Adaptation to new environments can start from new mutations or from standing variation already present in natural populations. Whether admixture constrains or facilitates adaptation from standing variation is largely unknown, especially in ecological keystone or foundation species. We examined patterns of neutral and adaptive population divergence in Populus tremula L., a widespread forest tree, using mapped molecular genetic markers. We detected the genetic signature of postglacial admixture between a Western and an Eastern lineage of P. tremula in Scandinavia, an area suspected to represent a zone of postglacial contact for many species of animals and plants. Stringent divergence‐based neutrality tests provided clear indications for locally varying selection at the European scale. Six of 12 polymorphisms under selection were located less than 1 kb away from the nearest gene predicted by the Populus trichocarpa genome sequence. Few of these loci exhibited a signature of ‘selective sweeps’ in diversity‐based tests, which is to be expected if adaptation occurs primarily from standing variation. In Scandinavia, admixture explained genomic patterns of ancestry and the nature of clinal variation and strength of selection for bud set, a phenological trait of great adaptive significance in temperate trees, measured in a common garden trial. Our data provide a hitherto missing direct link between past range shifts because of climatic oscillations, and levels of standing variation currently available for selection and adaptation in a terrestrial foundation species.
Background: Sex chromosomes have arisen independently in a wide variety of species, yet they share common characteristics, including the presence of suppressed recombination surrounding sex determination loci. Mammalian sex chromosomes contain multiple palindromic repeats across the non-recombining region that show sequence conservation through gene conversion and contain genes that are crucial for sexual reproduction. In plants, it is not clear if palindromic repeats play a role in maintaining sequence conservation in the absence of homologous recombination. Results: Here we present the first evidence of large palindromic structures in a plant sex chromosome, based on a highly contiguous assembly of the W chromosome of the dioecious shrub Salix purpurea. The W chromosome has an expanded number of genes due to transpositions from autosomes. It also contains two consecutive palindromes that span a region of 200 kb, with conspicuous 20-kb stretches of highly conserved sequences among the four arms that show evidence of gene conversion. Four genes in the palindrome are homologous to genes in the sex determination regions of the closely related genus Populus, which is located on a different chromosome. These genes show distinct, floral-biased expression patterns compared to paralogous copies on autosomes. Conclusion: The presence of palindromes in sex chromosomes of mammals and plants highlights the intrinsic importance of these features in adaptive evolution in the absence of recombination. Convergent evolution is driving both the independent establishment of sex chromosomes as well as their fine-scale sequence structure.
Summary Genome‐wide association studies (GWAS) have great promise for identifying the loci that contribute to adaptive variation, but the complex genetic architecture of many quantitative traits presents a substantial challenge. We measured 14 morphological and physiological traits and identified single nucleotide polymorphism (SNP)‐phenotype associations in a Populus trichocarpa population distributed from California, USA to British Columbia, Canada. We used whole‐genome resequencing data of 882 trees with more than 6.78 million SNPs, coupled with multitrait association to detect polymorphisms with potentially pleiotropic effects. Candidate genes were validated with functional data. Broad‐sense heritability (H2) ranged from 0.30 to 0.56 for morphological traits and 0.08 to 0.36 for physiological traits. In total, 4 and 20 gene models were detected using the single‐trait and multitrait association methods, respectively. Several of these associations were corroborated by additional lines of evidence, including co‐expression networks, metabolite analyses, and direct confirmation of gene function through RNAi. Multitrait association identified many more significant associations than single‐trait association, potentially revealing pleiotropic effects of individual genes. This approach can be particularly useful for challenging physiological traits such as water‐use efficiency or complex traits such as leaf morphology, for which we were able to identify credible candidate genes by combining multitrait association with gene co‐expression and co‐methylation data.
Dioecy has evolved numerous times in plants, but heteromorphic sex chromosomes are apparently rare. Sex determination has been studied in multiple Salix and Populus (Salicaceae) species, and P. trichocarpa has an XY sex determination system on chromosome 19, while S. suchowensis and S. viminalis have a ZW system on chromosome 15. Here we use whole genome sequencing coupled with quantitative trait locus mapping and a genome-wide association study to characterize the genomic composition of the non-recombining portion of the sex determination region. We demonstrate that Salix purpurea also has a ZW system on chromosome 15. The sex determination region has reduced recombination, high structural polymorphism, an abundance of transposable elements, and contains genes that are involved in sex expression in other plants. We also show that chromosome 19 contains sex-associated markers in this S. purpurea assembly, along with other autosomes. This raises the intriguing possibility of a translocation of the sex determination region within the Salicaceae lineage, suggesting a common evolutionary origin of the Populus and Salix sex determination loci.
