A Young Duplicate Gene Plays Essential Roles in Spermatogenesis by Regulating Several Y-Linked Male Fertility Genes
Gene duplication is supposed to be the major source for genetic innovations. However, how a new duplicate gene acquires functions by integrating into a pathway and results in adaptively important phenotypes has remained largely unknown. Here, we investigated the biological roles and the underlying molecular mechanism of the young kep1 gene family in the Drosophila melanogaster species subgroup to understand the origin and evolution of new genes with new functions. Sequence and expression analysis demonstrates that one of the new duplicates, nsr (novel spermatogenesis regulator), exhibits positive selection signals and novel subcellular localization pattern. Targeted mutagenesis and whole-transcriptome sequencing analysis provide evidence that nsr is required for male reproduction associated with sperm individualization, coiling, and structural integrity of the sperm axoneme via regulation of several Y chromosome fertility genes post-transcriptionally. The absence of nsr-like expression pattern and the presence of the corresponding cis-regulatory elements of the parental gene kep1 in the pre-duplication species Drosophila yakuba indicate that kep1 might not be ancestrally required for male functions and that nsr possibly has experienced the neofunctionalization process, facilitated by changes of trans-regulatory repertories. These findings not only present a comprehensive picture about the evolution of a new duplicate gene but also show that recently originated duplicate genes can acquire multiple biological roles and establish novel functional pathways by regulating essential genes.
Vyšlo v časopise:
A Young Duplicate Gene Plays Essential Roles in Spermatogenesis by Regulating Several Y-Linked Male Fertility Genes. PLoS Genet 6(12): e32767. doi:10.1371/journal.pgen.1001255
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001255
Souhrn
Gene duplication is supposed to be the major source for genetic innovations. However, how a new duplicate gene acquires functions by integrating into a pathway and results in adaptively important phenotypes has remained largely unknown. Here, we investigated the biological roles and the underlying molecular mechanism of the young kep1 gene family in the Drosophila melanogaster species subgroup to understand the origin and evolution of new genes with new functions. Sequence and expression analysis demonstrates that one of the new duplicates, nsr (novel spermatogenesis regulator), exhibits positive selection signals and novel subcellular localization pattern. Targeted mutagenesis and whole-transcriptome sequencing analysis provide evidence that nsr is required for male reproduction associated with sperm individualization, coiling, and structural integrity of the sperm axoneme via regulation of several Y chromosome fertility genes post-transcriptionally. The absence of nsr-like expression pattern and the presence of the corresponding cis-regulatory elements of the parental gene kep1 in the pre-duplication species Drosophila yakuba indicate that kep1 might not be ancestrally required for male functions and that nsr possibly has experienced the neofunctionalization process, facilitated by changes of trans-regulatory repertories. These findings not only present a comprehensive picture about the evolution of a new duplicate gene but also show that recently originated duplicate genes can acquire multiple biological roles and establish novel functional pathways by regulating essential genes.
