Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries

Gert, Krista R; Panser, Karin; Surm, Joachim M.; Steinmetz, Benjamin; Schleiffer, Alexander; Jovine, Luca; Moran, Yehu; Kondrashov, Fyodor A.; Pauli, Andrea

doi:10.1038/s41467-023-39317-4

Cited by 10 publications

(3 citation statements)

References 88 publications

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“…In other organisms like zebrafish or nematodes, IZUMO1 orthologs were described ( Binner et al, 2021 ; Nishimura et al, 2015 ; Takayama et al, 2021 ) but, since JUNO is present only in mammals ( Vance and Lee, 2020 ; Grayson, 2015 ), it is unclear whether male gametes in other species interact with different receptors on the female gamete. Therefore, it can be speculated, for instance, that the expression of a species-specific Bouncer will be required to activate the fusion of fish sperm ( Gert et al, 2023 ; Herberg et al, 2018 ) or Chlamydomonas FUS1 to mediate the fusion of the algae minus gamete ( Pinello et al, 2021 ; Ferris et al, 1996 ).…”

Section: Discussionmentioning

confidence: 99%

Sperm induction of somatic cell-cell fusion as a novel functional test

Brukman,

Valansi,

Podbilewicz

2024

eLife

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The fusion of mammalian gametes requires the interaction between IZUMO1 on the sperm and JUNO on the oocyte. We have recently shown that ectopic expression of mouse IZUMO1 induces cell-cell fusion and that sperm can fuse to fibroblasts expressing JUNO. Here, we found that the incubation of mouse sperm with hamster fibroblasts or human epithelial cells in culture induces the fusion between these somatic cells and formation of syncytia, a pattern previously observed with some animal viruses. This sperm-induced cell-cell fusion requires a species-matching JUNO on both fusing cells, can be blocked by an antibody against IZUMO1, and does not rely on the synthesis of new proteins. The fusion is dependent on the sperm's fusogenic capacity, making this a reliable, fast and simple method for predicting sperm function during the diagnosis of male infertility.

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Section: Discussionmentioning

confidence: 99%

Sperm induction of somatic cell-cell fusion as a novel functional test

Brukman,

Valansi,

Podbilewicz

2024

eLife

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“…Given that successful fertilization relies on the molecular compatibility between gametes, as long as sperm and egg can recognize and bind via their surface proteins, gamete fusion is possible between individuals of different species. This would be permissive of hybridization events possibly impacting speciation processes (Gert et al, 2023). From a conservation perspective it also means that declining small populations like jaguars in Argentina could be susceptible to hybridization, though on the other hand future efforts to enrich local gene pools by assisted migration from different conspecific populations - if considered necessary - would not be hampered by gamete incompatibility (Hoffmann et al 2021; Johnson et al 2010).…”

Section: Discussionmentioning

confidence: 99%

Positive selection in gamete interaction proteins inCarnivora

Pisciottano

Campos

Penna

et al. 2022

Preprint

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The jaguar (Panthera onca) is the most relevant predator in South America and an endangered species in Argentina. Therefore genomic, evolutionary and functional studies of this species are strategic to gain biological insights and support conservation efforts. With the advent of sequencing advances the study of relevant character species evolution has to be revisited. Recent comparative genomic analysis revealed a long history of hybridization among extant big cats, which indicates an absence of inter-specific isolation barriers. We aimed to uncover the molecular basis of this interspecies crossing and the evolution of the functional capacities of pantherine gamete interaction Zona Pellucida proteins (ZP) and JUNO. Hi-C long-range sequencing and chromosome-resolved jaguar genome assembly was used to resolve ZP genes loci and reconstruct the evolutionary history of these proteins. Exploring sequence variability in more that 30 Carnivora species, Feliforme and Caniforme sister groups show significant differences in average sequence identity for all studied proteins except ZP4, always showing Caniformes as a more diverse group than Feliformes. Molecular evolution of ZP isoforms involved in sperm-recognition, ZP3 and ZP2, showed similar phylogenetic histories, displaying signatures of positive selection among Carnivores and Caniformes, but not among Pantherines or Feliformes. On the other hand, structural cross-linking ZP subunits, ZP1 and ZP4, displayed a different evolutionary history. The fusion protein IZUMO1R was found to be highly conserved in all studied phylogenetic groups. These results strengthen the idea that ZPs are proteins more related to specific-specificity isolation than IZUMO1R, which is specialized in fusion events. Altogether, our findings indicate that sperm-oocyte interaction and fusion proteins lack the degree of diversification necessary to establish a prezygotic reproductive isolation barrier between pantherines, which would explain observed reticulated patterns of evolution in this clade.

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“…Given that successful fertilisation relies on the molecular compatibility between gametes, as long as sperm and egg can recognise and bind via their surface proteins, gamete fusion is possible between individuals of different species. This would be permissive of hybridisation events possibly impacting speciation processes (Gert et al, 2023). From a conservation perspective it also means that declining small populations like jaguars in Argentina could be susceptible to hybridisation, though on the other hand future efforts to enrich local gene pools by assisted migration from different conspecific populations-if considered necessary-would not be hampered by gamete incompatibility (Hoffmann et al, 2021;Johnson et al, 2010).…”

Section: Final Con Clus Ionsmentioning

confidence: 99%

Positive selection in gamete interaction proteins in Carnivora

Pisciottano,

Campos,

Penna

et al. 2024

Molecular Ecology

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The absence of robust interspecific isolation barriers among pantherines, including the iconic South American jaguar (Panthera onca), led us to study molecular evolution of typically rapidly evolving reproductive proteins within this subfamily and related groups. In this study, we delved into the evolutionary forces acting on the zona pellucida (ZP) gamete interaction protein family and the sperm‐oocyte fusion protein pair IZUMO1‐JUNO across the Carnivora order, distinguishing between Caniformia and Feliformia suborders and anticipating few significant diversifying changes in the Pantherinae subfamily. A chromosome‐resolved jaguar genome assembly facilitated coding sequences, enabling the reconstruction of protein evolutionary histories. Examining sequence variability across more than 30 Carnivora species revealed that Feliformia exhibited significantly lower diversity compared to its sister taxa, Caniformia. Molecular evolution analyses of ZP2 and ZP3, subunits directly involved in sperm‐recognition, unveiled diversifying positive selection in Feliformia, Caniformia and Pantherinae, although no significant changes were linked to sperm binding. Structural cross‐linking ZP subunits, ZP4 and ZP1 exhibited lower levels or complete absence of positive selection. Notably, the fusion protein IZUMO1 displayed prominent positive selection signatures and sites in basal lineages of both Caniformia and Feliformia, extending along the Caniformia subtree but absent in Pantherinae. Conversely, JUNO did not exhibit any positive selection signatures across tested lineages and clades. Eight Caniformia‐specific positive selected sites in IZUMO1 were detected within two JUNO‐interaction clusters. Our findings provide for the first time insights into the evolutionary trajectories of ZP proteins and the IZUMO1‐JUNO gamete interaction pair within the Carnivora order.

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Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries

Cited by 10 publications

References 88 publications

Sperm induction of somatic cell-cell fusion as a novel functional test

Sperm induction of somatic cell-cell fusion as a novel functional test

Positive selection in gamete interaction proteins inCarnivora

Positive selection in gamete interaction proteins in Carnivora

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