High rate of chimeric gene origination by retroposition in plant genomes

Plant Cell

Volumn 18, Issue 8, 2006, Pages 1791-1802

  Wang, Wen ^a,b   Zheng, Hongkun ^b,c   Fan, Chuanzhu ^d   Li, Jun ^b   Shi, Junjie ^b,e   Cai, Zhengqiu ^b   Zhang, Guojie ^a,b,f   Liu, Dongyuan ^b   Zhang, Jianguo ^b   Vang, Søren ^g   Lu, Zhike ^b   Wong, Gane Ka Shu ^b   Long, Manyuan ^d   Wang, Jun ^b,c,g  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d UNIVERSITY OF CHICAGO   (United States)

^e SHANDONG NORMAL UNIVERSITY   (China)

^f UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^g AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; DATA PROCESSING; GENETIC ENGINEERING; PLANT CELL CULTURE; RANDOM PROCESSES;

CHIMERICAL GENES; GENE ORIGINATION; LONG TERMINAL REPEAT (LTR); RETROTRANSPOSONS;

GENES;

CELLS; DATA PROCESSING; GENES; GENETIC ENGINEERING; RANDOM PROCESSES;

ANIMALIA; MAMMALIA; ORYZA SATIVA; PRIMATES; ZEA MAYS;

EID: 33747465505     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.041905     Document Type: Article

