Characterization and comparative analysis of transcriptional profiles of porcine colostrum and mature milk at different parities

Authors: Keel, Brittney; Lindholm-Perry, Amanda; Oliver, William; Wells, James - Jim; Jones, Shuna; Rempel, Lea

Submitted to: BMC Genomic Data
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/29/2021
Publication Date: 8/10/2021
Citation: Keel, B.N., Lindholm-Perry, A.K., Oliver, W.T., Wells, J.E., Jones, S.A., Rempel, L.A. 2021. Characterization and comparative analysis of transcriptional profiles of porcine colostrum and mature milk at different parities. BMC Genomic Data. 22. Article 25. https://doi.org/10.1186/s12863-021-00980-5.
DOI: https://doi.org/10.1186/s12863-021-00980-5

Interpretive Summary: Piglet growth and survival are critical to the swine industry. Progeny born to primiparous sows (gilts) are born lighter, grow slower, and have higher mortality rates than those born to multiparous sows. It has been hypothesized that differences in lifetime performance between gilt progeny and sow progeny may be due to differences in lactation performance. A limited number of transcriptomic studies related to porcine milk production have been reported. ARS scientists performed RNA-sequencing on porcine colostrum and mature milk samples, from dams in parities one through four, in order to characterize gene expression differences between colostrum and mature milk, as well as differences in gene expression across sow parities. A total of 44,234 transcripts were identified in the samples. These included 41,875 transcripts that have previously been annotated in the swine genome and 2,359 novel transcripts. Fifty genes were determined to be differentially expressed between colostrum and mature milk samples, regardless of parity, and 468 genes were found to be significantly different between colostrum and mature milk across parity. Many of these genes are involved in pathogen recognition and immune response. This is the first study to describe the whole milk transcriptomic profile of porcine colostrum and milk across multiple parities. Findings from the study have produced several highly specialized and functional candidate genes that may contribute to postnatal development and growth of piglets, as well as lactation in the sow.

Technical Abstract: Background: Porcine milk is a complex fluid, containing a myriad of immunological, biochemical, and cellular components, made to satisfy the nutritional requirements of the neonate. Whole milk contains many different cell types, including mammary epithelial cells, neutrophils, macrophages, and lymphocytes, as well nanoparticles, such as milk exosomes. To-date, only a limited number of livestock transcriptomic studies have reported sequencing of milk. Moreover, those studies focused only on sequencing somatic cells as a proxy for the mammary gland with the goal of investigating differences in the lactation process. Recent studies have indicated that RNA originating from multiple cell types present in milk can withstand harsh environments, such as the digestive system, and transmit regulatory molecules from maternal to neonate. Transcriptomic profiling of porcine whole milk, which is reflective of the combined cell populations, could help elucidate these mechanisms. To this end, total RNA from colostrum and mature milk samples were sequenced from 65 sows at differing parities. A stringent bioinformatic pipeline was used to identify and characterize 70,841 transcripts. Results: The 70,841 identified transcripts included 42,733 previously annotated transcripts and 28,108 novel transcripts. Differential gene expression analysis was conducted using a generalized linear model coupled with the Lancaster method for P-value aggregation across transcripts. In total, 1667 differentially expressed genes (DEG) were identified for the milk type main effect, and 33 DEG were identified for the milk type x parity interaction. Several gene ontology (GO) terms related to immune response were significant for the milk type main effect, supporting the well-known fact that immunoglobulins and immune cells are transferred to the neonate via colostrum. Conclusions: This is the first study to perform global transcriptome analysis from whole milk samples in sows from different parities. Our results provide important information and insight into synthesis of milk proteins and innate immunity and potential targets for future improvement of swine lactation and piglet development.