Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes
Ruminants are significant contributors to the livestock generated component of the greenhouse gas, methane (CH4). The CH4 is primarily produced by the rumen microbes. Although the composition of the diet and animal intake amount have the largest effect on CH4 production and yield (CH4 production/dry...
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Frontiers Media S.A.
2018-08-01
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| Series: | Frontiers in Genetics |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fgene.2018.00330/full |
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| author | Ruidong Xiang Ruidong Xiang Ruidong Xiang Jody McNally Jude Bond David Tucker Margaret Cameron Alistair J. Donaldson Katie L. Austin Suzanne Rowe Arjan Jonker Cesar S. Pinares-Patino Cesar S. Pinares-Patino John C. McEwan Phil E. Vercoe Phil E. Vercoe V. H. Oddy Brian P. Dalrymple Brian P. Dalrymple |
| author_facet | Ruidong Xiang Ruidong Xiang Ruidong Xiang Jody McNally Jude Bond David Tucker Margaret Cameron Alistair J. Donaldson Katie L. Austin Suzanne Rowe Arjan Jonker Cesar S. Pinares-Patino Cesar S. Pinares-Patino John C. McEwan Phil E. Vercoe Phil E. Vercoe V. H. Oddy Brian P. Dalrymple Brian P. Dalrymple |
| author_sort | Ruidong Xiang |
| collection | DOAJ |
| description | Ruminants are significant contributors to the livestock generated component of the greenhouse gas, methane (CH4). The CH4 is primarily produced by the rumen microbes. Although the composition of the diet and animal intake amount have the largest effect on CH4 production and yield (CH4 production/dry matter intake, DMI), the host also influences CH4 yield. Shorter rumen feed mean retention time (MRT) is associated with higher dry matter intake and lower CH4 yield, but the molecular mechanism(s) by which the host affects CH4 production remain unclear. We integrated rumen wall transcriptome data and CH4 phenotypes from two independent experiments conducted with sheep in Australia (AUS, n = 62) and New Zealand (NZ, n = 24). The inclusion of the AUS data validated the previously identified clusters and gene sets representing rumen epithelial, metabolic and muscular functions. In addition, the expression of the cell cycle genes as a group was consistently positively correlated with acetate and butyrate concentrations (p < 0.05, based on AUS and NZ data together). The expression of a group of metabolic genes showed positive correlations in both AUS and NZ datasets with CH4 production (p < 0.05) and yield (p < 0.01). These genes encode key enzymes in the ketone body synthesis pathway and included members of the poorly characterized aldo-keto reductase 1C (AKR1C) family. Several AKR1C family genes appear to have ruminant specific evolution patterns, supporting their specialized roles in the ruminants. Combining differential gene expression in the rumen wall muscle of the shortest and longest MRT AUS animals (no data available for the NZ animals) with correlation and network analysis, we identified a set of rumen muscle genes involved in cell junctions as potential regulators of MRT, presumably by influencing contraction rates of the smooth muscle component of the rumen wall. Higher rumen expression of these genes, including SYNPO (synaptopodin, p < 0.01) and NEXN (nexilin, p < 0.05), was associated with lower CH4 yield in both AUS and NZ datasets. Unlike the metabolic genes, the variations in the expression of which may reflect the availability of rumen metabolites, the muscle genes are currently our best candidates for causal genes that influence CH4 yield. |
| first_indexed | 2024-12-16T08:48:13Z |
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| last_indexed | 2024-12-16T08:48:13Z |
| publishDate | 2018-08-01 |
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| spelling | doaj.art-5d856b66b9964ff2a2d6e88ccbe9e02a2022-12-21T22:37:34ZengFrontiers Media S.A.Frontiers in Genetics1664-80212018-08-01910.3389/fgene.2018.00330374372Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related PhenotypesRuidong Xiang0Ruidong Xiang1Ruidong Xiang2Jody McNally3Jude Bond4David Tucker5Margaret Cameron6Alistair J. Donaldson7Katie L. Austin8Suzanne Rowe9Arjan Jonker10Cesar S. Pinares-Patino11Cesar S. Pinares-Patino12John C. McEwan13Phil E. Vercoe14Phil E. Vercoe15V. H. Oddy16Brian P. Dalrymple17Brian P. Dalrymple18CSIRO Agriculture & Food, Queensland Bioscience Precinct, St Lucia, QLD, AustraliaFaculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, AustraliaAgriculture Victoria, AgriBio, Centre for AgriBioscience, Bundoora, VIC, AustraliaF. D. McMaster Laboratory, CSIRO Agriculture & Food, Armidale, NSW, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaInvermay Agricultural Centre, AgResearch Limited, Mosgiel, New ZealandGrasslands Research Centre, AgResearch Limited, Palmerston North, New ZealandGrasslands Research Centre, AgResearch Limited, Palmerston North, New ZealandNew Zealand-Peru Dairy Support Project, MINAGRI, Lima, PeruInvermay Agricultural Centre, AgResearch Limited, Mosgiel, New ZealandSchool of Animal Biology, The University of Western Australia, Crawley, WA, Australia0Institute of Agriculture, The University of Western Australia, Crawley, WA, AustraliaNSW Department of Primary Industries, Extensive Livestock Industries Centre, University of New England, Armidale, NSW, AustraliaCSIRO Agriculture & Food, Queensland Bioscience Precinct, St Lucia, QLD, Australia0Institute of Agriculture, The University of Western Australia, Crawley, WA, AustraliaRuminants are significant contributors to the livestock generated component of the greenhouse gas, methane (CH4). The CH4 is primarily produced by the rumen microbes. Although the composition of the diet and animal intake amount have the largest effect on CH4 production and yield (CH4 production/dry matter intake, DMI), the host also influences CH4 yield. Shorter rumen feed mean retention time (MRT) is associated with higher dry matter intake and lower CH4 yield, but the molecular mechanism(s) by which the host affects CH4 production remain unclear. We integrated rumen wall transcriptome data and CH4 phenotypes from two independent experiments conducted with sheep in Australia (AUS, n = 62) and New Zealand (NZ, n = 24). The inclusion of the AUS data validated the previously identified clusters and gene sets representing rumen epithelial, metabolic and muscular functions. In addition, the expression of the cell cycle genes as a group was consistently positively correlated with acetate and butyrate concentrations (p < 0.05, based on AUS and NZ data together). The expression of a group of metabolic genes showed positive correlations in both AUS and NZ datasets with CH4 production (p < 0.05) and yield (p < 0.01). These genes encode key enzymes in the ketone body synthesis pathway and included members of the poorly characterized aldo-keto reductase 1C (AKR1C) family. Several AKR1C family genes appear to have ruminant specific evolution patterns, supporting their specialized roles in the ruminants. Combining differential gene expression in the rumen wall muscle of the shortest and longest MRT AUS animals (no data available for the NZ animals) with correlation and network analysis, we identified a set of rumen muscle genes involved in cell junctions as potential regulators of MRT, presumably by influencing contraction rates of the smooth muscle component of the rumen wall. Higher rumen expression of these genes, including SYNPO (synaptopodin, p < 0.01) and NEXN (nexilin, p < 0.05), was associated with lower CH4 yield in both AUS and NZ datasets. Unlike the metabolic genes, the variations in the expression of which may reflect the availability of rumen metabolites, the muscle genes are currently our best candidates for causal genes that influence CH4 yield.https://www.frontiersin.org/article/10.3389/fgene.2018.00330/fullsheeptranscriptomicsrumen mean retention timemethaneoxo-acid metabolismsmooth muscle |
| spellingShingle | Ruidong Xiang Ruidong Xiang Ruidong Xiang Jody McNally Jude Bond David Tucker Margaret Cameron Alistair J. Donaldson Katie L. Austin Suzanne Rowe Arjan Jonker Cesar S. Pinares-Patino Cesar S. Pinares-Patino John C. McEwan Phil E. Vercoe Phil E. Vercoe V. H. Oddy Brian P. Dalrymple Brian P. Dalrymple Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes Frontiers in Genetics sheep transcriptomics rumen mean retention time methane oxo-acid metabolism smooth muscle |
| title | Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes |
| title_full | Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes |
| title_fullStr | Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes |
| title_full_unstemmed | Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes |
| title_short | Across-Experiment Transcriptomics of Sheep Rumen Identifies Expression of Lipid/Oxo-Acid Metabolism and Muscle Cell Junction Genes Associated With Variation in Methane-Related Phenotypes |
| title_sort | across experiment transcriptomics of sheep rumen identifies expression of lipid oxo acid metabolism and muscle cell junction genes associated with variation in methane related phenotypes |
| topic | sheep transcriptomics rumen mean retention time methane oxo-acid metabolism smooth muscle |
| url | https://www.frontiersin.org/article/10.3389/fgene.2018.00330/full |
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