References (70)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
3. Arhondakis, S., Auletta, F., Torelli, G., and D'Onofrio, G. (2004). Base composition and expression level of human genes. Gene 325, 165-169.
4. Barbazuk, W.B., Bedell, J.A., and Rabinowicz, P.D. (2005). Reduced representation sequencing: A success in maize and a promise for other plant genomes. Bioessays 27, 839-848.
5. Bedell, J.A., et al. (2005). Sorghum genome sequencing by methylation filtration. PLoS Biol. 3, e13.
6. Bennetzen, J.L. (2005). Transposable elements, gene creation and genome rearrangement in flowering plants. Curr. Opin. Genet. Dev. 15, 621-627.
7. Betran, E., Emerson, J.J., Kaessmann, H., and Long, M. (2004). Sex chromosomes and male functions: Where do new genes go? Cell Cycle 3, 873-875.
8. Betran, E., Thornton, K., and Long, M. (2002). Retroposed new genes out of the X in Drosophila. Genome Res. 12, 1854-1859.
9. Birney, E., Clamp, M., and Durbin, R. (2004). GeneWise and Genomewise. Genome Res. 14, 988-995.
10. Boguski, M.S., Lowe, T.M., and Tolstoshev, C.M. (1993). dbEST-Database for "expressed sequence tags". Nat. Genet. 4, 332-333.
11. Brosius, J. (1991). Retroposons-Seeds of evolution. Science 251, 753.
12. Charlesworth, D., Charlesworth, B., and Marais, G. (2005). Steps in the evolution of heteromorphic sex chromosomes. Heredity 95, 118-128.
13. Charlesworth, D., Liu, F.L., and Zhang, L. (1998). The evolution of the alcohol dehydrogenase gene family by loss of introns in plants of the genus Leavenworthia (Brassicaceae). Mol. Biol. Evol. 15, 552-559.
14. Drouin, G., and Dover, G.A. (1990). Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phytogeny of angiosperm actin genes. J. Mol. Evol. 31, 132-150.
15. Emerson, J.J., Kaessmann, H., Betran, E., and Long, M. (2004). Extensive gene traffic on the mammalian X chromosome. Science 303, 537-540.
16. Esnault, C., Maestre, J., and Heidmann, T. (2000). Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24, 363-367.
17. Gaut, B.S., Morton, B.R., McCaig, B.C., and Clegg, M.T. (1996). Substitution rate comparisons between grasses and palms: Synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl. Acad. Sci. USA 93, 10274-10279.
18. Goncalves, I., Duret, L., and Mouchiroud, D. (2000). Nature and structure of human genes that generate retropseudogenes. Genome Res. 10, 672-678.
19. Goodier, J.L., Ostertag, E.M., and Kazazian, H.H., Jr. (2000). Transduction of 3′-flanking sequences is common in L1 retrotransposition. Hum. Mol. Genet. 9, 653-657.
20. International Rice Genome Sequencing Project (2005). The map-based sequence of the rice genome. Nature 436, 793-800.
21. Jang, S., Lee, B., Kim, C., Kim, S.-J., Yim, J., Han, J.-J., Lee, S., Kim, S.-R., and An, G. (2003). The OsFOR1 gene encodes a polygalacturonase- inhibiting protein (PGIP) that regulates floral organ number in rice. Plant Mol. Biol. 53, 357-369.
22. Jiang, N., Bao, Z., Zhang, X., Eddy, S.R., and Wessler, S.R. (2004). Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569-573.
23. Jin, Y.K., and Bennetzen, J.L. (1994). Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6, 1177-1186.
24. Jin, Y.K., and Bennetzen, J.L. (1989). Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc. Natl. Acad. Sci. USA 86, 6235-6239.
25. Jones, C.D., and Begun, D.J. (2005). Parallel evolution of chimeric fusion genes. Proc. Natl. Acad. Sci. USA 102, 11373-11378.
26. Jurka, J. (1998). Repeats in genomic DNA: Mining and meaning. Curr. Opin. Struct. Biol. 8, 333-337.
27. Karpen, G.H., and Allshire, R.C. (1997). The case for epigenetic effects on centromere identity and function. Trends Genet. 13, 489-496.
28. Kazazian, H.H.J. (2004). Mobile elements: Drivers of genome evolution. Science 303, 1626-1632.
29. Kellogg, E.A. (2001). Evolutionary history of the grasses. Plant Physiol. 125, 1198-1205.
30. Kent, W.J. (2002). BLAT - The BLAST-like alignment tool. Genome Res. 12, 656-664.
31. Kikuchi, S., et al. (2003). Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301, 376-379.
32. Kumar, A., and Bennetzen, J.L. (1999). Plant retrotransposons. Annu. Rev. Genet. 33, 479-532.
33. Li, W.H. (1997). Molecular Evolution. (Sunderland, MA: Sinauer Associates).
34. Long, M., Betran, E., Thornton, K., and Wang, W. (2003). The origin of new genes: Glimpses from the young and old. Nat. Rev. Genet. 4, 865-875.
35. Long, M., and Langley, C.H. (1993). Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science 260, 91-95.
36. Ma, J., and Bennetzen, J.L. (2004). Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl. Acad. Sci. USA 101, 12404-12410.
37. Ma, J., and Bennetzen, J.L. (2006). Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc. Natl. Acad. Sci. USA 103, 383-388.
38. Ma, J., Devos, K.M., and Bennetzen, J.L. (2004). Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res. 14, 860-869.