Zdroje
1. OhnoS
1970 Evolution by gene duplication. New York Springer-Verlag
2. ZhouQ
WangW
2008 On the origin and evolution of new genes–a genomic and experimental perspective. J Genet Genomics 35 639 648
3. LongM
BetranE
ThorntonK
WangW
2003 The origin of new genes: glimpses from the young and old. Nat Rev Genet 4 865 875
4. LynchM
ForceA
2000 The probability of duplicate gene preservation by subfunctionalization. Genetics 154 459 473
5. LynchM
ConeryJS
2000 The evolutionary fate and consequences of duplicate genes. Science 290 1151 1155
6. LoppinB
LepetitD
DorusS
CoubleP
KarrTL
2005 Origin and neofunctionalization of a Drosophila paternal effect gene essential for zygote viability. Curr Biol 15 87 93
7. KalameghamR
SturgillD
SiegfriedE
OliverB
2007 Drosophila mojoless, a retroposed GSK-3, has functionally diverged to acquire an essential role in male fertility. Mol Biol Evol 24 732 742
8. DaiH
ChenY
ChenS
MaoQ
KennedyD
2008 The evolution of courtship behaviors through the origination of a new gene in Drosophila. Proc Natl Acad Sci U S A 105 7478 7483
9. LiD
DongY
JiangY
JiangH
CaiJ
2010 A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand. Cell Res 20 408 420
10. RogersRL
BedfordT
LyonsAM
HartlDL
2010 Adaptive impact of the chimeric gene Quetzalcoatl in Drosophila melanogaster. Proc Natl Acad Sci U S A 107 10943 10948
11. ZhangJ
DeanAM
BrunetF
LongM
2004 Evolving protein functional diversity in new genes of Drosophila. Proc Natl Acad Sci U S A 101 16246 16250
12. NurminskyDI
NurminskayaMV
De AguiarD
HartlDL
1998 Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396 572 575
13. ZhangJ
ZhangYP
RosenbergHF
2002 Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet 30 411 415
14. WangW
BrunetFG
NevoE
LongM
2002 Origin of sphinx, a young chimeric RNA gene in Drosophila melanogaster. Proc Natl Acad Sci U S A 99 4448 4453
15. YangS
ArguelloJR
LiX
DingY
ZhouQ
2008 Repetitive element-mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet 4 e3 doi:10.1371/journal.pgen.0040003
16. Di FruscioM
StyhlerS
WikholmE
BoulangerMC
LaskoP
2003 Kep1 interacts genetically with dredd/caspase-8, and kep1 mutants alter the balance of dredd isoforms. Proc Natl Acad Sci U S A 100 1814 1819
17. YangZ
1998 Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15 568 573
18. TamuraK
SubramanianS
KumarS
2004 Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21 36 44
19. LiW
1997 Molecular Evoltuion. Sunderland Sinauer Associates
20. PritchardJK
SchaefferSW
1997 Polymorphism and divergence at a Drosophila pseudogene locus. Genetics 147 199 208
21. HegerA
PontingCP
2007 Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. Genome Res 17 1837 1849
22. Di FruscioM
ChenT
BonyadiS
LaskoP
RichardS
1998 The identification of two Drosophila K homology domain proteins. Kep1 and SAM are members of the Sam68 family of GSG domain proteins. J Biol Chem 273 30122 30130
23. VibranovskiMD
LopesHF
KarrTL
LongM
2009 Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet 5 e1000731 doi:10.1371/journal.pgen.1000731
