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A Comprehensive Genomic Scan Reveals Gene Dosage Balance Impacts on Quantitative Traits in Populus Trees

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A Comprehensive Genomic Scan Reveals Gene Dosage Balance Impacts on Quantitative Traits in Populus Trees A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees Héloïse Bastiaansea,b, Matthew Zinkgrafa,1, Courtney Canninga, Helen Tsaib,c, Meric Liebermanb,c, Luca Comaib,c, Isabelle Henryb,c, and Andrew Groovera,b,2 aPacific Southwest Research Station, US Department of Agriculture Forest Service, Davis, CA 95618; bDepartment of Plant Biology, University of California, Davis, CA 95616; and cGenome Center, University of California, Davis, CA 95616 Edited by James A. Birchler, Division of Biological Sciences, University of Missouri, Columbia, MO, and approved May 24, 2019 (received for review February 22, 2019) Gene dosage variation and the associated changes in gene expres- occurring CNV occurs more frequently in gene-poor regions (12) sion influence a wide variety of traits, ranging from cancer in and usually only encompasses a small proportion of the genome. humans to yield in plants. It is also expected to affect important For instance, in apple, maize, and barley, natural CNV has been traits of ecological and agronomic importance in forest trees, but this detected only in 3.5, 10, and 14.9% of the genome, respectively (6, variation has not been systematically characterized or exploited. 13, 14), and therefore does not provide the power to systematically Here we performed a comprehensive scan of the Populus genome survey the effect of gene dosage variation on plant function. for dosage-sensitive loci affecting quantitative trait variation for Perennial growth is a fundamental feature of forest trees that spring and fall phenology and biomass production. The study pop- is not shared by herbaceous annual model plants such as Ara- ulation was a large collection of clonally propagated F1 hybrid lines bidopsis or maize. Temperate trees have strictly regulated phe- of Populus that saturate the genome 10-fold with deletions and nology, controlling the timing of onset of dormancy in insertions (indels) of known sizes and positions. As a group, the preparation for winter and the breaking of dormancy and initi- ation of growth in the spring (15). Phenology thus describes phenotypic means of the indel lines consistently differed from con- adaptive traits that balance maximizing the growing season while trol nonindel lines, with an overall negative effect of both insertions minimizing the danger of frost damage (16). Temperature and and deletions on all biomass-related traits but more diverse effects photoperiod are key agents in controlling phenology in most and an overall wider phenotypic distribution of the indel lines for the temperate woody plants (16–19). Typical of temperate trees, phenology-related traits. We also investigated the correlation be- Populus species primarily respond to shortening photoperiods in tween gene dosage at specific chromosomal locations and pheno- the late summer/early fall by developing vegetative buds con- type, to identify dosage quantitative trait loci (dQTL). Such dQTL taining preformed shoots and leaves, followed by cessation of were detected for most phenotypes examined, but stronger effect growth and dormancy (20). Exposure to a cumulative amount of dQTL were identified for the phenology-related traits than for the cold temperatures during the winter is needed to establish biomass traits. Our genome-wide screen for dosage sensitivity in a competency to respond to returning warm temperatures in the higher eukaryote demonstrates the importance of global genomic spring resulting in outgrowth of the preformed stems and leaves balance and the impact of dosage on life history traits. (bud burst). Phenology is a major determinant of geographical gene dosage | quantitative trait | forest trees | genome balance | Significance copy number variation Phenotypic trait variation can be linked to genomic sequence he causative factors underlying quantitative trait variation variation. These differences range from a single nucleotide to Thave been modeled and debated for over a century. Notably, larger insertion and deletion (indel) of chromosomal segments. Fisher’s seminal work provided the statistical framework for Indels can change the copy number of affected genes, which modeling quantitative trait variation as the cumulative effects of can create complex phenotypic trait variation through effects individual genes, whose alleles can exert additive, dominance, on gene expression. For example, gene dosage variation has and epistatic effects (1). Today, DNA sequencing technology been associated with various human chronic diseases. Here we enables genome-wide survey of allelic variation, yet significant systematically explored the