Transcriptome-wide analysis of introgression-resistant regions reveals genetic divergence genes under positive selection in Populus trichocarpa

Abstract

Comparing gene expression patterns and genetic polymorphisms between populations is of central importance for understanding the origin and maintenance of biodiversity. Based on population-specific gene expression levels and allele frequency differences, we sought to identify population divergence (PD) genes across the introgression-resistant genomic regions of Populus trichocarpa. Genes containing highly diverged loci [i.e., genetic divergence (GD)] or showing expression divergence (ED) between populations were widely distributed in the genome and substantially enriched in functional categories related to stress responses, disease resistance, timing of flowering, cell cycle regulation, plant growth, and development. Nine genomic regions showing evidence of strong positive selection were overlapped with GD genes, which had significant differences between Oregon (a southernmost peripheral deme) and the other demes. However, we did not find evidence that genes under positive selection show an enrichment for ED. PD genes and genes under selection pertained to the same gene classes, such as SERINE/CYSTEINE PROTEASE, ABC TRANSPORTER, GLYCOSYLTRANSFERASE and other transferases. Our analysis also revealed that GD genes were polymorphic within the species (41.9 ± 3.66 biallelic variants per gene), as previously reported in herbaceous plants. By contrast, ED genes contained less genetic variants (10.73 ± 1.14) and were likely highly expressed. In addition, we found that trans- rather than cis-acting variants considerably contribute to the evolution of >90% PD genes. Overall, this study elucidates that cohorts of PD genes agree with the general attributes of known speciation genes and GD genes will provide substrates for positive selection to operate on.

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Fig. 1: Introgression-resistant transcriptome-wide portrait of population divergence at genetic and expression levels.
Fig. 2: Integrated results of transcriptomes, selective scans, and selected SNPs.
Fig. 3: Partial representation of mean individuals for each deme and groups representation based on the first six principal components (Dim 1–6) of the MFA.
Fig. 4: eQTL, clustering, and GO enrichment of ED genes.
Fig. 5: Merge of loci showing strong positive selection and PD with those distinct in Oregon.
Fig. 6: Local ancestry analysis and comparisons of gene expression (mean ± SE) and allele frequency between pure and hybrid individuals.

Data availability

The original genotyping data have been deposited on SRA under the accession PRJNA276056. The RNA-sequencing data have been deposited on SRA under the accession PRJNA300564. All the intermediate data supporting the findings of this study are available upon reasonable request.

Code availability

Custom Python scripts have been made available as a notebook appendix in the Supporting Information.

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Acknowledgements

This work was supported by funds of the Genome Canada Large-Scale Applied Research Program (POPCAN; project 168BIO) to YAE (and other leading PIs of the project team: C. J. Douglas, R. D. Guy, S. D. Mansfield, and Q. C. B. Cronk), and by a National Sciences and Engineering Research Council of Canada Discovery Grant to YAE. We thank Q. C. B. Cronk (UBC) for assistance in RNA-seq data pre-processing. We are equally grateful for Compute Canada (Cedar system) to afford part of computational simulations. Finally, we thank the Editor and anonymous referees for their helpful comments after thorough reading and granting an extended time for revision due to the COVID pandemic.

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YAE led and coordinated the project (experimental design and data collection); YL conceived of this study, performed data analyses, and wrote the manuscript with supportive inputs from YAE. All authors read and approved the final version.

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Correspondence to Yang Liu.

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Liu, Y., El-Kassaby, Y.A. Transcriptome-wide analysis of introgression-resistant regions reveals genetic divergence genes under positive selection in Populus trichocarpa. Heredity (2020). https://doi.org/10.1038/s41437-020-00388-4

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