Duplicate Abalone Egg Coat Proteins Bind Sperm Lysin Similarly, but Evolve Oppositely, Consistent with Molecular Mimicry at Fertilization

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Aagaard, Jan E ^a   Springer, Stevan A ^b   Soelberg, Scott D ^a   Swanson, Willie J ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EGG PROTEIN; LYSINE; SPERM LYSINE; UNCLASSIFIED DRUG; VITELLINE ENVELOPE RECEPTOR FOR LYSINE; VITELLINE ENVELOPE ZONA PELLUCIDA 14 PROTEIN;

ABALONE; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; COEVOLUTION; FERTILIZATION; MATING; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; OOCYTE; PHYLOGENY; PROTEIN BINDING; PROTEIN MOTIF; SPERM; STATISTICAL MODEL;

ANIMALS; EGG PROTEINS; EVOLUTION, MOLECULAR; FEMALE; FERTILIZATION; GASTROPODA; MALE; MOLECULAR MIMICRY; MUCOPROTEINS; PHYLOGENY; REPRODUCTIVE ISOLATION; SELECTION, GENETIC; SPERMATOZOA;

EID: 84874783190     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003287     Document Type: Article

References (56)

1. Clark AG, Glanowski S, Nielsen R, Thomas PD, Kejariwal A, et al. (2003) Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 302: 1960-1963.
2. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, 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. George RD, McVicker G, Diederich R, Ng SB, MacKenzie AP, 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. Swanson WJ, Vacquier VD, (2002) Rapid evolution of reproductive proteins. Nature Reviews Genetics 3: 137-144.
6. Clark NL, Aagaard JE, Swanson WJ, (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131: 11-22.
7. Lyon JD, Vacquier VD, (1999) Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelline envelope. Developmental Biology 214: 151-159.
8. Clark NL, Aquadro CF, (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. Clark NL, Gasper J, Sekino M, Springer SA, Aquadro CF, et al. (2009) Coevolution of interacting fertilization proteins. PLoS Genet 5: e1000570 doi:10.1371/journal.pgen.1000570.
10. Swanson WJ, Vacquier VD, (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. Kamei N, Glabe CG, (2003) The species-specific egg receptor for sea urchin sperm adhesion is EBR1,a novel ADAMTS protein. Genes Dev 17: 2502-2507.
12. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, et al. (2008) Mechanism of self-sterility in a hermaphroditic chordate. Science 320: 548-550.
13. Lewis CA, Talbot CF, Vacquier VD, (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. Galindo BE, Moy GW, Swanson WJ, Vacquier VD, (2002) Full Length Sequence of VERL, the egg vitelline envelope receptor for abalone sperm lysin. Gene 288: 111-117.
16. Kresge N, Vacquier VD, Stout CD, (2001) Abalone lysin: the dissolving and evolving sperm protein. Bioessays 23: 95-103.
17. Lee Y-H, Vacquier VD, (1995) Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Marine Biology 124: 267-268.
18. Galindo BE, Vacquier VD, Swanson WJ, (2003) Positive selection in the egg receptor for abalone sperm lysin. Proc Natl Acad Sci U S A 100: 4639-4643.
19. Aagaard JE, Vacquier VD, MacCoss MJ, Swanson WJ, (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. Aagaard JE, Yi X, MacCoss MJ, Swanson WJ, (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. Jovine L, Darie CC, Litscher ES, Wassarman PM, (2005) Zona pellucida domain proteins. Annual Review of Biochemistry 74: 83-114.
22. Swanson WJ, Aagaard JE, Vacquier VD, Monne M, Sadat Al Hosseini H, et al. (2011) The molecular basis of sex: linking yeast to human. Mol Biol Evol 28: 1963-1966.
23. Monne M, Han L, Schwend T, Burendahl S, Jovine L, (2008) Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 456: 653-657.
24. Chen MH, Shen ZM, Bobin S, Kahn PC, Lipke PN, (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. Vacquier VD, Swanson WJ, Lee YH, (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. Lipke PN, Kurjan J, (1992) Sexual agglutination in budding yeasts: structure, function, and regulation of adhesion glycoproteins. Microbiol Rev 56: 180-194.
27. Dranginis AM, Rauceo JM, Coronado JE, Lipke PN, (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71: 282-294.
28. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, et al. (2001) The sequence of the human genome. Science 291: 1304-1351.
29. Wong JL, Wessel GM, (2006) Defending the zygote: search for the ancestral animal block to polyspermy. Curr Top Dev Biol 72: 1-151.
30. Gould MC, Stephano JL, (2003) Polyspermy prevention in marine invertebrates. Microsc Res Tech 61: 379-388.
31. Mozingo NM, Vacquier VD, Chandler DE, (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. Lee YH, Vacquier VD, (1992) The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biological Bulletin (Woods Hole) 182: 97-104.
33. Dean J, (2004) Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays 26: 29-38.
34. Palumbi SR, (2009) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102: 66-76.
35. Vacquier VD, (1998) Evolution of gamete recognition proteins. Science 281: 1995-1998.
36. Woolhouse ME, Webster JP, Domingo E, Charlesworth B, Levin BR, (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet 32: 569-577.
37. Swanson WJ, Vacquier VD, (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. Sirot LK, Brockmann HJ, (2001) Costs of sexual interactions to females in Rambur's forktail damselfly, Ischnura ramburi (Zygoptera: Coenagrionidae). Animal Behaviour 61: 415-424.
41. Saetre G-P, Slagsvold T, (1996) The significance of female mimicry in male contests. American Naturalist 147: 981-995.
42. Muller MN, Wrangham R, (2002) Sexual mimicry in hyenas. Q Rev Biol 77: 3-16.
43. Robertson HM, (1985) Female dimorphism and mating behavior in a damselfly, Ischnura ramburi: females mimicking males. Animal Behaviour 33: 805-809.
44. Mantovani A, Locati M, Vecchi A, Sozzani S, Allavena P, (2001) Decoy receptors: a strategy to regulate inflammatory cytokines and chemokines. Trends Immunol 22: 328-336.
45. Force A, Lynch M, Pickett FB, Amores A, Yan YL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
46. Yang Z, Swanson WJ, Vacquier VD, (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. Clark NL, Alani E, Aquadro CF, (2012) Evolutionary rate covariation reveals shared functionality and co-expression of genes. Genome Research.
48. Yang Z, Nielsen R, (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. Yang Z, Wong WS, Nielsen R, (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
52. Schrodinger LLC, (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
53. Kresge N, Vacquier VD, Stout CD, (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. Chinowsky TM, Soelberg SD, Baker P, Swanson NR, Kauffman P, et al. (2007) Portable 24-analyte surface plasmon resonance instruments for rapid, versatile biodetection. Biosens Bioelectron 22: 2268-2275.
55. Vacquier VD, Lee YH, (1993) Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1: 181-196.
56. Hayashi TI, Vose M, Gavrilets S, (2007) Genetic differentiation by sexual conflict. Evolution 61: 516-529.