Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork

Abstract Pork is the most consumed meat in the world, and its quality is associated with human health. Intramuscular fat (IMF) deposition (also called marbling) is a key factor positively correlated with various quality traits and lipo-nutritional values of meat. However, the cell dynamics and trans...

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Main Authors: Liyi Wang, Xueyan Zhao, Shiqi Liu, Wenjing You, Yuqin Huang, Yanbing Zhou, Wentao Chen, Shu Zhang, Jiying Wang, Qiankun Zheng, Yizhen Wang, Tizhong Shan
Format: Article
Language:English
Published: Nature Portfolio 2023-06-01
Series:npj Science of Food
Online Access:https://doi.org/10.1038/s41538-023-00203-4
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author Liyi Wang
Xueyan Zhao
Shiqi Liu
Wenjing You
Yuqin Huang
Yanbing Zhou
Wentao Chen
Shu Zhang
Jiying Wang
Qiankun Zheng
Yizhen Wang
Tizhong Shan
author_facet Liyi Wang
Xueyan Zhao
Shiqi Liu
Wenjing You
Yuqin Huang
Yanbing Zhou
Wentao Chen
Shu Zhang
Jiying Wang
Qiankun Zheng
Yizhen Wang
Tizhong Shan
author_sort Liyi Wang
collection DOAJ
description Abstract Pork is the most consumed meat in the world, and its quality is associated with human health. Intramuscular fat (IMF) deposition (also called marbling) is a key factor positively correlated with various quality traits and lipo-nutritional values of meat. However, the cell dynamics and transcriptional programs underlying lipid deposition in highly marbled meat are still unclear. Here, we used Laiwu pigs with high (HLW) or low (LLW) IMF contents to explore the cellular and transcriptional mechanisms underlying lipid deposition in highly-marbled pork by single-nucleus RNA sequencing (snRNA-seq) and bulk RNA sequencing. The HLW group had higher IMF contents but less drip loss than the LLW group. Lipidomics results revelled the changes of overall lipid classes composition (e.g., glycerolipids including triglycerides, diglycerides, and monoglycerides; sphingolipids including ceramides and monohexose ceramide significantly increased) between HLW and LLW groups. SnRNA-seq revealed nine distinct cell clusters, and the HLW group had a higher percentage of adipocytes (1.40% vs. 0.17%) than the LLW group. We identified 3 subpopulations of adipocytes, including PDE4D+/PDE7B+ (in HLW and LLW), DGAT2+/SCD+ (mostly in HLW) and FABP5+/SIAH1+ cells (mostly in HLW). Moreover, we showed that fibro/adipogenic progenitors could differentiate into IMF cells and contribute to 43.35% of adipocytes in mice. In addition, RNA-seq revealed different genes involved in lipid metabolism and fatty acid elongation. Our study provides new insights into the cellular and molecular signatures of marbling formation; such knowledge may facilitate the development of new strategies to increase IMF deposition and the lipo-nutritional quality of high marbled pork.
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spelling doaj.art-6a113cd9eb614d248e4bf97b918b99492023-06-04T11:39:26ZengNature Portfolionpj Science of Food2396-83702023-06-017111510.1038/s41538-023-00203-4Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled porkLiyi Wang0Xueyan Zhao1Shiqi Liu2Wenjing You3Yuqin Huang4Yanbing Zhou5Wentao Chen6Shu Zhang7Jiying Wang8Qiankun Zheng9Yizhen Wang10Tizhong Shan11College of Animal Sciences, Zhejiang UniversityInstitute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityInstitute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural SciencesDELISI GROUP Co. LtdCollege of Animal Sciences, Zhejiang UniversityCollege of Animal Sciences, Zhejiang UniversityAbstract Pork is the most consumed meat in the world, and its quality is associated with human health. Intramuscular fat (IMF) deposition (also called marbling) is a key factor positively correlated with various quality traits and lipo-nutritional values of meat. However, the cell dynamics and transcriptional programs underlying lipid deposition in highly marbled meat are still unclear. Here, we used Laiwu pigs with high (HLW) or low (LLW) IMF contents to explore the cellular and transcriptional mechanisms underlying lipid deposition in highly-marbled pork by single-nucleus RNA sequencing (snRNA-seq) and bulk RNA sequencing. The HLW group had higher IMF contents but less drip loss than the LLW group. Lipidomics results revelled the changes of overall lipid classes composition (e.g., glycerolipids including triglycerides, diglycerides, and monoglycerides; sphingolipids including ceramides and monohexose ceramide significantly increased) between HLW and LLW groups. SnRNA-seq revealed nine distinct cell clusters, and the HLW group had a higher percentage of adipocytes (1.40% vs. 0.17%) than the LLW group. We identified 3 subpopulations of adipocytes, including PDE4D+/PDE7B+ (in HLW and LLW), DGAT2+/SCD+ (mostly in HLW) and FABP5+/SIAH1+ cells (mostly in HLW). Moreover, we showed that fibro/adipogenic progenitors could differentiate into IMF cells and contribute to 43.35% of adipocytes in mice. In addition, RNA-seq revealed different genes involved in lipid metabolism and fatty acid elongation. Our study provides new insights into the cellular and molecular signatures of marbling formation; such knowledge may facilitate the development of new strategies to increase IMF deposition and the lipo-nutritional quality of high marbled pork.https://doi.org/10.1038/s41538-023-00203-4
spellingShingle Liyi Wang
Xueyan Zhao
Shiqi Liu
Wenjing You
Yuqin Huang
Yanbing Zhou
Wentao Chen
Shu Zhang
Jiying Wang
Qiankun Zheng
Yizhen Wang
Tizhong Shan
Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
npj Science of Food
title Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
title_full Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
title_fullStr Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
title_full_unstemmed Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
title_short Single-nucleus and bulk RNA sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
title_sort single nucleus and bulk rna sequencing reveal cellular and transcriptional mechanisms underlying lipid dynamics in high marbled pork
url https://doi.org/10.1038/s41538-023-00203-4
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