Multi-Tissue Omics Analyses Reveal Molecular Regulatory Networks for Puberty in Composite Beef Cattle

Cánovas, Ángela; Reverter, Antônio; DeAtley, K. L.; Ashley, Ryan L.; Colgrave, Michelle L.; Fortes, M. R. S.; Islas‐Trejo, Alma; Lehnert, S. A.; Porto-Neto, Laércio R.; Rincón, Gonzalo; Silver, G. A.; Snelling, W. M.; Medrano, Juan F.; Thomas, M. G.

doi:10.1371/journal.pone.0102551

Cited by 122 publications

(159 citation statements)

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“…Heifers were handled and managed as per approval of the Institutional Animal Care and Use Committee of New Mexico State University (protocol #2010-013; Cánovas et al, 2014). Eight heifers representing the pedigree diversity of the population used in genome-wide association study (GWAS) of fertility traits were selected from a Brangus (3/8 Brahman x 5/8 Angus) cattle breeding program .…”

Section: Discovery Populationmentioning

confidence: 99%

“…RNA extraction, library construction, and sequencing were performed for each tissue and animal as described by Cánovas et al (2014). Additionally, libraries were multiplexed, six libraries per lane, and sequenced with an Illumina HiSeq 2000 analyzer.…”

Section: Discovery Populationmentioning

confidence: 99%

“…Table 1. Genes harboring SNPs associated with heifer fertility either differentially expressed or with tissue-specific expression in RNA-Seq analysis in pre-and post-pubertal Brangus heifers (adapted from Cánovas et al, 2014 …”

Section: Candidate Genesmentioning

confidence: 99%

“…SNP discovery analysis within RNA from fibroblasts of Holstein calves revealed 728 SNPs within 31 genes, with an average of 23.5 ± 5.9 SNPs per gene. Four genes contained one SNP The studies involving Brangus and Brahman cattle were the only ones designed to specifically study differences between pre and post-pubertal animals (Fortes et al, 2012;Cánovas et al, 2014;Fortes et al, 2016). These are the only breeds from which RNA was extracted from tissues associated with reproduction.…”

Section: Genes In Which No Snps Were Detected Included Cdx2 Dppa4 Ementioning

confidence: 99%

“…Since publication of the bovine reference genome in 2009 (Elsik et al, 2009), development and increased knowledge of the -"omics" technologies have accelerated the investigation of the genetic regulation of bovine fertility traits (Fortes et al, 2012;Snelling et al, 2013;Cánovas et al, 2014, Nascimento et al, 2016. Moreover, it is important to delineate candidate genes and to determine whether polymorphisms exist within genes that influence these traits.…”

Section: Introductionmentioning

confidence: 99%

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SNP detection using RNA-sequences of candidate genes associated with puberty in cattle

et al. 2017

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ABSTRACT. Fertility traits, such as heifer pregnancy, are economically important in cattle production systems, and are therefore, used in genetic selection programs. The aim of this study was to identify single nucleotide polymorphisms (SNPs) using RNA-sequencing (RNA-Seq) data from ovary, uterus, endometrium, pituitary gland, hypothalamus, liver, longissimus dorsi muscle, and adipose tissue in 62 candidate genes associated with heifer puberty in cattle. RNA-Seq reads were assembled to the bovine reference genome (UMD 3.1.1) and analyzed in five cattle breeds; Brangus, Brahman, Nellore, Angus, and Holstein. Two approaches used the Brangus data for SNP discovery 1) pooling all samples, and 2) within each individual sample. These approaches revealed 1157 SNPs. These were compared with those identified in the pooled samples of the other breeds. Overall, 172 SNPs within 13 genes (CPNE5, FAM19A4, FOXN4, KLF1, LOC777593, MGC157266, NEBL, NRXN3, PEPT-1, PPP3CA, SCG5, TSG101, and TSHR) were concordant in the five breeds. Using Ensembl's Variant Effector Predictor, we determined that 12% of SNPs were in exons (71% synonymous, 29% nonsynonymous), 1% were in untranslated regions (UTRs), 86% were in introns, and 1% were in intergenic regions. Since these SNPs were discovered in RNA, the variants were predicted to be within exons or UTRs. Overall, 160 novel transcripts in 42 candidate genes and five novel genes overlapping five candidate genes were observed. In conclusion, 1157 SNPs were identified in 62 candidate genes associated with puberty in Brangus cattle, of which, 172 were concordant in the five cattle breeds. Novel transcripts and genes were also identified.

