O. N. DANILEVSKAYA, K. LOWENHAUPT, F. SLOT, and K. L. TRAVERSE. 1996. Drosophila telomeres: new views on chromosome evolution. Trends Genet. 12:48-52.
76. PIMPINELLI, S., M. BERLOCO, L. FANTI, P. DIMITRI, S. BONACCORSI, E. MARCHETTI, and R. CAIZZI. 1995. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc. Natl. Acad. Sci. USA 92:3804-3808.
77. PRIIMAGI, A. F., L. J. MIZROKHI, and Y. V. ILYIN. 1988. The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins. Gene 70:253-262.
78. RAO, P. S., and K. S. RAI. 1987. Inter and intraspecific variation in nuclear DNA content in Aedes mosquitoes. Heredity 59: 253-258.
79. ROBERTSON, H. M. 1993. The mariner transposable element is widespread in insects. Nature 362:241-245.
80. ROBERTSON, H. M., and D. J. LAMPE. 1995. Distribution of transposable elements in arthropods. Annu. Rev. Entomol. 40:333-357.
81. ROMANS, P., R. K. BHATTACHARYYA, and A. C. COLAVITA. 1998. Ikirara, a novel transposon family from the malaria vector mosquito Anopheles gambiae. Insect Mol. Biol. 7:1-10.
82. ROMANS, P., Z. TU, Z. KE, and H. H. HAGEDORN. 1995. Analysis of a vitellogenin gene of the mosquito, Aedes aegypti and comparisons to vitellogenins from other organisms. Insect Biochem. Mol. Biol. 25:939-958.
83. SAMBROOK, J., E. F. FRITSCH, and T. MANIATIS. 1989. Molecular cloning: A laboratory manual, 2nd edition. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
84. SANMIGUEL, P., A. TIKHONOV, Y.-K. JIN et al. (11 co-authors). 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765-768.
85. SCHWARZ-SOMMER, Z., L. LECLERCQ, X. GOEBEL, and H. SAEDLER. 1987. Cin4, an insert altering the structure of the A1 gene of Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 6:3873-3880.
86. SHERRATT, D. J. 1995. Mobile genetic elements. Oxford University Press, Oxford.
87. SHINNICK, T. M., R. A. LERNER, and J. G. SUTCLIFFE. 1981. Nucleotide sequence of moloney murine leukaemia virus. Nature 293:543-548.
88. SMIT, A. F. A. 1996. The origin of interspersed repeats in the human genome. Curr. Opin. Genet. Dev. 6:743-748.
89. STEINEMANN, M., and S. STEINEMANN. 1991. Preferential Y chromosomal location of TRIM, a novel transposable element of Drosophila miranda, obscura group. Chromosoma 101:169-179.
90. SWOFFORD, D. L. 1997. PAUP* version 4.0d59. (A test version, used with permission of D. L. Swofford; completed version 4.0 to be distributed by Sinauer, Sunderland, Mass.
91. TAKAHASHI, H., S. OKAZAKI, and H. FUJIWARA. 1997. A new family of site-specific retrotransposons SART1, is inserted into telomeric repeats of the silkworm, Bombyx mori. Nucleic Acids Res. 25:1578-1584.
92. TENG, S. C., S. X. WANG, and A. GABRIEL. 1995. A new non-LTR retrotransposon provides evidence for multiple distinct site-specific elements in Crithidia fasciculata miniexon arrays. Nucleic Acids Res. 23:2929-2936.
93. TU, Z. 1997. Three novel families of miniature inverted-repeat transposable elements are associated with genes of the yellow fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. USA 94:7475-7480.
94. Tu, Z., and H. H. HAGEDORN. 1997. Biochemical, molecular, and phylogenetic analysis of pyruvate carboxylase in the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol. Biol. 27:133-147.
95. UDOMKIT, A., S. FORBES, G. DALGLEISH, and D. J. FINNEGAN. 1995. BS, a novel LINE-like element in Drosophila melanogaster. Nucleic Acids Res. 23:1354-1358.
96. VAURY, C., A. BUCHETON, and A. PELISSON. 1989. The β heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98: 215-224.
97. VOYTAS, D. F. 1996. Retroelements in genome organization. Science 274:737-738.
98. WARREN, A. M., and J. M. CRAMPTON. 1991. The Aedes aegypti genome: complexity and organization. Genet. Res. 58: 225-232.
99. WARREN, A. M., M. A. HUGHES, and J. M. CRAMPTON. 1997. Zebedee: a novel copia-Ty1 transposable element in the genome of the medically important mosquito, Aedes aegypti. Mol. Gen. Genet. 254:505-513.
100. WESSLER, S. R., T. E. BUREAU, and S. E. WHITE. 1995. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5:814-821.
101. WILSON, R., R. AINSCOUGH, K. ANDERSON et al. (53 co-authors). 1994. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368: 32-38.
102. WRIGHT, D. A., N. KE, J. SMALLE, B. HAUGE, H. M. GOODMAN, and D. F. VOYTAS. 1996. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics 142:569-578.
103. XIONG, Y., and T. H. EICKBUSH. 1988a. Similarities of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 5:675-690.
104. _. 1988b. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol. Cell. Biol. 8:114-123.
105. _. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9: 3353-3362.
106. YOUNGMAN, S., H. G. VAN LUENEN, and R. H. PLASTERK. 1996. Rte-1, a retrotransposon-like element in Caenorhabditis elegans. FEBS Lett. 380:1-7.