A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle

Deposition of intramuscular fat (IM), also known as marbling, is the deciding factor of beef quality grade in the U.S. Defining molecular mechanisms underlying the differential deposition of adipose tissue in distinct anatomical areas in beef cattle is key to the development of strategies for marbli...

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Main Authors: Mollie M. Green, Hunter R. Ford, Alexandra P. Tegeler, Oscar J. Benitez, Bradley J. Johnson, Clarissa Strieder-Barboza
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Agriculture
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Online Access:https://www.mdpi.com/2077-0472/15/14/1545
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author Mollie M. Green
Hunter R. Ford
Alexandra P. Tegeler
Oscar J. Benitez
Bradley J. Johnson
Clarissa Strieder-Barboza
author_facet Mollie M. Green
Hunter R. Ford
Alexandra P. Tegeler
Oscar J. Benitez
Bradley J. Johnson
Clarissa Strieder-Barboza
author_sort Mollie M. Green
collection DOAJ
description Deposition of intramuscular fat (IM), also known as marbling, is the deciding factor of beef quality grade in the U.S. Defining molecular mechanisms underlying the differential deposition of adipose tissue in distinct anatomical areas in beef cattle is key to the development of strategies for marbling enhancement while limiting the accumulation of excessive subcutaneous adipose tissue (SAT). The objective of this exploratory study was to define the IM and SAT transcriptional heterogeneity at the whole tissue and single-nuclei levels in beef steers. Longissimus dorsi muscle samples (9–11th rib) were collected from two finished beef steers at harvest to dissect matched IM and adjacent SAT (backfat). Total RNA from IM and SAT was isolated and sequenced in an Illumina NovaSeq 6000. Nuclei from the same samples were isolated by dounce homogenization, libraries generated with 10× Genomics, and sequenced in an Illumina NovaSeq 6000, followed by analysis via Cell Ranger pipeline and Seurat in RStudio (v4.3.2) By the expression of signature marker genes, single-nuclei RNA sequencing (snRNAseq) analysis identified mature adipocytes (AD; <i>ADIPOQ</i>, <i>LEP</i>), adipose stromal and progenitor cells (ASPC; <i>PDGFRA</i>), endothelial cells (EC; <i>VWF</i>, <i>PECAM1</i>), smooth muscle cells (SMC; <i>NOTCH3</i>, <i>MYL9</i>) and immune cells (IMC; <i>CD163</i>, <i>MRC1</i>). We detected six cell clusters in SAT and nine in IM. Across IM and SAT, AD was the most abundant cell type, followed by ASPC, SMC, and IMC. In SAT, AD made up 50% of the cellular population, followed by ASPC (31%), EC (14%), IMC (1%), and SMC (4%). In IM depot, AD made up 23% of the cellular population, followed by ASPC at 19% of the population, EC at 28%, IMC at 7% and SMC at 12%. The abundance of ASPC and AD was lower in IM vs. SAT, while IMC was increased, suggesting a potential involvement of immune cells on IM deposition. Accordingly, both bulk RNAseq and snRNAseq analyses identified activated pathways of inflammation and metabolic function in IM. These results demonstrate distinct transcriptional cellular heterogeneity between SAT and IM depots in beef steers, which may underly the mechanisms by which fat deposits in each depot. The identification of depot-specific cell populations in IM and SAT via snRNAseq analysis has the potential to reveal target genes for the modulation of fat deposition in beef cattle.
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spelling doaj-art-6f4ed776ae454ec58c4fc40973556e4d2025-08-20T03:55:49ZengMDPI AGAgriculture2077-04722025-07-011514154510.3390/agriculture15141545A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef CattleMollie M. Green0Hunter R. Ford1Alexandra P. Tegeler2Oscar J. Benitez3Bradley J. Johnson4Clarissa Strieder-Barboza5Department of Veterinary Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Veterinary Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Veterinary Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Veterinary Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Animal and Food Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Veterinary Sciences, Texas Tech University, Lubbock, TX 79409, USADeposition of intramuscular fat (IM), also known as marbling, is the deciding factor of beef quality grade in the U.S. Defining molecular mechanisms underlying the differential deposition of adipose tissue in distinct anatomical areas in beef cattle is key to the development of strategies for marbling enhancement while limiting the accumulation of excessive subcutaneous adipose tissue (SAT). The objective of this exploratory study was to define the IM and SAT transcriptional heterogeneity at the whole tissue and single-nuclei levels in beef steers. Longissimus dorsi muscle samples (9–11th rib) were collected from two finished beef steers at harvest to dissect matched IM and adjacent SAT (backfat). Total RNA from IM and SAT was isolated and sequenced in an Illumina NovaSeq 6000. Nuclei from the same samples were isolated by dounce homogenization, libraries generated with 10× Genomics, and sequenced in an Illumina NovaSeq 6000, followed by analysis via Cell Ranger pipeline and Seurat in RStudio (v4.3.2) By the expression of signature marker genes, single-nuclei RNA sequencing (snRNAseq) analysis identified mature adipocytes (AD; <i>ADIPOQ</i>, <i>LEP</i>), adipose stromal and progenitor cells (ASPC; <i>PDGFRA</i>), endothelial cells (EC; <i>VWF</i>, <i>PECAM1</i>), smooth muscle cells (SMC; <i>NOTCH3</i>, <i>MYL9</i>) and immune cells (IMC; <i>CD163</i>, <i>MRC1</i>). We detected six cell clusters in SAT and nine in IM. Across IM and SAT, AD was the most abundant cell type, followed by ASPC, SMC, and IMC. In SAT, AD made up 50% of the cellular population, followed by ASPC (31%), EC (14%), IMC (1%), and SMC (4%). In IM depot, AD made up 23% of the cellular population, followed by ASPC at 19% of the population, EC at 28%, IMC at 7% and SMC at 12%. The abundance of ASPC and AD was lower in IM vs. SAT, while IMC was increased, suggesting a potential involvement of immune cells on IM deposition. Accordingly, both bulk RNAseq and snRNAseq analyses identified activated pathways of inflammation and metabolic function in IM. These results demonstrate distinct transcriptional cellular heterogeneity between SAT and IM depots in beef steers, which may underly the mechanisms by which fat deposits in each depot. The identification of depot-specific cell populations in IM and SAT via snRNAseq analysis has the potential to reveal target genes for the modulation of fat deposition in beef cattle.https://www.mdpi.com/2077-0472/15/14/1545single-celltranscriptomebeef cattlemarblingadipose tissuefat
spellingShingle Mollie M. Green
Hunter R. Ford
Alexandra P. Tegeler
Oscar J. Benitez
Bradley J. Johnson
Clarissa Strieder-Barboza
A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
Agriculture
single-cell
transcriptome
beef cattle
marbling
adipose tissue
fat
title A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
title_full A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
title_fullStr A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
title_full_unstemmed A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
title_short A Single-Cell Assessment of Intramuscular and Subcutaneous Adipose Tissue in Beef Cattle
title_sort single cell assessment of intramuscular and subcutaneous adipose tissue in beef cattle
topic single-cell
transcriptome
beef cattle
marbling
adipose tissue
fat
url https://www.mdpi.com/2077-0472/15/14/1545
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