Bos taurus-indicus hybridization correlates with intralocus sexual-conflicting effects of PRDM9 on male and female fertility in Holstein cattle

Authors: SEROUSSI, EYAL - Agricultural Research Organization Of Israel; SHIRAK, ANDREY - Agricultural Research Organization Of Israel; GERSHONI, MORAN - Agricultural Research Organization Of Israel; EZRA, EPHRAIM - Collaborator; SANTOS, DANIEL - University Of Maryland; MA, LI - University Of Maryland; Liu, Ge - George

Submitted to: BMC Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/21/2019
Publication Date: 8/28/2019
Citation: Seroussi, E., Shirak, A., Gershoni, M., Ezra, E., Santos, D.J., Ma, L., Liu, G. 2019. Bos taurus-indicus hybridization correlates with intralocus sexual-conflicting effects of PRDM9 on male and female fertility in Holstein cattle. BMC Genetics. 20:71. https://doi.org/10.1186/s12863-019-0773-5.
DOI: https://doi.org/10.1186/s12863-019-0773-5

Interpretive Summary: Recombination during meiosis is facilitated by chromosomal crossover. Using computational and experimnatl methods, we found PRDM9 alleles that had the negative impact on male fertility had the most positive effects on female fertility traits. These results fill our knowledge gaps and provide the foundation for future studies of recombination's functional role in genome evolution and selection. Farmers, scientist, and policy planners who need improve animal health and production based on genome-enable animal selection will benefit from this study.

Technical Abstract: Background: Crossover-localization during meiotic recombination is mediated by the fast-evolving zinc-finger (ZF) domain of the PRDM9 gene. To study its impact on the dairy cattle performance, we compared its genetic variation between the relative small Israeli (IL) and the North American (US) Holstein that count millions. Results: Initially, we analyzed the major BTA1 haplotypes present in Israeli Holsteins based on the 10 most telomeric SNPs of BovineSNP50 BeadChip. Sequencing of representative haplotype-carriers indicated that for all frequent haplotypes (> 6%) the PRDM9 variable ZF-array consisted of seven tandem ZnF-repeats. Two rare haplotypes (frequency < 4%) carried an indicine PRDM9, while all others were variants of the taurine type. These two haplotypes included the minor SNP allele, which was perfectly linked with a previously described PRDM9 allele known to induce unique localization of recombination hotspots. One of them had a significant (p = 0.03) negative effect on IL sire fertility. This haplotype combined the rare minor alleles of the only SNPs with significant (p < 0.05) negative substitution effects on US sire fertility (SCR). Analysis of telomeric SNPs indicated general agreement of allele frequencies (R = 0.95) and of the substitution effects on sire fertility (SCR, R = 0.6) between the US and IL samples. Surprisingly, the alleles that had the negative impact on male fertility had the most positive substitution effects on female fertility traits (DPR, CCR and HCR). Conclusions: Negative genetic correlation between male and female fertility is encoded within the BTA1 telomere. Cloning the taurine PRDM9 gene, which is the common form carried by Holsteins, we encountered the infiltration of an indicine PRDM9 variant into this population. During meiosis, in heterozygote males, indicine PRDM9 variant may induce incompatibility of recombination hotspots and male infertility. However, this variant is associated with a favorable female fertility, which can explain its survival and the general negative correlation (R = -0.3) that was observed between male and female fertility in US Holsteins. Further research is needed to explain the mechanism behind this positive effect and how to devise a methodology to unlink it from the negative effect on male fertility during breeding.