A protein-coding gene expression atlas from the brain of pregnant and non-pregnant goats

Front Genet. 2023 Jul 14:14:1114749. doi: 10.3389/fgene.2023.1114749. eCollection 2023.

Abstract

Background: The brain is an extraordinarily complex organ with multiple anatomical structures involved in highly specialized functions related with behavior and physiological homeostasis. Our goal was to build an atlas of protein-coding gene expression in the goat brain by sequencing the transcriptomes of 12 brain regions in seven female Murciano-Granadina goats, from which three of them were 1-month pregnant. Results: Between 14,889 (cerebellar hemisphere) and 15,592 (pineal gland) protein-coding genes were expressed in goat brain regions, and most of them displayed ubiquitous or broad patterns of expression across tissues. Principal component analysis and hierarchical clustering based on the patterns of mRNA expression revealed that samples from certain brain regions tend to group according to their position in the anterior-posterior axis of the neural tube, i.e., hindbrain (pons and medulla oblongata), midbrain (rostral colliculus) and forebrain (frontal neocortex, olfactory bulb, hypothalamus, and hippocampus). Exceptions to this observation were cerebellum and glandular tissues (pineal gland and hypophysis), which showed highly divergent mRNA expression profiles. Differential expression analysis between pregnant and non-pregnant goats revealed moderate changes of mRNA expression in the frontal neocortex, hippocampus, adenohypophysis and pons, and very dramatic changes in the olfactory bulb. Many genes showing differential expression in this organ are related to olfactory function and behavior in humans. Conclusion: With the exception of cerebellum and glandular tissues, there is a relationship between the cellular origin of sampled regions along the anterior-posterior axis of the neural tube and their mRNA expression patterns in the goat adult brain. Gestation induces substantial changes in the mRNA expression of the olfactory bulb, a finding consistent with the key role of this anatomical structure on the development of maternal behavior.

Keywords: RNA-Seq; differential gene expression (DGE); embryonic vesicle; encephalon; gestation; goat.

Grants and funding

This research was funded by the European Regional Development Fund (FEDER)/Ministerio de Ciencia e Innovación—Agencia Estatal de Investigación/Project Reference grants: AGL2016-76108-R and also by project PID2019-105805RB-I00 funded by MCIN/AEI/10.13039/501100011033. We also acknowledge the support of the CERCA Programme/Generalitat de Catalunya and of the Spanish Ministry of Economy and Competitivity for the Center of Excellence Severo Ochoa 2020-2023 (CEX2019-000902-S) grant awarded to the Centre for Research in Agricultural Genomics (CRAG, Bellaterra, Spain). Maria Luigi-Sierra was funded with a PhD fellowship “Formación de Personal Investigador” (BES-2017-079709) awarded by the Spanish Ministry of Economy and Competitivity and by “ESF Investing in your future”. Dailu Guan was funded by a PhD fellowship from the China Scholarship Council (CSC). Emilio Mármol-Sánchez was funded with a FPU Ph.D. grant from the Spanish Ministry of Education (FPU15/01733).