Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.)
Abstract Intraspecific genetic variation in foundation species such as aspen (Populus tremuloides Michx.) shapes their impact on forest structure and function. Identifying genes underlying ecologically important traits is key to understanding that impact. Previous studies, using single‐locus genome‐...
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| Format: | Article |
| Language: | English |
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Wiley
2023-10-01
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| Series: | Ecology and Evolution |
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| Online Access: | https://doi.org/10.1002/ece3.10541 |
| _version_ | 1827782330132987904 |
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| author | Jennifer F. L. Riehl Christopher T. Cole Clay J. Morrow Hilary L. Barker Carolina Bernhardsson Kennedy Rubert‐Nason Pär K. Ingvarsson Richard L. Lindroth |
| author_facet | Jennifer F. L. Riehl Christopher T. Cole Clay J. Morrow Hilary L. Barker Carolina Bernhardsson Kennedy Rubert‐Nason Pär K. Ingvarsson Richard L. Lindroth |
| author_sort | Jennifer F. L. Riehl |
| collection | DOAJ |
| description | Abstract Intraspecific genetic variation in foundation species such as aspen (Populus tremuloides Michx.) shapes their impact on forest structure and function. Identifying genes underlying ecologically important traits is key to understanding that impact. Previous studies, using single‐locus genome‐wide association (GWA) analyses to identify candidate genes, have identified fewer genes than anticipated for highly heritable quantitative traits. Mounting evidence suggests that polygenic control of quantitative traits is largely responsible for this “missing heritability” phenomenon. Our research characterized the genetic architecture of 30 ecologically important traits using a common garden of aspen through genomic and transcriptomic analyses. A multilocus association model revealed that most traits displayed a highly polygenic architecture, with most variation explained by loci with small effects (likely below the detection levels of single‐locus GWA methods). Consistent with a polygenic architecture, our single‐locus GWA analyses found only 38 significant SNPs in 22 genes across 15 traits. Next, we used differential expression analysis on a subset of aspen genets with divergent concentrations of salicinoid phenolic glycosides (key defense traits). This complementary method to traditional GWA discovered 1243 differentially expressed genes for a polygenic trait. Soft clustering analysis revealed three gene clusters (241 candidate genes) involved in secondary metabolite biosynthesis and regulation. Our work reveals that ecologically important traits governing higher‐order community‐ and ecosystem‐level attributes of a foundation forest tree species have complex underlying genetic structures and will require methods beyond traditional GWA analyses to unravel. |
| first_indexed | 2024-03-11T15:30:40Z |
| format | Article |
| id | doaj.art-fe30468aa6e94e41ad6fb0b2248f80f5 |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-03-11T15:30:40Z |
| publishDate | 2023-10-01 |
| publisher | Wiley |
| record_format | Article |
| series | Ecology and Evolution |
| spelling | doaj.art-fe30468aa6e94e41ad6fb0b2248f80f52023-10-27T04:40:51ZengWileyEcology and Evolution2045-77582023-10-011310n/an/a10.1002/ece3.10541Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.)Jennifer F. L. Riehl0Christopher T. Cole1Clay J. Morrow2Hilary L. Barker3Carolina Bernhardsson4Kennedy Rubert‐Nason5Pär K. Ingvarsson6Richard L. Lindroth7Department of Entomology University of Wisconsin‐Madison Madison Wisconsin USADepartment of Entomology University of Wisconsin‐Madison Madison Wisconsin USADepartment of Forest and Wildlife Ecology University of Wisconsin‐Madison Madison Wisconsin USADepartment of Entomology University of Wisconsin‐Madison Madison Wisconsin USADepartment of Ecology and Environmental Science Umeå University Umeå SwedenDepartment of Entomology University of Wisconsin‐Madison Madison Wisconsin USADepartment of Plant Biology Swedish University of Agricultural Sciences, Uppsala BioCenter Uppsala SwedenDepartment of Entomology University of Wisconsin‐Madison Madison Wisconsin USAAbstract Intraspecific genetic variation in foundation species such as aspen (Populus tremuloides Michx.) shapes their impact on forest structure and function. Identifying genes underlying ecologically important traits is key to understanding that impact. Previous studies, using single‐locus genome‐wide association (GWA) analyses to identify candidate genes, have identified fewer genes than anticipated for highly heritable quantitative traits. Mounting evidence suggests that polygenic control of quantitative traits is largely responsible for this “missing heritability” phenomenon. Our research characterized the genetic architecture of 30 ecologically important traits using a common garden of aspen through genomic and transcriptomic analyses. A multilocus association model revealed that most traits displayed a highly polygenic architecture, with most variation explained by loci with small effects (likely below the detection levels of single‐locus GWA methods). Consistent with a polygenic architecture, our single‐locus GWA analyses found only 38 significant SNPs in 22 genes across 15 traits. Next, we used differential expression analysis on a subset of aspen genets with divergent concentrations of salicinoid phenolic glycosides (key defense traits). This complementary method to traditional GWA discovered 1243 differentially expressed genes for a polygenic trait. Soft clustering analysis revealed three gene clusters (241 candidate genes) involved in secondary metabolite biosynthesis and regulation. Our work reveals that ecologically important traits governing higher‐order community‐ and ecosystem‐level attributes of a foundation forest tree species have complex underlying genetic structures and will require methods beyond traditional GWA analyses to unravel.https://doi.org/10.1002/ece3.10541community geneticsdifferential expressionmultilocus association modelomnigenic modelpolygenic architecturesalicinoids |
| spellingShingle | Jennifer F. L. Riehl Christopher T. Cole Clay J. Morrow Hilary L. Barker Carolina Bernhardsson Kennedy Rubert‐Nason Pär K. Ingvarsson Richard L. Lindroth Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) Ecology and Evolution community genetics differential expression multilocus association model omnigenic model polygenic architecture salicinoids |
| title | Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) |
| title_full | Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) |
| title_fullStr | Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) |
| title_full_unstemmed | Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) |
| title_short | Genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen (Populus tremuloides Michx.) |
| title_sort | genomic and transcriptomic analyses reveal polygenic architecture for ecologically important traits in aspen populus tremuloides michx |
| topic | community genetics differential expression multilocus association model omnigenic model polygenic architecture salicinoids |
| url | https://doi.org/10.1002/ece3.10541 |
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