Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein

Vacquier, Victor D.; Lee, Youn-Ho

doi:10.1017/s0967199400001465

Cited by 80 publications

(57 citation statements)

References 48 publications

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“…Neubaum & Wolfner 1999) in identifying possible interactions in other seminal products. Variations in male reproductive traits are well documented (Anderson 1982;Houde 1987;Basolo 1998) and, while the direct contributions of sperm in gametic incompatibilities have not been previously measured, variation in the sea urchin sperm protein bindin has recently been reported (Vacquier & Lee 1993;Palumbi 1999). Females of the sea urchin genus Echinomerta can fertilize eggs assortatively based on di¡er-ences in bindin genotype, which appears to be polymorphic within a species (Palumbi 1999).…”

Section: Discussionmentioning

confidence: 99%

Gametic incompatibilities between races ofDrosophila melanogaster

Alipaz

Wu²,

Karr

2001

Proc. R. Soc. Lond. B

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Reproductive-isolating mechanisms between nascent species may involve sperm^egg recognition and have been best described in externally fertilizing organisms where such recognition is essential in preventing undesirable fertilizations. However, reproductive barriers in internally fertilizing species di¡er in signi¢cant ways, and a direct role for sperm^egg interactions has yet to be demonstrated. Females of many strains of Drosophila melanogaster from Zimbabwe, Africa, do not mate readily with cosmopolitan males. This polymorphism in mate choice is postulated to represent incipient speciation. We now report that, in one direction, crosses between the above populations produce far fewer o¡spring than reciprocal crosses due to a lower rate of egg hatch. We established that egg inviability in these crosses was due to defects in fertilization. Thus, even in taxa with internal fertilization, gametic incompatibility may be a mechanism relevant to reproductive isolation during incipient speciation.

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Section: Discussionmentioning

confidence: 99%

Gametic incompatibilities between races ofDrosophila melanogaster

Alipaz

Wu²,

Karr

2001

Proc. R. Soc. Lond. B

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“…Sequence comparison of triA and atzA indicates a lack of silent mutations, suggesting that strong selective pressure occurred relatively quickly (18,42). Moreover, the 9 amino acid differences are positioned throughout the proteins, indicating that catalytic differences are most likely not due to an alteration in tertiary structure but rather due to localized changes.…”

Section: Discussionmentioning

confidence: 99%

Melamine Deaminase and Atrazine Chlorohydrolase: 98 Percent Identical but Functionally Different

et al. 2001

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The gene encoding melamine deaminase (TriA) from Pseudomonas sp. strain NRRL B-12227 was identified, cloned into Escherichia coli, sequenced, and expressed for in vitro study of enzyme activity. Melamine deaminase displaced two of the three amino groups from melamine, producing ammeline and ammelide as sequential products. The first deamination reaction occurred more than 10 times faster than the second. Ammelide did not inhibit the first or second deamination reaction, suggesting that the lower rate of ammeline hydrolysis was due to differential substrate turnover rather than product inhibition. Remarkably, melamine deaminase is 98% identical to the enzyme atrazine chlorohydrolase (AtzA) from Pseudomonas sp. strain ADP. Each enzyme consists of 475 amino acids and differs by only 9 amino acids. AtzA was shown to exclusively catalyze dehalogenation of halo-substituted triazine ring compounds and had no activity with melamine and ammeline. Similarly, melamine deaminase had no detectable activity with the halo-triazine substrates. Melamine deaminase was active in deamination of a substrate that was structurally identical to atrazine, except for the substitution of an amino group for the chlorine atom. Moreover, melamine deaminase and AtzA are found in bacteria that grow on melamine and atrazine compounds, respectively. These data strongly suggest that the 9 amino acid differences between melamine deaminase and AtzA represent a short evolutionary pathway connecting enzymes catalyzing physiologically relevant deamination and dehalogenation reactions, respectively.

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“…In sea urchins (1, 2) and abalone (3,4), several closely related, congeneric species may have overlapping breeding seasons and habitats. Such species usually exhibit species selectivity (specificity) in experimental cross-fertilizations, meaning that fertilization occurs more readily between homospecific mixtures of sperm and eggs than between heterospecific mixtures.…”

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confidence: 99%

The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

Swanson

Vacquier

1997

Proc. Natl. Acad. Sci. U.S.A.

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114

149

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Abalone sperm lysin is a 16-kDa acrosomal protein, which nonenzymatically and species selectively creates a hole in the egg vitelline envelope (VE) through which the sperm passes to reach the egg cell membrane. The crystal structures of both monomeric and dimeric lysins have been solved and the sequences of lysins from 20 abalone species have been determined. As a first step in understanding the molecular mechanism by which lysin creates a hole in the VE, its VE receptor was isolated. The VE receptor for lysin (VERL) is an unbranched, rod-like molecule with an approximate relative molecular mass of 2 million; half the mass being carbohydrate. Fluorescence polarization studies showed positive cooperativity in the binding of lysin to VERL (EC 50 Ϸ9 nM) and were consistent with the species selectivity of lysin in dissolving VEs. Each molecule of VERL bound between 126 and 142 molecules of monomeric lysin (two independent assays), showing that VERL possesses repetitive lysin-binding motifs.Many marine invertebrate species spawn gametes into seawater, where fertilization and embryogenesis occur. In sea urchins (1, 2) and abalone (3, 4), several closely related, congeneric species may have overlapping breeding seasons and habitats. Such species usually exhibit species selectivity (specificity) in experimental cross-fertilizations, meaning that fertilization occurs more readily between homospecific mixtures of sperm and eggs than between heterospecific mixtures. The demonstrated species selectivity in the recognition events between invertebrate sperm and egg is a valuable model bearing on the general problem of the biochemistry of molecular recognition between cells.In marine invertebrates, the study of gamete recognition proteins may also yield information on the mechanism by which species arise in the sea, where barriers to larval transport are not readily apparent (5). Evidence that gamete recognition proteins may be involved in speciation comes from analyses of nucleotide substitutions in sea urchin sperm bindins (1) and abalone sperm acrosomal proteins (4, 6). Such analyses show that the evolution of these proteins has been promoted by positive Darwinian selection, suggesting there is significant adaptive value in altering their primary structure.The availability of large quantities of marine invertebrate gametes permits a detailed characterization of their gamete surface molecules involved in fertilization. The abalone egg is surrounded by an elevated, glycoproteinaceous vitelline envelope (VE) 0.6 m in diameter (7,8). Spermatozoa bind to the VE, their acrosomal granule exocytoses, and lysin is released. Lysin creates a 3-m diameter hole in the VE through which the spermatozoan passes to reach the egg cell membrane. Electron micrographs of the lysin-created hole show it is composed of splayed-apart fibers of 13-nm diameter; covalent bonds are not broken when lysin disrupts the VE (7).Although gamete recognition proteins have been cloned from both mammals (9-13) and invertebrates (1-4, 6, 14-16), the molec...

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Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein

Cited by 80 publications

References 48 publications

Gametic incompatibilities between races ofDrosophila melanogaster

Gametic incompatibilities between races ofDrosophila melanogaster

Melamine Deaminase and Atrazine Chlorohydrolase: 98 Percent Identical but Functionally Different

The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule

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