Folate Deficiency during Early-Mid Pregnancy Affects the Skeletal Muscle Transcriptome of Piglets from a Reciprocal Cross

Yi Li,Yunliang Jiang,Li Kang,Yanxiao Sun,Qiang Feng,Guanglei Li,Xinxing Cui,Xu Zhang,Meng Wang,Qiong Wu

doi:10.1371/journal.pone.0082616

Abstract

Folate deficiency (FD) during pregnancy can cause fetal intrauterine growth restriction in pigs, of which the skeletal dysplasia is a major manifestation. Factors influencing muscle development are very important in the formation of porcine meat quality trait. However, the effect of folate deficiency on skeletal muscle development and its molecular mechanisms are unknown. The objective of this study is to determine the effect of maternal folate deficiency on the skeletal muscle transcriptome of piglets from a reciprocal cross, in which full-sibling Landrace (LR) and full-sibling Chinese local breed Laiwu (LW) pigs were used for reciprocal cross matings, and sows were fed either a folate deficient or a normal diet during early-mid gestation. In addition, the difference in the responsiveness of the piglets to folate deficiency during early-mid pregnancy between reciprocal cross groups was investigated. Longissimus dorsi (LD) muscle samples were collected from newborn piglets and a 4 × 44K Agilent porcine oligo microarray was used for transcriptome analysis of porcine LD muscle. The results showed that folate deficiency during early-mid pregnancy affected piglet body weight, LD muscle fiber number and content of intramuscular triglyceride. The microarray results indicated that 3154 genes were differentially expressed between folate deficient and normal piglets from the LR♂ × LW♀ cross, and 3885 differentially expressed genes (DEGs) in the ones from the LW♂ × LR♀ cross. From functional analyses, sow folate deficiency affected almost all biological processes in the progeny. Lipid metabolism-related genes and associated metabolic pathways were regulated extensively by folate deficiency, especially in LR♂ × LW♀ cross piglets. Most of the genes that are regulated by folate deficiency in the LD muscle of piglets were different between LR♂ × LW♀ and LW♂ × LR♀ crosses, suggesting some epigenetic effects of FD exist in genes underlying myogenesis and intramuscular fat deposition in piglets.

Highlights

Improving meat quality has become a research focus for pig breeding experts in the 21st century [1]
It can be seen from haematoxylin and eosin (HE) staining that the Longissimus dorsi (LD) muscle cross section of newborn piglets contained a lot of skeletal muscle fiber, and blood vessels, nerves and dense connective tissues were around muscle bundle (Figure 1A-D)
The content of intramuscular triglyceride (IMTG) of LD muscle was significantly higher in piglets from the

Summary

Introduction

Improving meat quality has become a research focus for pig breeding experts in the 21st century [1]. Meat quality is related to the expression of genes controlling myogenesis and lipid metabolism, which is affected by living conditions, nutrition, and other factors [2,3]. Many studies have demonstrated a link between folate deficiency during early pregnancy and developmental abnormalities, such as neural tube defects [10], abnormal embryonic development [11,12], and tumor formation [13]. For these reasons, dietary folate supplementation is routinely recommended during early pregnancy in human [14]. Another indication that folate status during early pregnancy can significantly change offspring phenotype is that folate supplementation during pregnancy in

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