24. LamondAI
SpectorDL
2003 Nuclear speckles: a model for nuclear organelles. Nat Rev Mol Cell Biol 4 605 612
25. SpectorDL
1993 Nuclear organization of pre-mRNA processing. Curr Opin Cell Biol 5 442 447
26. Byun-McKaySA
GeetaR
2007 Protein subcellular relocalization: a new perspective on the origin of novel genes. Trends Ecol Evol 22 338 344
27. XieHB
GolicKG
2004 Gene deletions by ends-in targeting in Drosophila melanogaster. Genetics 168 1477 1489
28. RobertsonHM
PrestonCR
PhillisRW
Johnson-SchlitzDM
BenzWK
1988 A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118 461 470
29. LindsleyDL
TokuyasuKT
1980 Spermatogensis.
AshburnerM
WrightTR
Genetics and Biology of Drosophila New York Academic Press 225 294
30. FabrizioJJ
HimeG
LemmonSK
BazinetC
1998 Genetic dissection of sperm individualization in Drosophila melanogaster. Development 125 1833 1843
31. SantelA
WinhauerT
BlumerN
Renkawitz-PohlR
1997 The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech Dev 64 19 30
32. WangZ
GersteinM
SnyderM
2009 RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10 57 63
33. GoldsteinLS
HardyRW
LindsleyDL
1982 Structural genes on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A 79 7405 7409
34. GepnerJ
HaysTS
1993 A fertility region on the Y chromosome of Drosophila melanogaster encodes a dynein microtubule motor. Proc Natl Acad Sci U S A 90 11132 11136
35. CarvalhoAB
LazzaroBP
ClarkAG
2000 Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. Proc Natl Acad Sci U S A 97 13239 13244
36. HardyRW
LindsleyDL
LivakKJ
LewisB
SiverstenAL
1984 Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics 107 591 610
37. HardyRW
TokuyasuKT
LindsleyDL
1981 Analysis of spermatogenesis in Drosophila melanogaster bearing deletions for Y-chromosome fertility genes. Chromosoma 83 593 617
38. ZhangP
StankiewiczRL
1998 Y-Linked male sterile mutations induced by P element in Drosophila melanogaster. Genetics 150 735 744
39. TimakovB
ZhangP
2000 Genetic analysis of a Y-chromosome region that induces triplosterile phenotypes and is essential for spermatid individualization in Drosophila melanogaster. Genetics 155 179 189
40. ZhaoJ
HymanL
MooreC
1999 Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63 405 445
41. KenanDJ
QueryCC
KeeneJD
1991 RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16 214 220
42. SinghR
ValcarcelJ
2005 Building specificity with nonspecific RNA-binding proteins. Nat Struct Mol Biol 12 645 653
43. MarquesAC
DupanloupI
VinckenboschN
ReymondA
KaessmannH
2005 Emergence of young human genes after a burst of retroposition in primates. PLoS Biol 3 e357 doi:10.1371/journal.pbio.0030357
44. VinckenboschN
DupanloupI
KaessmannH
2006 Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci U S A 103 3220 3225
45. ZhangY
SturgillD
ParisiM
KumarS
OliverB
2007 Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450 233 237
46. KaessmannH
VinckenboschN
LongM
2009 RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 10 19 31
47. VibranovskiMD
ZhangY
LongM
2009 General gene movement off the X chromosome in the Drosophila genus. Genome Res 19 897 903
48. de KresterDM
KerrJB
1994 The cytology of testis. The Physiology of Reproduction New York Raven Press Ltd 1177 1290
49. JouannetP
EscallerD
SerresC
DavidG
1983 Motility of human sperm without outer dynein arms. J Submicrosc Cytol 15 67 71
50. WolfJP
FeneuxD
EscalierD
RodriguesD
FrydmanR
1993 Pregnancy after subzonal insemination with spermatozoa lacking outer dynein arms. J Reprod Fertil 97 487 492
51. KeatingJ
GrundyCE
FiveyPS
ElliottM
RobinsonJ
1997 Investigation of the association between the presence of cytoplasmic residues on the human sperm midpiece and defective sperm function. J Reprod Fertil 110 71 77
52. KumarS
TamuraK
NeiM
2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 150 163
53. YangZ
NielsenR
2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17 32 43
54. RubinGM
SpradlingAC
1982 Genetic transformation of Drosophila with transposable element vectors. Science 218 348 353
55. BaroloS
CarverLA
PosakonyJW
2000 GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29 726, 728, 730, 732
56. PuigO
CasparyF
RigautG
RutzB
BouveretE
2001 The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24 218 229
57. WangZ
MannRS
2003 Requirement for two nearly identical TGIF-related homeobox genes in Drosophila spermatogenesis. Development 130 2853 2865
58. HeatwoleVM
HaynesSR
1996 Association of RB97D, an RRM protein required for male fertility, with a Y chromosome lampbrush loop in Drosophila spermatocytes. Chromosoma 105 285 292
59. TusherVG
TibshiraniR
ChuG
2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121
60. LiR
YuC
LiY
LamTW
YiuSM
2009 SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25 1966 1967
61. WangL
FengZ
WangX
ZhangX
2010 DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26 136 138
62. MortazaviA
WilliamsBA
McCueK
SchaefferL
WoldB
2008 Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5 621 628
63. KieferBI
1970 Development, organization, and degeneration of the Drosophila sperm flagellum. J Cell Sci 6 177 194
64. MitchisonTJ
MitchisonHM
2010 How cilia beat. Nature 463 308 309
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 12
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