39. Ma, L., et al. (2005). A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. Genome Res. 15, 1274-1283.
40. Marques, A.C., Dupanloup, I., Vinckenbosch, N., Reymond, A., and Kaessmann, H. (2005). Emergence of young human genes after a burst of retroposition in primates. PLoS Biol. 3, e357.
41. May, B.P., Lippman, Z.B., Fang, Y., Spector, D.L., and Martienssen, R.A. (2005). Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet. 1, e79.
42. McCarthy, E.M., Liu, J., Lizhi, G., and McDonald, J.F. (2002). Long terminal repeat retrotransposons of Oryza sativa. Genome Biol. 3, RESEARCH0053.
43. McCarthy, E.M., and McDonald, J.F. (2003). LTR_STRUC: A novel search and identification program for LTR retrotransposons. Bioinformatics 19, 362-367.
44. Moore, R.C., and Purugganan, M.D. (2003). The early stages of duplicate gene evolution. Proc. Natl. Acad. Sci. USA 100, 15682-15687.
45. Moran, J.V., DeBerardinis, R.J., and Kazazian, H.H., Jr. (1999). Exon shuffling by L1 retrotransposition. Science 283, 1530-1534.
46. Morgante, M., Brunner, S., Pea, G., Fengler, K., Zuccolo, A., and Rafalski, A. (2005). Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat. Genet. 37, 997-1002.
47. Nei, M., and Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418-426.
48. Nekrutenko, A., Makova, K.D., and Li, W.H. (2002). The K(A)/K(S) ratio test for assessing the protein-coding potential of genomic regions: An empirical and simulation study. Genome Res. 12, 198-202.
49. Nisole, S., Lynch, C., Stoye, J.P., and Yap, M.W. (2004). A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. USA 101, 13324-13328.
50. Nozawa, M., Aotsuka, T., and Tamura, K. (2005). A novel chimeric gene, siren, with retroposed promoter sequence in the Drosophila bipectinata complex. Genetics 171, 1719-1727.
51. Okazaki, Y., et al. (2002). Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420, 563-573.
52. Ostertag, E.M., and Kazazian, H.H., Jr. (2001). Biology of mammalian L1 retrotransposons. Annu. Rev. Genet. 35, 501-538.
53. Patthy, L. (1999). Genome evolution and the evolution of exon-shuffling - A review. Gene 238, 103-114.
54. Pavlicek, A., Gentles, A.J., Paces, J., Paces, V., and Jurka, J. (2006). Retroposition of processed pseudogenes: The impact of RNA stability and translational control. Trends Genet. 22, 69-73.
55. Petrov, D.A., Lozovskaya, E.R., and Hartl, D.L. (1996). High intrinsic rate of DNA loss in Drosophila. Nature 384, 346-349.
56. Pickeral, O.K., Makalowski, W., Boguski, M.S., and Boeke, J.D. (2000). Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. Genome Res. 10, 411-415.
57. Sayah, D.M., Sokolskaja, E., Berthoux, L., and Luban, J. (2004). Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
58. Schwarz-Sommer, Z., Leclercq, L., Gobel, E., and Saedler, H. (1987). Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 6, 3873-3880.
59. Torrents, D., Suyama, M., Zdobnov, E., and Bork, P. (2003). A genome-wide survey of human pseudogenes. Genome Res. 13, 2559-2567.
60. Venter, J.C., et al. (2001). The sequence of the human genome. Science 291, 1304-1351.
61. Vinckenbosch, N., Dupanloup, I., and Kaessmann, H. (2006). Evolutionary fate of retroposed gene copies in the human genome. Proc. Natl. Acad. Sci. USA 103, 3220-3225.
62. Wang, J., Zhang, J., Zheng, H., Li, J., Liu, D., Li, H., Samudrala, R., Yu, J., and Wong, G.K.-S. (2004). Mouse transcriptome: Neutral evolution of 'non-coding' complementary DNAs. Nature 431, 757.
63. Wang, W., Brunet, F.G., Nevo, E., and Long, M. (2002). Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 99, 4448-4453.
64. Wei, W., Gilbert, N., Ooi, S.L., Lawler, J.F., Ostertag, E.M., Kazazian, H.H., Boeke, J.D., and Moran, J.V. (2001). Human L1 retrotransposition: Cis preference versus trans complementation. Mol. Cell. Biol. 21, 1429-1439.
65. Whitelaw, C.A., et al. (2003). Enrichment of gene-coding sequences in maize by genome filtration. Science 302, 2118-2120.
66. Yang, Z. (1997). PAML: A program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555-556.
67. Yu, J., Wang, J., Lin, W., Li, S., Li, H., Zhou, J., Ni, P., Dong, W., Hu, S., Zeng, C., Zhang, J., Zhang, Y., et al. (2005). The genomes of Oryza sativa: A history of duplications. PLoS Biol. 3, e38.
68. Zhang, J., Dean, A.M., Brunet, F., and Long, M. (2004). Evolving protein functional diversity in new genes of Drosophila. Proc. Natl. Acad. Sci. USA 101, 16246-16250.
69. Zhang, Y., Wu, Y., Liu, Y., and Han, B. (2005). Computational identification of 69 retroposons in Arabidopsis. Plant Physiol. 138, 935-948.
70. Zhang, Z., Harrison, P.M., Liu, Y., and Gerstein, M. (2003). Millions of years of evolution preserved: A comprehensive catalog of the processed pseudogenes in the human genome. Genome Res. 13, 2541-2558.