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Genomic Structure and Marker-Derived Gene Networks for Growth and Meat Quality Traits of Brazilian Nelore Beef Cattle Maurício A

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Genomic Structure and Marker-Derived Gene Networks for Growth and Meat Quality Traits of Brazilian Nelore Beef Cattle Maurício A Mudadu et al. BMC Genomics (2016) 17:235 DOI 10.1186/s12864-016-2535-3 RESEARCH ARTICLE Open Access Genomic structure and marker-derived gene networks for growth and meat quality traits of Brazilian Nelore beef cattle Maurício A. Mudadu1,2*† , Laercio R. Porto-Neto3†, Fabiana B. Mokry4†, Polyana C. Tizioto4, Priscila S. N. Oliveira4, Rymer R. Tullio2, Renata T. Nassu2, Simone C. M. Niciura2, Patrícia Tholon2, Maurício M. Alencar2, Roberto H. Higa1, Antônio N. Rosa5, Gélson L. D. Feijó5, André L. J. Ferraz6, Luiz O. C. Silva5, Sérgio R. Medeiros5, Dante P. Lanna7, Michele L. Nascimento7, Amália S. Chaves7, Andrea R. D. L. Souza8, Irineu U. Packer7ˆ, Roberto A. A. Torres Jr.5, Fabiane Siqueira5, Gerson B. Mourão7, Luiz L. Coutinho7, Antonio Reverter3 and Luciana C. A. Regitano2 Abstract Background: Nelore is the major beef cattle breed in Brazil with more than 130 million heads. Genome-wide association studies (GWAS) are often used to associate markers and genomic regions to growth and meat quality traits that can be used to assist selection programs. An alternative methodology to traditional GWAS that involves the construction of gene network interactions, derived from results of several GWAS is the AWM (Association Weight Matrices)/PCIT (Partial Correlation and Information Theory). With the aim of evaluating the genetic architecture of Brazilian Nelore cattle, we used high-density SNP genotyping data (~770,000 SNP) from 780 Nelore animals comprising 34 half-sibling families derived from highly disseminated and unrelated sires from across Brazil. The AWM/PCIT methodology was employed to evaluate the genes that participate in a series of eight phenotypes related to growth and meat quality obtained from this Nelore sample. Results: Our results indicate a lack of structuring between the individuals studied since principal component analyses were not able to differentiate families by its sires or by its ancestral lineages. The application of the AWM/PCIT methodology revealed a trio of transcription factors (comprising VDR, LHX9 and ZEB1) which in combination connected 66 genes through 359 edges and whose biological functions were inspected, some revealing to participate in biological growth processes in literature searches. Conclusions: The diversity of the Nelore sample studied is not high enough to differentiate among families neither by sires nor by using the available ancestral lineage information. The gene networks constructed from the AWM/PCIT methodology were a useful alternative in characterizing genes and gene networks that were allegedly influential in growth and meat quality traits in Nelore cattle. Keywords: Genotyping, AWM, PCIT, GWAS * Correspondence: [email protected] †Equal contributors ˆDeceased 1Embrapa Agricultural Informatics, Av. André Tosello, 209, Campinas, SP, Brazil 2Embrapa Southeast Livestock, Rodovia Washington Luiz, Km 234, São Carlos, SP, Brazil Full list of author information is available at the end of the article © 2016 Mudadu et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mudadu et al. BMC Genomics (2016) 17:235 Page 2 of 16 Background samples of Brazilian Nelore cattle, systematically sourced Brazilian livestock began with taurine cattle introduced to represent 34 highly influential sires and their 746 half- from Europe in the colonial period, around 450 years sibs from across Brazil. Further, we inferred a gene ago. Several years later, starting in 1930 but mainly in network focused on growth and meat quality traits 1960 and 1962, a Bos indicus cattle breed named Nelore and found several genes implicated in the regulation was introduced in Brazil from India and the herd of these phenotypes. expanded to the majority of the territory due to its good adaptability to tropical climate. It is estimated that 7000 Results Nelore cattle were introduced from India, the majority Genetic profile of Brazilian Nelore beef cattle were descendants from 6 main sires named Karvadi, Taj After quality control filters we retained genotypes of Mahal, Kurupathy, Golias, Godhavari and Rasta [1]. The 449,203 SNPs for linkage disequilibrium and haplotype Nelore, a breed with white or gray pelage and short block analysis, and 224,969 TagSNPs from 780 Nelore horns, is nowadays the most representative breed in animals, including 34 prominent sires and their 746 Brazil and dominates