TEAD3, Implicated by Association to Grilsing in Atlantic Salmon

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TEAD3, Implicated by Association to Grilsing in Atlantic Salmon Edinburgh Research Explorer TEAD3, implicated by association to grilsing in Atlantic salmon Citation for published version: Christensen, KA, Gutierrez Silva, A, Lubieniecki, KP & Davidson, WS 2017, 'TEAD3, implicated by association to grilsing in Atlantic salmon', Aquaculture, vol. 479, pp. 571-578. https://doi.org/10.1016/j.aquaculture.2017.06.026 Digital Object Identifier (DOI): 10.1016/j.aquaculture.2017.06.026 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Aquaculture General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 29. Sep. 2021 Aquaculture 479 (2017) 571–578 Contents lists available at ScienceDirect Aquaculture journal homepage: www.elsevier.com/locate/aquaculture TEAD3, implicated by association to grilsing in Atlantic salmon MARK ⁎ Kris A. Christensen , Alejandro P. Gutierrez1, Krzysztof P. Lubieniecki, William S. Davidson Molecular Biology and Biochemistry, Simon Fraser University, South Sciences Building Room 8166, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada ARTICLE INFO ABSTRACT Keywords: With the recent finding that the vestigial-like family member 3 (Vgll3) gene is associated with early maturation, Early maturation we decided to re-examine previously reported quantitative trait loci (QTL) and genome wide association (GWA) Grilsing studies, involved with early maturation, to see if Vgll3 was the source of any of these associations. Using a Salmon TaqMan assay for Vgll3, we were able to verify that a prominent QTL for early maturation was indeed associated Vestigial with Vgll3. Next, we used Vgll3 genotypes as a cofactor to re-examine for any additional QTLs or GWAs. Several QTL were found at the chromosome-wide significance level. By examining interacting partners of Vgll3 from other GWA organisms, we identified several candidate genes that may interact with Vgll3 in Atlantic salmon and effect early maturation. The location of these genes were determined from the genome sequence, while markers near QTL were examined to see if they were near any Vgll3 interacting genes. In this way, we identified TEAD3 as a putative gene also influencing early maturation in Atlantic salmon. A TaqMan assay was used to genotype TEAD3. These genotypes appear to be associated with early maturation. 1. Introduction (Fleming, 1996; Gross, 1985). Larger males tend to have an aggressive mating style, fighting for mating opportunities; while the smaller males New Brunswick Atlantic salmon farming generated an estimated often use a strategy of wait and sneak-in (Gross, 1985). In environments $250 million CAD in 2002 (McClure et al., 2007). Of this, between where there are many large males, a sneak fertilization may be a highly $11–$24 million CAD was estimated to be lost due to early maturation effective strategy of reproduction, but when there are many small fish (known as grilsing in Atlantic salmon) (McClure et al., 2007). Typically, trying to sneak-in, fighting may be more effective (Fleming, 1996; the loss in revenue from early maturation has to do with the flesh Gross, 1985). quality degradation that accompanies maturation (Aksnes et al., 1986). Genetic variation associated with age at maturity has been seen in Understanding why some fish mature earlier than others offers Atlantic quantitative trait loci (QTL) and genome wide association (GWA) stu- salmon producers a potential mechanism where they may be able to dies (Gutierrez et al., 2015, 2014; Johnston et al., 2014). More recently, reduce these losses. two research groups have posited that the vestigial-like family member Variation of age at maturity may benefit a species in the wild. The 3(Vgll3) gene may partially regulate the timing of maturity in Atlantic variation in age at maturation can preserve genetic diversity by main- Salmon (Ayllon et al., 2015; Barson et al., 2015). This makes Vgll3 a taining alleles that would be detrimental if only a single age at ma- focus for possible use in marker assisted selection to reduce the number turation existed. This variation may also increase the number of po- of early maturing individuals. tential spawners during a single year, which would help maintain The homologs of the Vgll3 gene have been studied extensively in genetic diversity (Saunders and Schom, 1985). The diversity main- other organisms. In Drosophila, vestigial was found to be involved in tained by multiple life-histories may also make Atlantic salmon more wing formation (Kim et al., 1996). Later, it was found that another able to adapt to different environments (e.g. low-flow and high-flow protein, scalloped (a homolog of transcription enhancer factor-1 in ver- streams, reviewed in (Fleming, 1996)) and potentially explains part of tebrates), was needed in wing formation and that the proteins of these the reason why they have been successful at colonizing so many loca- two genes interacted to do so (S. Paumard-Rigal, 1998; Simmonds et al., tions. 