Duplicate Abalone Egg Coat Proteins Bind Sperm Lysin Similarly, but Evolve Oppositely, Consistent with Molecular Mimicry at Fertilization
Sperm and egg proteins constitute a remarkable paradigm in evolutionary biology:
despite their fundamental role in mediating fertilization (suggesting stasis), some of these molecules are among the most rapidly evolving ones known, and their divergence can lead to reproductive isolation. Because of strong selection to maintain function among interbreeding individuals, interacting fertilization proteins should also exhibit a strong signal of correlated divergence among closely related species. We use evidence of such molecular co-evolution to target biochemical studies of fertilization in North Pacific abalone (Haliotis spp.), a model system of reproductive protein evolution. We test the evolutionary rates (dN/dS) of abalone sperm lysin and two duplicated egg coat proteins (VERL and VEZP14), and find a signal of co-evolution specific to ZP-N, a putative sperm binding motif previously identified by homology modeling. Positively selected residues in VERL and VEZP14 occur on the same face of the structural model, suggesting a common mode of interaction with sperm lysin. We test this computational prediction biochemically, confirming that the ZP-N motif is sufficient to bind lysin and that the affinities of VERL and VEZP14 are comparable. However, we also find that on phylogenetic lineages where lysin and VERL evolve rapidly, VEZP14 evolves slowly, and vice versa. We describe a model of sexual conflict that can recreate this pattern of anti-correlated evolution by assuming that VEZP14 acts as a VERL mimic, reducing the intensity of sexual conflict and slowing the co-evolution of lysin and VERL.
Vyšlo v časopise:
Duplicate Abalone Egg Coat Proteins Bind Sperm Lysin Similarly, but Evolve Oppositely, Consistent with Molecular Mimicry at Fertilization. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003287
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003287
Souhrn
Sperm and egg proteins constitute a remarkable paradigm in evolutionary biology:
despite their fundamental role in mediating fertilization (suggesting stasis), some of these molecules are among the most rapidly evolving ones known, and their divergence can lead to reproductive isolation. Because of strong selection to maintain function among interbreeding individuals, interacting fertilization proteins should also exhibit a strong signal of correlated divergence among closely related species. We use evidence of such molecular co-evolution to target biochemical studies of fertilization in North Pacific abalone (Haliotis spp.), a model system of reproductive protein evolution. We test the evolutionary rates (dN/dS) of abalone sperm lysin and two duplicated egg coat proteins (VERL and VEZP14), and find a signal of co-evolution specific to ZP-N, a putative sperm binding motif previously identified by homology modeling. Positively selected residues in VERL and VEZP14 occur on the same face of the structural model, suggesting a common mode of interaction with sperm lysin. We test this computational prediction biochemically, confirming that the ZP-N motif is sufficient to bind lysin and that the affinities of VERL and VEZP14 are comparable. However, we also find that on phylogenetic lineages where lysin and VERL evolve rapidly, VEZP14 evolves slowly, and vice versa. We describe a model of sexual conflict that can recreate this pattern of anti-correlated evolution by assuming that VEZP14 acts as a VERL mimic, reducing the intensity of sexual conflict and slowing the co-evolution of lysin and VERL.
Zdroje
1. ClarkAG, GlanowskiS, NielsenR, ThomasPD, KejariwalA, et al. (2003) Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302: 1960–1963.
2. NielsenR, BustamanteC, ClarkAG, GlanowskiS, SacktonTB, et al. (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 3: e170 doi:10.1371/journal.pbio.0030170.
3. GeorgeRD, McVickerG, DiederichR, NgSB, MacKenzieAP, et al. (2011) Trans genomic capture and sequencing of primate exomes reveals new targets of positive selection. Genome Res 21: 1686–1694.
4. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218.
5. SwansonWJ, VacquierVD (2002) Rapid evolution of reproductive proteins. Nature Reviews Genetics 3: 137–144.
6. ClarkNL, AagaardJE, SwansonWJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131: 11–22.
7. LyonJD, VacquierVD (1999) Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelline envelope. Developmental Biology 214: 151–159.
8. ClarkNL, AquadroCF (2010) A novel method to detect proteins evolving at correlated rates: identifying new functional relationships between coevolving proteins. Mol Biol Evol 27: 1152–1161.
9. ClarkNL, GasperJ, SekinoM, SpringerSA, AquadroCF, et al. (2009) Coevolution of interacting fertilization proteins. PLoS Genet 5: e1000570 doi:10.1371/journal.pgen.1000570.
10. SwansonWJ, VacquierVD (1997) The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proceedings of the National Academy of Sciences of the United States of America 94: 6724–6729.
11. KameiN, GlabeCG (2003) The species-specific egg receptor for sea urchin sperm adhesion is EBR1,a novel ADAMTS protein. Genes Dev 17: 2502–2507.
12. HaradaY, TakagakiY, SunagawaM, SaitoT, YamadaL, et al. (2008) Mechanism of self-sterility in a hermaphroditic chordate. Science 320: 548–550.
13. LewisCA, TalbotCF, VacquierVD (1982) A protein from abalone sperm dissolves the egg vitelline layer by a nonenzymatic mechanism. Developmental Biology 92: 227–239.
14. Leighton DL (2000) The Biology and Culture of the California Abalones. Pittsburgh, PA: Dorrance Publishing Co. 216 p.
15. GalindoBE, MoyGW, SwansonWJ, VacquierVD (2002) Full Length Sequence of VERL, the egg vitelline envelope receptor for abalone sperm lysin. Gene 288: 111–117.
16. KresgeN, VacquierVD, StoutCD (2001) Abalone lysin: the dissolving and evolving sperm protein. Bioessays 23: 95–103.
17. LeeY-H, VacquierVD (1995) Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Marine Biology 124: 267–268.
18. GalindoBE, VacquierVD, SwansonWJ (2003) Positive selection in the egg receptor for abalone sperm lysin. Proc Natl Acad Sci U S A 100: 4639–4643.