effect of induced gene dosage gaps remain in the ability to fully explain the observed pheno- variation on quantitative trait variation in Populus. We show typic variation. Structural variation, including copy number var- that gene dosage variation at specific chromosomal locations iation (CNV), has been shown to affect many traits in plants and and also gene dosage balance at a global genomic scale are animals (1–7), although its relevance remains to be assessed at both major determinants of quantitative trait variation in the genome-wide level. a plant species. Mechanistically, structural variation can change the relative dosage of affected genes, which in turn can affect the concen- Author contributions: H.B., M.Z., L.C., I.H., and A.G. designed research; H.B., M.Z., C.C., tration of the encoded protein or RNA product in proportion to H.T., and M.L. performed research; H.B., L.C., and I.H. analyzed data; and H.B. wrote gene copy number (1, 8). If a molecular pathway contributing to the paper. a phenotypic trait is sensitive to dosage, a quantitative variation The authors declare no conflict of interest. of the phenotypic trait results. Differences in gene copy number This article is a PNAS Direct Submission. (or in cis-regulatory regions) have been identified as causal Published under the PNAS license. variants of previously identified plant quantitative trait loci Data deposition: The sequences reported in this paper have been deposited in the Na- (QTL), in contrast to differences in protein sequence (9, 10). So tional Center for Biotechnology Information BioProject database (accession no. far, such DNA structural variations are incompletely assessed by PRJNA241273). common genotyping approaches, and dosage effects may not 1Present address: College of Science and Engineering, Western Washington University, necessarily conform to traditional quantitative genetic models. Bellingham, WA 98225-9063. CNV and dosage may thus contribute to the missing heritability 2To whom correspondence may be addressed. Email: [email protected]. of traditional mapping studies (11). Data so far have focused This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. mostly on domesticated crops of agricultural importance and 1073/pnas.1903229116/-/DCSupplemental. suggest that although present over thousands of sites, naturally Published online June 18, 2019. 13690–13699 | PNAS | July 2, 2019 | vol. 116 | no. 27 www.pnas.org/cgi/doi/10.1073/pnas.1903229116 range (21), affects species migration in response to climate Populus deltoides female parents (Materials and Methods). Here change, and is correlated with biomass traits important for we characterized a second set of F1 hybrids from the same commercial forestry and bioenergy application. crosses, for a full population of 646 lines. We phenotyped 592 of The genetic control of phenology and biomass traits in Populus these lines in a replicated field trial (SI Appendix, Additional species has been examined at the population and molecular Table 1), carrying structural variation similar to that previously genetic levels. Population genomics of Populus trichocarpa described (SI Appendix, Additional Table 2). Briefly, ∼58% of and Populus tremula identified strong genetic differentiation the irradiated lines carried indel mutations, of which 71% were according to their geographical origin (22–24). Interestingly, in deletions and 29% were insertions. Most irradiation mutants both species, such genomic regions that were associated with were diploid, but triploid individuals were also recovered, which positive and/or divergent selection were also found to be on average carried more mutations than their diploid counter- enriched with candidate genes related to phenology. This trend parts. Indels spanned the 19 chromosomes of Populus, with each reveals the importance of natural selection in phenotypic tree region being affected by at least 1 indel and at most 31, with an adaptation (23). At the molecular level, there is evidence of average of 10 indels per chromosomal region (SI Appendix, cooption or cross talk between Arabidopsis flowering/seed dor- Additional Figs. 1 and 2). Only 6.2 Mbp (∼1.6%) of the 19 as- mancy pathways and the regulation of bud set in Populus, as well sembled chromosomes lacked any indel, corresponding to as in other plant species (25–28). Such shared pathways revealed 132 genes in the reference P. trichocarpa genome (SI Appendix, the importance of the phytohormone abscisic acid (ABA) (29, Additional Table 3). It is possible that indels in these regions 30) as well as components of the CONSTANS/FLOWERING impair plant fitness or simply that by chance no indels were re- LOCUS T (FT) regulatory module (25, 31, 32) and GIGANTEA covered in these regions. Indel mutations varied in length (from (GI)-like genes (33). Recent studies described a key component 0.3 Mbp
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