Bainbridge RE et al. (2025), Genomic Insights into Fertilization: Tracing PL...

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Genome Biol Evol 2025 Apr 03;174:. doi: 10.1093/gbe/evaf052.

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Genomic Insights into Fertilization: Tracing PLCZ1 Orthologs Across Amphibian Lineages.

Bainbridge RE , Rosenbaum JC , Sau P , Carlson AE .

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Fertilization triggers a cascade of events, including a rise in egg cytosolic calcium that marks the onset of embryonic development. In mammals and birds, this critical process is mediated by the sperm-derived phospholipase C zeta (PLCζ), which is pivotal in releasing calcium from the endoplasmic reticulum in the egg and initiating embryonic activation. Intriguingly, Xenopus laevis, a key model organism in reproductive biology, lacks an annotated PLCZ1 gene, prompting questions about its calcium release mechanism during fertilization. Using bioinformatics and RNA sequencing of adult X. laevis testes, we investigated the presence of a PLCZ1 ortholog in amphibians. While we identified PLCZ1 homologs in 25 amphibian species, including 14 previously uncharacterized orthologs, we found none in X. laevis or its close relative, Xenopus tropicalis. Additionally, we found no compensatory expression of other PLC isoforms in these species. Synteny analysis revealed a PLCZ1 deletion in species within the Pipidae family and another intriguing deletion of potential sperm factor PLCD4 in the mountain slow frog, Nanorana parkeri. Our findings indicate that the calcium release mechanism in frog eggs involves a signaling pathway distinct from the PLCζ-mediated process observed in mammals.

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Species referenced: Xenopus laevis Xenopus borealis
Genes referenced: astl2b cfh dazl h1-10 hormad1 pbk plcb1 plcb3 plcd1 plcd3 plcd4 plcg1 rflcii ribc1 sycp3 syngr4 tubb4b

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	Fig. 1. Identification of amphibian PLCζ isozymes and characterization of PLC orthologs in amphibians. (A) Cladogram illustrating the occurrence of PLCZ1 orthologs in amphibian species. Annotated orthologs are colored black, orthologs identified in transcriptome assemblies are blue, those identified in WGS assemblies are pink, and species missing orthologs are orange. (B) Unrooted phylogram illustrating the alignment of newly identified PLCZ1 orthologs (pink) with annotated amphibian PLCs. Bootstrap support values for branching at the PLCZ node are highlighted.
	Fig. 2. Synteny analysis of PLCZ1 and PLD4 loci. (A) Local synteny comparison around the PLCZ1 locus suggests its deletion in species from the Pipidae family. The chromosome source for each block is noted in parentheses. Blocks marked with an symbol have had their order reversed for clarity. Species with an asterisk (*) signify incomplete assemblies for that region, with coverage and annotation methods detailed in table 3. (B) The local synteny comparison for the PLCD4 locus indicates a deletion in Nanorana parkeri.
	Fig. 3. Expression heatmap of sperm factors in anuran and mouse testis. (A) Comparison of transcript counts between this study and previous ones (Session, et al. 2016); Spearman rank correlation shown for each comparison is shown at the bottom. (B) Heatmaps depicting the expression levels of annotated PLC genes from the specified animals, displayed as log2 transformed transcripts per million. Grey boxes indicate transcripts lacking annotation. For anurans, plcz1 is highlighted in red to emphasize its absence from Xenopus. The putative sperm factor wbp2nl is also included for reference. The X. laevis (outbred) data is from this study, X. laevis (J strain) from GSE73419 (Session, et al. 2016), X. tropicalis from GSM5230669 (unpublished), B. orientalis from GSE163874 (unpublished), and 3-month-old mice from GSE181426 (Huang, et al. 2021).