19. AagaardJE, VacquierVD, MacCossMJ, SwansonWJ (2010) ZP domain proteins in the abalone egg coat include a paralog of VERL under positive selection that binds lysin and 18-kDa sperm proteins. Mol Biol Evol 27: 193–203.
20. AagaardJE, YiX, MacCossMJ, SwansonWJ (2006) Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs. Proc Natl Acad Sci U S A 103: 17302–17307.
21. JovineL, DarieCC, LitscherES, WassarmanPM (2005) Zona pellucida domain proteins. Annual Review of Biochemistry 74: 83–114.
22. SwansonWJ, AagaardJE, VacquierVD, MonneM, Sadat Al HosseiniH, et al. (2011) The molecular basis of sex: linking yeast to human. Mol Biol Evol 28: 1963–1966.
23. MonneM, HanL, SchwendT, BurendahlS, JovineL (2008) Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456: 653–657.
24. ChenMH, ShenZM, BobinS, KahnPC, LipkePN (1995) Structure of Saccharomyces cerevisiae alpha-agglutinin. Evidence for a yeast cell wall protein with multiple immunoglobulin-like domains with atypical disulfides. J Biol Chem 270: 26168–26177.
25. VacquierVD, SwansonWJ, LeeYH (1997) Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? Journal of Molecular Evolution 44: S15–S22.
26. LipkePN, KurjanJ (1992) Sexual agglutination in budding yeasts: structure, function, and regulation of adhesion glycoproteins. Microbiol Rev 56: 180–194.
27. DranginisAM, RauceoJM, CoronadoJE, LipkePN (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71: 282–294.
28. VenterJC, AdamsMD, MyersEW, LiPW, MuralRJ, et al. (2001) The sequence of the human genome. Science 291: 1304–1351.
29. WongJL, WesselGM (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72: 1–151.
30. GouldMC, StephanoJL (2003) Polyspermy prevention in marine invertebrates. Microsc Res Tech 61: 379–388.
31. MozingoNM, VacquierVD, ChandlerDE (1995) Structural features of the abalone egg extracellular matrix and its role in gamete interaction during fertilization. Molecular Reproduction and Development 41: 493–502.
32. LeeYH, VacquierVD (1992) The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biological Bulletin (Woods Hole) 182: 97–104.
33. DeanJ (2004) Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays 26: 29–38.
34. PalumbiSR (2009) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102: 66–76.
35. VacquierVD (1998) Evolution of gamete recognition proteins. Science 281: 1995–1998.
36. WoolhouseME, WebsterJP, DomingoE, CharlesworthB, LevinBR (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet 32: 569–577.
37. SwansonWJ, VacquierVD (1995) Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. Proceedings of the National Academy of Sciences of the United States of America 92: 4957–4961.
38. Wallace AR (1889) Darwinism. London: MacMillan and Co. 494 p.
39. Darwin C (1859) On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life. London: J. Murray.
40. SirotLK, BrockmannHJ (2001) Costs of sexual interactions to females in Rambur's forktail damselfly, Ischnura ramburi (Zygoptera: Coenagrionidae). Animal Behaviour 61: 415–424.
41. SaetreG-P, SlagsvoldT (1996) The significance of female mimicry in male contests. American Naturalist 147: 981–995.
42. MullerMN, WranghamR (2002) Sexual mimicry in hyenas. Q Rev Biol 77: 3–16.
43. RobertsonHM (1985) Female dimorphism and mating behavior in a damselfly, Ischnura ramburi: females mimicking males. Animal Behaviour 33: 805–809.
44. MantovaniA, LocatiM, VecchiA, SozzaniS, AllavenaP (2001) Decoy receptors: a strategy to regulate inflammatory cytokines and chemokines. Trends Immunol 22: 328–336.
45. ForceA, LynchM, PickettFB, AmoresA, YanYL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545.
46. YangZ, SwansonWJ, VacquierVD (2000) Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Molecular Biology and Evolution 17: 1446–1455.
47. ClarkNL, AlaniE, AquadroCF (2012) Evolutionary rate covariation reveals shared functionality and co-expression of genes. Genome Research
48. YangZ, NielsenR (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. Journal of Molecular Evolution 46: 409–418.
49. Yang Z (2000) Phylogenetic Analysis by Maximum Likelihood (PAML). 3.1 ed. London: University College London.
50. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computinhg.
51. YangZ, WongWS, NielsenR (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107–1118.
52. SchrodingerLLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
53. KresgeN, VacquierVD, StoutCD (2000) The high resolution crystal structure of green abalone sperm lysin: implications for species-specific binding of the egg receptor. Journal of Molecular Biology 296: 1225–1234.
54. ChinowskyTM, SoelbergSD, BakerP, SwansonNR, KauffmanP, et al. (2007) Portable 24-analyte surface plasmon resonance instruments for rapid, versatile biodetection. Biosens Bioelectron 22: 2268–2275.
55. VacquierVD, LeeYH (1993) Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1: 181–196.
56. HayashiTI, VoseM, GavriletsS (2007) Genetic differentiation by sexual conflict. Evolution 61: 516–529.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 2
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Complex Inheritance of Melanoma and Pigmentation of Coat and Skin in Grey Horses
- Coordination of Chromatid Separation and Spindle Elongation by Antagonistic Activities of Mitotic and S-Phase CDKs
- Autophagy Induction Is a Tor- and Tp53-Independent Cell Survival Response in a Zebrafish Model of Disrupted Ribosome Biogenesis
- Assembly of the Auditory Circuitry by a Genetic Network in the Mouse Brainstem