Mechanism of continuous high temperature affecting growth performance, meat quality, and muscle biochemical properties of finishing pigs

Ma et al. Genes & Nutrition (2019) 14:23 https://doi.org/10.1186/s12263-019-0643-9 RESEARCH Open Access Mechanism of continuous high temperature affecting growth performance, meat quality, and muscle biochemical properties of finishing pigs Xianyong Ma1,2,3,4,5* , Li Wang1,2,3,4,5, Zibiao Shi1,2,3,4,5, Wei Chen1,2,3,4,5, Xuefen Yang1,2,3,4,5, Youjun Hu1,2,3,4,5, Chuntian Zheng1,2,3,4,5 and Zongyong Jiang1,2,3,4,5* Abstract Background: The mechanism of high ambient temperature affecting meat quality is not clear till now. This study investigated the effect of high ambient temperature on meat quality and nutrition metabolism in finishing pigs. Methods: All pigs received the same corn-soybean meal diet. A total of 24 Landrace × Large White pigs (60 kg BW, all were female) were assigned to three groups: 22AL (fed ad libitum at 22 °C), 35AL (ad libitum fed at 35 °C), and 22PF (at 22 °C, but fed the amount consumed by pigs raised at 35 °C) and the experiment lasted for 30 days. Results: Feed intake, weight gain, and intramuscular fat (IMF) content of pigs were reduced, both directly by high temperature and indirectly through reduced feed intake. Transcriptome analysis of longissimus dorsi (LM) showed that downregulated genes caused by feed restriction were mainly involved in muscle development and energy metabolism; and upregulated genes were mainly involved in response to nutrient metabolism or extracellular stimulus. Apart from the direct effects of feed restriction, high temperature negatively affected the muscle structure and development, energy, or catabolic metabolism, and upregulated genes were mainly involved in DNA or protein damage or recombination, cell cycle process or biogenesis, stress response, or immune response. Conclusion: Both high temperature and reduced feed intake affected growth performance and meat quality. Apart from the effects of reducing feed intake, high temperature per se negatively downregulated cell cycle and upregulated heat stress response. High temperature also decreased the energy or catabolic metabolism level through PPAR signaling pathway. Keywords: Growth performance, High ambient temperature, Meat quality, mRNA array, Restricted feed intake Introduction Continuous high temperature, especially in summer in tropical or subtropical countries, is an unfavorable factor in swine production. Persistent exposure to high temperature decreases feed intake [1], growth performance [2], and meat quality [3, 4]. For example, high temperature reduced intramuscular fat (IMF) deposition [5, 6] and changed the pH value of the meat [3, 7]. These alterations were traditionally believed to result from the * Correspondence: ; 1 Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, People’s Republic of China Full list of author information is available at the end of the article decreased feed intake, but more recent studies have shown that heat stress per se also reduced metabolic rates and altered post-absorptive metabolism, regardless of decreased feed intake [8, 9]. Heat stress also changed expression of some genes related to oxidative metabolism, through adaptive physiological mechanisms, to reduce thermogenesis [7, 10]. Although inferior meat quality induced by heat stress has been intensively studied, the molecular mechanisms underlying the pathophysiological changes remain to be defined. As heat stress does decrease feed intake, it remains unclear what changes are dependent or independent low nutrient availability. Gene expression profiles of longissimus © The Author(s). 2019 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. Ma et al. Genes & Nutrition (2019) 14:23 muscle (LM) have been used here to further examine how heat stress affects meat quality and the extent to which it is dependent on reduced feed intake. Materials and methods Animals and diets A total of 24 Landrace × Large White pigs (60 kg BW) were assigned randomly to three groups with eight pigs per group. Pigs were housed individually in wire cages (139 × 67 × 115 cm) in one of three temperaturecontrolled rooms at the Institute of Animal Science, Guangdong Academy of Agricultural Sciences. After adaption for 1 week, pigs were treated as follows: a control group of pigs had ad libitum access to feed at 22 °C (RT) (22AL); the heat-stressed group had ad libitum access to feed at 35 °C (35AL); and pair-fed pigs at 22 °C (22PF) were fed the amount consumed by pigs raised at 35 °C. All pigs were fed twice daily with a typical cornsoybean meal-based diet for finishing pigs (the diet formula is available as Additional file 1: Table S1). The temperature in one room was increased from 22 to 35 °C within approximately 2 h and then remained at 35 °C for the 30-d experimental period; other rooms were maintained at 22 °C. Water was available ad libitum for all pigs. Page 2 of 15 Machine (Instron model 4411; Instron, Canton, MA, USA) and drip loss was measured by weight loss over 24 h at 4 °C in a plastic bag, also as described by Mason et al. [12]. The IMF content was measured by petroleum ether extraction of powdered, lyophilized muscle using the Soxtec 2055 fat extraction system (Foss Tecator AB, Höganäs, Sweden), according to the Association of Official Analytical Chemists method [13]. RNA extraction and target labeling Total RNA was isolated from LM using the TRIzol reagent (Invitrogen, Carlsbad, CA, USA) and purified using a QIAGEN RNeasy® Mini Kit (QIAGEN, Chatsworth, CA, USA) according the manufacturer’s instructions. The RNA quality was checked with a spectrophotometer (ND1000, Nano-Drop Technologies, Wilmington, DE, USA). Each RNA sample was annealed with a primer containing a poly-dT and a T7 polymerase promoter. Reverse transcriptase produced primary and secondary cDNA strands. T7 RNA polymerase was then used to create cRNA from the double-stranded cDNA by incorporating cyanine-3labeled cytidine 3-CTP according to the labeling kit recommendations (Agilent Technologies, Santa Clara, CA, USA). The quality of the labeled cRNA was again verified. Hybridization, scanning, and feature extraction Feeding, slaughter procedure, and sample collection All aspects of the experiment including transport and slaughtering procedures were carried out in accordance with the Chinese guidelines for the use of experimental animals and animal welfare [11] and approved by the Animal Experimental Committee of the Institute of Anim (...truncated)