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Section: Discovery Populationmentioning

confidence: 99%

Section: Discovery Populationmentioning

confidence: 99%

Section: Candidate Genesmentioning

confidence: 99%

Section: Genes In Which No Snps Were Detected Included Cdx2 Dppa4 Ementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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SNP detection using RNA-sequences of candidate genes associated with puberty in cattle

et al. 2017

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Investigating the role of genetic variation in vgll3 and six6 in the domestication of gilthead seabream (Sparus aurata Linnaeus) and European seabass (Dicentrarchus labrax Linnaeus)

Moulistanos,

Nikolaou,

Sismanoglou

et al. 2023

Ecology and Evolution

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Gene function conservation is crucial in molecular ecology, especially for key traits like growth and maturation in teleost fish. The vgll3 and six6 genes are known to influence age‐at‐maturity in Atlantic salmon, but their impact on other fish species is poorly understood. Here, we investigated the association of vgll3 and six6 in the domestication of gilthead seabream and European seabass, both undergoing selective breeding for growth‐related traits in the Mediterranean. We analysed two different sets of samples using two different genotyping approaches. The first dataset comprised farmed and wild populations from Greece, genotyped for SNPs within the two genes (‘gene‐level genotyping’). The second dataset examined 300–600 k SNPs located in the chromosomes of the two genes, derived from a meta‐analysis of a Pool‐Seq experiment involving farmed and wild populations distributed widely across the Mediterranean (‘chromosome‐level genotyping’). The gene‐level analysis revealed a statistically significant allele frequency differences between farmed and wild populations on both genes in each species. This finding was partially supported by the chromosome‐level analysis, identifying highly differentiated regions may be involved in the domestication process at varying distances from the candidate genes. Noteworthy genomic features were found, such as a CpG island in gilthead seabream and novel candidate genes in European seabass, warranting further investigation. These findings support a putative role of vgll3 and six6 in the maturation and growth of gilthead seabream and European seabass, emphasizing the need for further research on their conserved function.

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Gene regulation could be attributed to TCF3 and other key transcription factors in the muscle of pubertal heifers

Lau

Nguyen

Reverter

et al. 2020

Veterinary Medicine & Sci

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Puberty is a whole‐body event, driven by the hypothalamic integration of peripheral signals such as leptin or IGF‐1. In the process of puberty, reproductive development is simultaneous to growth, including muscle growth. To enhance our understanding of muscle function related to puberty, we performed transcriptome analyses of muscle samples from six pre‐ and six post‐pubertal Brahman heifers (Bos indicus). Our aims were to perform differential expression analyses and co‐expression analyses to derive a regulatory gene network associate with puberty. As a result, we identified 431 differentially expressed (DEx) transcripts (genes and non‐coding RNAs) when comparing pre‐ to post‐pubertal average gene expression. The DEx transcripts were compared with all expressed transcripts in our samples (over 14,000 transcripts) for functional enrichment analyses. The DEx transcripts were associated with “extracellular region,” “inflammatory response” and “hormone activity” (adjusted p < .05). Inflammatory response for muscle regeneration is a necessary aspect of muscle growth, which is accelerated during puberty. The term “hormone activity” may signal genes that respond to progesterone signalling in the muscle, as the presence of this hormone is an important difference between pre‐ and post‐pubertal heifers in our experimental design. The DEx transcript with the highest average expression difference was a mitochondrial gene, ENSBTAG00000043574 that might be another important link between energy metabolism and puberty. In the derived co‐expression gene network, we identified six hub genes: CDC5L, MYC, TCF3, RUNX2, ATF2 and CREB1. In the same network, 48 key regulators of DEx transcripts were identified, using a regulatory impact factor metric. The hub gene TCF3 was also a key regulator. The majority of the key regulators (22 genes) are members of the zinc finger family, which has been implicated in bovine puberty in other tissues. In conclusion, we described how puberty may affect muscle gene expression in cattle.

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Multi-Tissue Omics Analyses Reveal Molecular Regulatory Networks for Puberty in Composite Beef Cattle

Cited by 122 publications

References 95 publications

SNP detection using RNA-sequences of candidate genes associated with puberty in cattle

SNP detection using RNA-sequences of candidate genes associated with puberty in cattle

Investigating the role of genetic variation in vgll3 and six6 in the domestication of gilthead seabream (Sparus aurata Linnaeus) and European seabass (Dicentrarchus labrax Linnaeus)

Gene regulation could be attributed to TCF3 and other key transcription factors in the muscle of pubertal heifers

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