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RNA Profiles of the Korat Chicken Breast Muscle with Increased Carnosine Content Produced Through Dietary Supplementation With animals Article RNA Profiles of the Korat Chicken Breast Muscle with Increased Carnosine Content Produced through Dietary Supplementation with β-Alanine or L-Histidine Satoshi Kubota * , Kasarat Promkhun, Panpradub Sinpru , Chanadda Suwanvichanee, Wittawat Molee and Amonrat Molee School of Animal Technology and Innovation, Institute of Agricultural Technology, Suranaree University of Technology, Nakhon Ratchasima 30000, Thailand; [email protected] (K.P.); [email protected] (P.S.); [email protected] (C.S.); [email protected] (W.M.); [email protected] (A.M.) * Correspondence: [email protected]; Tel.: +66-44224370 Simple Summary: Carnosine is a bioactive food component with several potential health benefits for humans due to its physiological functions. Dietary supplementation with β-alanine or L-histidine can increase the carnosine content of skeletal muscles in chickens. Dietary supplementation with β-alanine or L-histidine has produced a slow-growing chicken variety with high carnosine content in the breast meat; however, the supplementation with L-histidine alone softens the meat toughness, which may affect consumers’ willingness to buy the meat. Gene expression is a key factor that influences meat quality. Understanding the molecular mechanisms that affect carnosine content Citation: Kubota, S.; Promkhun, K.; and meat toughness would allow the production of more value-added slow-growing chickens. Sinpru, P.; Suwanvichanee, C.; Molee, We compared global gene expression in chicken breast muscles with differing carnosine contents W.; Molee, A. RNA Profiles of the and meat toughness produced through dietary supplementation with β-alanine or L-histidine. We Korat Chicken Breast Muscle with identified differentially expressed genes involved in regulating myosin, collagen, intramuscular fat, Increased Carnosine Content and calpain—factors that may affect meat tenderness. Pathway enrichment analysis indicated that Produced through Dietary the insulin-related and adipocytokine signaling pathways were altered by dietary supplementation Supplementation with β-Alanine or with β-alanine or L-histidine. These data will be useful for future studies on carnosine content and L-Histidine. Animals 2021, 11, 2596. meat toughness in slow-growing chickens. https://doi.org/10.3390/ani11092596 Abstract: Korat chicken (KRC) is a slow-growing chicken bred in Thailand, whose meat exhibits a Academic Editors: Francesca Soglia unique toughness. A previous study produced KRC breast meat containing high carnosine content and Simona Mattioli through dietary supplementation with β-alanine or L-histidine; however, the KRC that were fed Received: 29 July 2021 an L-histidine-supplemented diet produced meat that was significantly more tender. Herein, we Accepted: 31 August 2021 performed RNA-Seq to identify candidate genes involved in the regulation of carnosine content and Published: 3 September 2021 meat toughness. Total RNA was isolated from five female KRC breast muscles in each treatment group that KRC fed diets without supplementation, supplemented with β-alanine or L-histidine. Publisher’s Note: MDPI stays neutral Compared to the non-supplemented group, we identified 118 and 198 differentially expressed genes with regard to jurisdictional claims in (DEGs) in the β-alanine or L-histidine supplementation groups, respectively. Genes potentially published maps and institutional affil- related to meat tenderness—i.e., those regulating myosin, collagen, intramuscular fat, and calpain— iations. were upregulated (LOC107051274, ACSBG1, and CAPNS2) and downregulated (MYO7B, MYBPH, SERPINH1, and PGAM1). However, carnosine synthase gene was not identified. Functional en- richment analysis identified pathways affected by dietary supplementation, including the insulin signaling pathway (β-alanine supplementation) and the insulin resistance and adipocytokine sig- Copyright: © 2021 by the authors. naling pathways (L-histidine supplementation). The FoxO signaling pathway was identified as a Licensee MDPI, Basel, Switzerland. regulatory network for both supplementation groups. The identified genes can be used as molecular This article is an open access article markers of meat tenderness in slow-growing chickens. distributed under the terms and conditions of the Creative Commons Keywords: RNA-Seq; slow-growing chicken; breast meat; carnosine content; meat toughness Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Animals 2021, 11, 2596. https://doi.org/10.3390/ani11092596 https://www.mdpi.com/journal/animals Animals 2021, 11, 2596 2 of 14 1. Introduction Korat chicken (KRC) is produced by crossing the males of Thai indigenous chickens with the female Suranaree University of Technology (SUT) breeder line, and has a slow growth rate. KRC meat contains lower levels of fat and higher quantities of collagen compared to the meat from a commercial broiler. It also has a firm and chewy texture, which attracts domestic consumers to a greater extent than broiler meat in Thailand [1]. However, female KRCs are not as preferred by farmers because they grow at a slower rate than males, but have the same selling price. Thus, adding more value to female KRCs is desirable. Intarapichet and Maikhunthod [2] reported that meat from Thai indigenous female chickens contains higher levels of carnosine than meat from males. Carnosine is well-known for its physiological functions, and intake of carnosine has been shown to contribute to human health in many age-associated diseases and conditions [3,4]. Carnosine concentration in the skeletal muscles of broiler chickens can be enhanced by dietary supplementation with the constituent amino acids of carnosine (i.e., β-alanine and L-histidine) [5,6]. Suwanvichanee et al. [7] reported that compared to KRCs fed a diet without supplementation, female KRCs fed a diet supplemented with β-alanine or L-histidine have significantly higher carnosine content in breast muscles (by 26.42 and 32.76%, respectively). Growth and slaughtering performances were not significantly different between dietary treatments; however, meat toughness (as measured by shear force value) was significantly reduced only by supplementation with L-histidine [7]. These findings suggest that female KRCs with increased carnosine content produced through supplemented diets can increase the consumers’ demand as a functional food, which motivates farmers’ willingness to raise them. However, dietary supplementation with L-histidine also reduces the toughness of the meat, which is a unique property of KRC meat. Among the traits that strongly affect the quality of meat and consumers’ willingness to purchase poultry products, tenderness is the most important attribute [8]. Many factors contribute to the wide variation in tenderness of poultry meat, including bird strain, age, sex, environment, antemortem and/or postmortem handling conditions, and cooking method [9]. Several studies have identified the genetic basis of tenderness—including genes encoding the proteins of the calpain system (CAPN1)—in broiler chickens [10]. Using a whole transcriptomic analysis, Piórkowska et al. [11] identified biological processes and genes that are potentially associated with factors affecting chicken breast meat ten- derness, such as degradation of filamins (ASB2), lipogenesis (PLIN1 and THRSP), and collagen synthesis (COL16A1, COL20A1, LEPREL4, PCOLCE2, P4HA3, and VWA1). These findings suggest that such candidate genes can be used as markers to determine meat tenderness; however, it is unclear how the actions of these genes are affected in chickens fed a supplemented diet to increase carnosine content. Transcriptome sequencing technology (RNA-Seq) can help elucidate the genetic and physiological processes that regulate the phenotype of particular quantitative traits [12]. Di- etary supplementation has been shown to alter the transcriptomic profile of breast muscles in chickens, and RNA-Seq can be used to identify key genes and molecular regulatory mech- anisms related to factors affecting meat quality, such as color and taste [13], and melanin deposition [14]. In this study, we performed RNA-Seq in female KRC breast muscle to identify differentially expressed genes and underlying molecular mechanisms affected by the diets supplemented with β-alanine or L-histidine. To the best of our knowledge, this is the first study on global gene expression in chicken breast muscle with differing carnosine contents and meat toughness produced through dietary supplementation. The identified genes can be used as a molecular marker associated with carnosine content and meat tenderness in slow-growing chickens. Animals 2021, 11, 2596 3 of 14 2. Materials and Methods 2.1. Animals and Sample Collection All animal procedures applied in this research were approved by the Ethics Com- mittee on Animal Use of the Suranaree University of Technology (user application ID: U1-08780-2563). In this study, we used the 15 breast muscles of female KRCs collected in a previous study by Suwanvichanee et al. [7]. Briefly, a total of 300 one-day-old female KRCs were generated by crossbreeding male Thai indigenous chickens and the female SUT breeder line. All chicks were reared in open-sided housing from 0 to 3 weeks of age. KRC feeding management is designed as three different phases based on the age of the chicken: 0 to 3, 4 to 6, and 7 to 10 weeks. The basal diet at the initial, second, and final phases contains 21, 19, and 17% of protein, respectively. Birds were raised on a basal diet at the initial phase before
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