New genes originated via multiple recombinational pathways in the beta-globin gene family of rodents.
Species differences in the size or membership composition of multigene families can be attributed to lineage-specific additions of new genes via duplication, losses of genes via deletion or inactivation, and the creation of chimeric genes via domain shuffling or gene fusion. In principle, it should be possible to infer the recombinational pathways responsible for each of these different types of genomic change by conducting detailed comparative analyses of genomic sequence data. Here, we report an attempt to unravel the complex evolutionary history of the beta-globin gene family in a taxonomically diverse set of rodent species. The main objectives were: 1) to characterize the genomic structure of the beta-globin gene cluster of rodents; 2) to assign orthologous and paralogous relationships among duplicate copies of beta-like globin genes; and 3) to infer the specific recombinational pathways responsible for gene duplications, gene deletions, and the creation of chimeric fusion genes. Results of our comparative genomic analyses revealed that variation in gene family size among rodent species is mainly attributable to the differential gain and loss of later expressed beta-globin genes via unequal crossing-over. However, two distinct recombinational mechanisms were implicated in the creation of chimeric fusion genes. In muroid rodents, a chimeric gamma/epsilon fusion gene was created by unequal crossing-over between the embryonic epsilon- and gamma-globin genes. Interestingly, this gamma/epsilon fusion gene was generated in the same fashion as the "anti-Lepore" 5'-delta-(beta/delta)-beta-3' duplication mutant in humans (the reciprocal exchange product of the pathological hemoglobin Lepore deletion mutant). By contrast, in the house mouse, Mus musculus, a chimeric beta/delta fusion pseudogene was created by a beta-globin --> delta-globin gene conversion event. Although the gamma/epsilon and beta/delta fusion genes share a similar chimeric gene structure, they originated via completely different recombinational pathways.
Hoffmann
Federico G
FG
School of Biological Sciences, University of Nebraska, USA.
Opazo
Juan C
JC
Storz
Jay F
JF
D000818:Animals; D019143:Evolution, Molecular; D051379:Mice; D005810:Multigene Family; D051381:Rats; D011995:Recombination, Genetic; D012377:Rodentia / Q000235:genetics*; D055544:beta-Globins / Q000235:genetics*
D055544:beta-Globins
FEMS Microbiol Lett. 1999 May 15;174(2):247-50
10339815
Mol Biol Evol. 2008 Mar;25(3):591-602
18178968
J Mol Biol. 1984 Dec 25;180(4):803-23
6527390
Science. 2001 Dec 14;294(5550):2348-51
11743200
Nucleic Acids Res. 1997 Dec 15;25(24):4876-82
9396791
Cell. 1980 Apr;19(4):959-72
6155216
Prog Nucleic Acid Res Mol Biol. 1984;31:315-462
6397774
Gene. 1989 Jun 30;79(1):139-50
2777087
Cell. 1987 Dec 24;51(6):975-85
3690667
Mol Cell Biol. 1992 Mar;12(3):1292-303
1545810
Mol Biol Evol. 1985 Nov;2(6):514-25
3870874
Nat Rev Genet. 2003 Nov;4(11):865-75
14634634
Genetics. 2008 Mar;178(3):1623-38
18245844
J Biol Chem. 1984 Mar 25;259(6):3748-56
6706976
Mol Biol Evol. 1996 Sep;13(7):1012-22
8752008
PLoS Genet. 2007 Nov;3(11):e197
17997610
Gene. 1997 Dec 31;205(1-2):73-94
9461381
Mol Biol Evol. 1984 Jul;1(4):302-16
6599969
Genome Res. 2005 Jan;15(1):184-94
15590941
BMC Evol Biol. 2004 Jun 28;4:18
15222900
Nucleic Acids Res. 2003 Jul 1;31(13):3518-24
12824357
J Biol Chem. 1991 Apr 25;266(12):7469-80
2019578
Nat Rev Genet. 2006 Feb;7(2):85-97
16418744
PLoS One. 2006 Dec 20;1:e85
17183716
Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10950-5
17573529
Syst Biol. 2004 Aug;53(4):533-53
15371245
J Theor Biol. 1990 Feb 22;142(4):485-501
2338834
Mol Biol Evol. 2008 Sep;25(9):1795-808
18453548
J Biol Chem. 1984 Mar 25;259(6):3739-47
6323438
Mol Phylogenet Evol. 2005 Apr;35(1):225-34
15737593
Mol Biol Evol. 1985 Jul;2(4):304-20
3870864
Proc Natl Acad Sci U S A. 1990 Oct;87(19):7693-7
2217202
Proc Natl Acad Sci U S A. 1984 Nov;81(21):6589-93
6593719
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7122-7
17438280
PLoS Genet. 2007 Mar 30;3(3):e45
17397259
Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14560-5
11121057
Genes Genet Syst. 2006 Oct;81(5):367-71
17159299
Proc Natl Acad Sci U S A. 2008 Sep 2;105(35):12950-5
18755893
J Mol Evol. 1989 Mar;28(3):175-84
2494347
Genetics. 2007 Sep;177(1):481-500
17660536
Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1590-5
18216242
Mol Biol Evol. 1984 Sep;1(5):390-410
6599973
Hum Mol Genet. 2006 Apr 1;15(7):1099-111
16501000
Genetics. 2007 Nov;177(3):1941-9
17947411
J Mol Biol. 1989 Jan 5;205(1):15-40
2486295
Mol Biol Evol. 1986 May;3(3):243-61
3444401
J Exp Biol. 1998 Apr;201(Pt 8):1099-117
9510523
Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4701-6
10758160
Mol Biol Evol. 1988 Mar;5(2):134-40
3367782
Bioinformatics. 2003 Aug 12;19(12):1572-4
12912839
Hum Mol Genet. 2002 Feb 1;11(3):207-15
11823440
J Mol Biol. 1982 Apr 15;156(3):487-503
6214636
J Biol Chem. 1989 Jan 5;264(1):68-79
2491855
J Mol Biol. 1997 Apr 25;268(1):78-94
9149143
Mol Biol Evol. 1993 Jan;10(1):73-102
8383794
PLoS Genet. 2005 Dec;1(6):e49
16444292
Genome Res. 2000 Apr;10(4):577-86
10779500
Hum Mol Genet. 2004 Apr 1;13 Spec No 1:R57-64
14764619
Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):8921-7
16709669
Genetics. 1991 May;128(1):143-61
2060774
Mol Biol Evol. 1990 Sep;7(5):407-22
2263193
Cold Spring Harb Symp Quant Biol. 1987;52:875-90
3454296
Proc Natl Acad Sci U S A. 1988 Jun;85(11):3893-7
3375246
J Mol Biol. 1989 Jan 5;205(1):41-62
2926808