1998). Simmonds et al. (1998), suggested that vestigial was a tissue- The mechanism maintaining variation in age at maturity is likely specific co-factor of the transcription factor scalloped. complex, but may reflect a balance between male mating strategies In vertebrates, three vestigial homologs were characterized that all ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (K.A. Christensen), [email protected] (A.P. Gutierrez), [email protected] (K.P. Lubieniecki), [email protected] (W.S. Davidson). 1 Present address: The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, Scotland, UK. http://dx.doi.org/10.1016/j.aquaculture.2017.06.026 Received 8 December 2016; Received in revised form 16 June 2017; Accepted 18 June 2017 Available online 19 June 2017 0044-8486/ © 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). K.A. Christensen et al. Aquaculture 479 (2017) 571–578 contain a transcription enhancer factor-1 (TEF-1 commonly referred to as used to identify if any of the markers near QTL were physically linked TEAD genes) interacting domain (Maeda et al., 2002). The vestigial to binding partners of Vgll3. homologs appear to form heterodimers with TEF-1 (Maeda et al., 2002). This interaction appeared to play a role in skeletal muscle differentia- 2. Materials and methods tion in a mouse model (Maeda et al., 2002). Again, suggesting that the vestigial homologs act as transcriptional co-factors. It has also been 2.1. Population and dataset shown that vertebrate TEF-1 shares enough similarity with Drosophila scalloped, that TEF-1 can be substituted for scalloped and still have Five Atlantic salmon families utilized by Gutierrez et al. (2014) wingblade development (Deshpande et al., 1997). Similarly, human were used for QTL analysis, GWA analysis, and association testing. vestigial homologs can also be substituted for vestigial in Drosophila and These families are from the Mowi strain and were bred for Mainstream wing development will still continue (Vaudin et al., 1999). Canada (now Cermaq) as part of their broodstock program (Gutierrez Early estimates of the number of TEF-1 genes in mammalian gen- et al., 2014). Fertilization occurred in late 2005, the fry from these omes was three to five (Kaneko and DePamphilis, 1998). It was shown families were pooled in February 2006, and phenotypes were scored as that each gene contains a TEA DNA (TEAD) binding domain, with late as 2009 (Gutierrez et al., 2014). An additional 160 individuals (80 nearly identical amino acid sequence. This allows each of them to bind Grilse and 80 Non-Grilse) and 192 parents from the 2005 broodstock conserved non-coding DNA elements (Kaneko and DePamphilis, 1998). year were utilized in a GWA analysis. These individuals were originally Expression of these genes varies from tissues, but nearly every tissue a part of a GWA study conducted by Gutierrez et al. (2015). Genotype expresses at least one TEAD gene. These observations led researchers to information was also collected by Gutierrez et al. (2014) and Gutierrez conclude that in order for TEAD genes to differentially regulate genes in et al. (2015). separate tissues, there must a mechanism for ubiquitous TEAD proteins to only bind a subset of the possible conserved non-coding DNA ele- 2.2. Genotyping Vgll3 ments (Kaneko and DePamphilis, 1998). All these pieces of evidence support the idea that TEAD genes and vestigial homologs (Vgll1–4) are Two genotyping assays were used to interrogate the Vgll3 genotypes involved in regulating transcription in both vertebrates and in- of all of the individuals (Fig. 1). The preliminary assay utilized re- vertebrates, and that vestigial homologs are tissue-specific co-factors for striction fragment length polymorphisms (RFLP) to determine if
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