the Brazilian beef cattle production progeny (Table 1). These genotypes were coupled with with more than 75 % of the total herd which equates to genotypes of the same SNP for a sample of 46 Brahman, more than 130 million heads of Nelore cattle. Artificial Hereford and 44 Angus cattle sourced from the Bovine insemination is widely used in Brazil [2] and semen for HapMap project [17, 18], and used to calculate a genomic only a few sires has been intensively used nationwide. relationship matrix (GRM) that was used in a principal With the advent of the Illumina BovineHD BeadChip component analysis (PCA) [19]. This analysis (Fig. 1a, (Illumina Inc., San Diego, CA), a high density SNP panel inset) shows that the first component, explaining 86 % of comprising over 770,000 markers, we were able to meas- the variation in genotype profiles, separates the taurine ure the genomic diversity of the Brazilian Nelore from (Angus and Hereford) from the indicine (Brahman and the main commercial sire families and characterize their Nelore) breeds, indicating that the genotyping data is genomic relationship and genetic profiles across a series reliable. A GRM considering only the 780 Nelore animals of phenotypes. Traditional phenotype-based selection and the 224,969 TagSNPs was also constructed and used has been focused primarily on improving growth and for a PCA analysis exclusive for the Brazilian Nelore maternal traits [3]. However, marker-assisted or genomic sample. The results for the PCA (Fig. 1a) shows that selection is particularly valuable for traits that have late, although some half-sib families are well distinguished (e.g. onerous and expensive measurement such as meat the NE001383, NE001398 and NE001362 families), the quality, yield and feed efficiency [4]. Despite production bulk of the samples were not well separated by the first advantages of Bos indicus composite breeds in tropical component, indicating a lack of structuring. The first and and subtropical environments, the inferiority of beef second components only explain 8.1 % and 6.8 % of the quality, especially tenderness, is a worrying issue for variation respectively. It is interesting to note in Fig. 1a producers [5, 6]. It is known that Nelore breed show that the distance from a given sire (greater labeled circles) moderate heritability for meat quality [7] as well as for to its corresponding cluster of half-sibs is visually symmet- growth-related traits [8], which make the application of rical to the distance of the half-sib cluster to the center of genomic tools feasible. the figure. We suggest that this effect is due to the Genome-Wide Association Studies, or GWAS, are today randomness diversity of the genetic effect of the dams that a common practice in order to find associations of gen- would bring more related individuals to the center of the ome regions to phenotypes of interest such as meat quality figure, indicating that these sires are less related to its traits[7,9,10].However,GWASaresometimeselusive half-sib families and even less related to the bulk of more regarding the low power of association of the markers related individuals in the center. The average genomic to the trait and also to the association of regions of the inbreeding coefficient from the GRM (FGRM) reports genome that lack apparent relation to the trait being values of 2 % (± 5 % SD) for sires and 0 % (± 3 % SD) for studied [11, 12]. Some meta-analysis approaches are progeny. Also, inbreeding coefficient derived from runs of appealing as they attempt to enrich GWAS analyses homozygosity (FROH) reports values of 9 % (± 5 % SD) with information from other sources. One of these for sires, and 6 % (± 2 % SD) for progeny, showing that methodsisthesystem’s biology AWM/PCIT method- the 34 sires are more inbred than their progeny, and that ology, which involves the construction of SNP-based the random genetic pool from the dams brought more gene network interactions, integrating results from several variability into this sample. The distribution of these GWAS by means of the Association Weight Matrices inbreeding coefficients (FGRM and FROH) can be seen in (AWM) and Partial Correlation and Information Theory Fig. 2. Additional file 1: Figure S1C depicts the pedigree (PCIT) [13–16]. We took advantage of this methodology with the information of the dams showing that some dams to explore growth and meat quality traits from 780 participate in more than one family. Mudadu et al. BMC Genomics (2016) 17:235 Page 3 of 16 Table 1 Genetic background of the sires white border line for some squares that follows the red Sire ID Number mtDNA Lineage Lineage lines in the upper palette
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