1 Background 2 Sex chromosomes in a wide variety of species share common characteristics, including the 3 presence of suppressed recombination surrounding sex determination loci. They have arisen 4 independently in numerous lineages, providing a conclusive example of convergent evolution. 5Mammalian sex chromosomes contain multiple palindromic repeats across the non-recombining 6 region that facilitate sequence conservation through gene conversion, and contain genes that are 7 crucial for sexual reproduction. Plant sex chromosomes are less well understood, and in 8 particular it is not clear how coding sequence conservation is maintained in the absence of 9 homologous recombination. 10 Results 11 Here we present the first evidence of large palindromic structures in a plant sex chromosome, 12 based on a highly contiguous assembly of the W chromosome of the dioecious shrub Salix 13 purpurea. Two consecutive palindromes span over a region of 200 kb, with conspicuous 20 kb 14 stretches of highly conserved sequences among the four arms. The closely-related species S. 15 suchowensis also has two copies of a portion of the palindrome arm and provides strong 16 evidence for gene conversion. Four genes in the palindrome are homologous to genes in the SDR 17 of the closely-related genus Populus, which is located on a different chromosome. These genes 18 show distinct, floral-biased expression patterns compared to paralogous copies on autosomes.19 Conclusion 20The presence of palindromic structures in sex chromosomes of mammals and plants highlights 21 the intrinsic importance of these features in adaptive evolution in the absence of recombination. 22Convergent evolution is driving both the independent establishment of sex chromosomes as well 23 as their fine-scale sequence structure. 24 26 103 297 kb in length lacked mapped markers and could not be placed unambiguously. 104Location of the SDR 105 We repeated sex association analysis with our new assembly with Chr15Z removed. 106Among 54,959 tested SNPs, all 105 significantly sex-associated SNPs were present only on 107 Chr15W (Fig. 1a; Additional File 2: Figure S2a-c), and markers from PARs and other scaffolds 108 in the main genome did not show any sex association (Additional File 2: Figure S2a). The eight 109 top-ranking sex-associated markers were distributed from 7.66 Mb to 8.66 Mb. Sex-associated 110 markers were primarily heterozygous in females and homozygous in males, confirming our 111 previously-reported observation of ZW sex determination in S. purpurea [18].
Molecular genetic analyses of experimental crosses provide important information on the strength and nature of postmating barriers to gene exchange between divergent populations, which are topics of great interest to evolutionary geneticists and breeders. Although not a trivial task in longlived organisms such as trees, experimental interspecific recombinants can sometimes be created through controlled crosses involving natural F 1 's. Here, we used this approach to understand the genetics of post-mating isolation and barriers to introgression in Populus alba and Populus tremula, two ecologically divergent, hybridizing forest trees. We studied 86 interspecific backcross (BC 1 ) progeny and 4350 individuals from natural populations of these species for up to 98 nuclear genetic markers, including microsatellites, indels and single nucleotide polymorphisms, and inferred the origin of the cytoplasm of the cross with plastid DNA. Genetic analysis of the BC 1 revealed extensive segregation distortions on six chromosomes, and 490% of these (12 out of 13) favored P. tremula donor alleles in the heterospecific genomic background. Since selection was documented during early diploid stages of the progeny, this surprising result was attributed to epistasis, cyto-nuclear coadaptation, heterozygote advantage at nuclear loci experiencing introgression or a combination of these. Our results indicate that gene flow across 'porous' species barriers affects these poplars and aspens beyond neutral, Mendelian expectations and suggests the mechanisms responsible. Contrary to expectations, the Populus sex determination region is not protected from introgression. Understanding the population dynamics of the Populus sex determination region will require tests based on natural interspecific hybrid zones.
Uncovering the genetic architecture of species differences is of central importance for understanding the origin and maintenance of biological diversity. Admixture mapping can be used to identify the number and effect sizes of genes that contribute to the divergence of ecologically important traits, even in taxa that are not amenable to laboratory crosses because of their long generation time or other limitations. Here, we apply admixture mapping to naturally occurring hybrids between two ecologically divergent Populus species. We map quantitative trait loci for eight leaf morphological traits using 77 mapped microsatellite markers from all 19 chromosomes of Populus. We apply multivariate linear regression analysis allowing the modeling of additive and non-additive gene action and identify several candidate genomic regions associated with leaf morphology using an information-theoretic approach. We perform simulation studies to assess the power and limitations of admixture mapping of quantitative traits in natural hybrid populations for a variety of genetic architectures and modes of gene action. Our results indicate that (1) admixture mapping has considerable power to identify the genetic architecture of species differences if sample sizes and marker densities are sufficiently high, (2) modeling of non-additive gene action can help to elucidate the discrepancy between genotype and phenotype sometimes seen in interspecific hybrids, and (3) the genetic architecture of leaf morphological traits in the studied Populus species involves complementary and overdominant gene action, providing the basis for rapid adaptation of these ecologically important forest trees.
Biological organisms are complex systems that are composed of functional networks of interacting molecules and macro-molecules. Complex phenotypes are the result of orchestrated, hierarchical, heterogeneous collections of expressed genomic variants. However, the effects of these variants are the result of historic selective pressure and current environmental and epigenetic signals, and, as such, their co-occurrence can be seen as genome-wide correlations in a number of different manners. Biomass recalcitrance (i.e., the resistance of plants to degradation or deconstruction, which ultimately enables access to a plant's sugars) is a complex polygenic phenotype of high importance to biofuels initiatives. This study makes use of data derived from the re-sequenced genomes from over 800 different Populus trichocarpa genotypes in combination with metabolomic and pyMBMS data across this population, as well as co-expression and co-methylation networks in order to better understand the molecular interactions involved in recalcitrance, and identify target genes involved in lignin biosynthesis/degradation. A Lines Of Evidence (LOE) scoring system is developed to integrate the information in the different layers and quantify the number of lines of evidence linking genes to target functions. This new scoring system was applied to quantify the lines of evidence linking genes to lignin-related genes and phenotypes across the network layers, and allowed for the generation of new hypotheses surrounding potential new candidate genes involved in lignin biosynthesis in P. trichocarpa, including various AGAMOUS-LIKE genes. The resulting Genome Wide Association Study networks, integrated with Single Nucleotide Polymorphism (SNP) correlation, co-methylation, and co-expression networks through the LOE scores are proving to be a powerful approach to determine the pleiotropic and epistatic relationships underlying cellular functions and, as such, the molecular basis for complex phenotypes, such as recalcitrance.
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