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Ingvarsson, P. K.

Publications and source records attributed to Ingvarsson, P. K..

At least 19 recordsLinked to original sources

Species-specific genetic routes to a shared phenotype: convergent adaptation of beans to European long days

The loss of photoperiod sensitivity was a key prerequisite for the adaptation of common bean (Phaseolus vulgaris) and scarlet runner bean (P. coccineus) to European environments. While the genetic architecture of this trait has been studied for decades, primarily through QTL mapping in RILs and NILs, its molecular basis remains incompletely resolved. Here, we combine whole-genome resequencing of over 200 P. vulgaris accessions spanning Mesoamerican, Andean, and European origins with 130 P. coccineus cultivars from Mesoamerica and Europe. Phenotyping under controlled long-day conditions revealed distinct distributions of photoperiod sensitivity across species and gene pools. Genome-wide association and haplotype analyses identified single nucleotide variants strongly linked to flowering under long days. Consistent with prior studies, signals of selection reflect independent domestication events in the Americas. Importantly, we detect species-specific selection on core photoperiod regulators, demonstrating that both species achieved similar adaptive outcomes via functionally convergent genetic routes. By explicitly accounting for major loci shaping growth habit in our analyses, we were able to unmask additional genomic regions contributing to flowering responses in European cultivars. Together, these results show that adaptation to long-day environments occurred through stepwise, species-specific genomic innovations, first during domestication in the Americas and later under European cultivation. Our findings highlight the role of pathway-level convergent evolution in shaping complex domestication traits and underscore the potential of parallel genomic strategies for crop adaptation.

plant biology↗

Contrasting patterns of local adaptation and climate resilience across forest management regimes in Norway spruce (Picea abies): implications for reforestation practices under climate change

This study investigates the contrasting patterns of genetic diversity and local adaptation between old-growth and recently planted Norway spruce (Picea abies) stands in northern Sweden. We assess neutral genetic variation, adaptive genetic differentiation, and the potential for future adaptation using samples collected from old-growth forests and recently planted stands. Our results reveal no significant differences in overall genetic diversity between natural and planted populations, indicating that current forest management practices have not substantially reduced genetic variation. However, analyses of adaptive variation demonstrate stronger signatures of local adaptation in old-growth populations, with clear correlations between genetic and environmental distances. In contrast, planted stands show weaker adaptive signals and are at greater risk of non-adaptiveness under future climate scenarios. These findings highlight the importance of conserving and promoting adaptive genetic variation within forest management to ensure resilience against ongoing climate change, while also recognising that current practices preserve much of the neutral genetic diversity necessary for long-term forest health.

plant biology↗

Evolutionary responses and genomic consequences of polyploidization in natural populations of Orychophragmus

Polyploidization has occurred throughout the tree of life and is particularly common in plants. Despite its ubiquity, our understanding of the short- and long-term effects and consequences of genome doubling in natural populations remains incomplete. In this study, we identified a novel ploidy-variable species system within the ornamental and industrial oilseed genus Orychophragmus (Brassicaceae), which comprises six species, including diploid and tetraploid cytotypes of O. taibaiensis. By integrating population-scale genomic and transcriptomic datasets across the species in this genus, we constructed a robust phylogenetic framework and investigated the divergence and demographic history of O. taibaiensis in comparison to its relatives. Specifically, we characterized the geographical distribution patterns of diploids and tetraploids in natural populations of O. taibaiensis, confirmed the autopolyploid origin of tetraploids, and inferred their origin time relative to diploid counterparts. Our findings further revealed that, following genome doubling, tetraploids accumulated a higher genetic load of deleterious mutations, likely due to relaxed purifying selection facilitated by allelic redundancy. Additionally, genome doubling was associated with pronounced changes in gene expression patterns, with differentially expressed genes evolving under relaxed selective constraints. These results highlight that the initial masking of deleterious mutations, changes in expression regulation, and divergent efficacy of selection likely all contribute to shaping the establishment and evolutionary potential of polyploids.

molecular biology↗

QTL mapping of the narrow-branch "Pendula" phenotype in Norway spruce (Picea abies L. Karst.)

Pendula-phenotyped Norway spruce has a potential forestry interest for high density plantations. This phenotype is believed to be caused by a dominant single mutation. Despite the availability of RAPD markers linked to the trait, the nature of the mutation is yet unknown. We performed a Quantitative Trait Loci (QTL) mapping based on two different progenies of F1 crosses between pendula and normal crowned trees using NGS technologies. Approximately 25 % of all gene bearing scaffolds of Picea abies genome assembly v1.0 were mapped to 12 linkage groups and a single QTL, positioned near the center of LG VI, was found in both crosses. The closest probe-markers placed on the maps were positioned 0.82 cM and 0.48 cM away from the Pendula marker in two independent pendula-crowned x normal-crowned wildtype crosses, respectively. We have identified genes close to the QTL region with differential mutations on coding regions and discussed their potential role in changing branch architecture.

genomics↗

Genomic insights into present local adaptation and future climate change vulnerability of a keystone forest tree species in East Asian

Rapid global climate change is posing a huge threat to biodiversity. Assessments of the adaptive capacity for most taxa is usually performed on the species as a whole, but fails to incorporate intraspecific adaptive variation that may play a fundamental role in buffering future shifting climates. Here we generate a chromosome-scale genome assembly for Populus koreana, a pioneer and keystone tree species in East Asia temperate forests. We also obtain whole-genome sequences of 230 individuals collected from 24 natural populations. An integration of population genomics and environmental variables was performed to reveal the genomic basis of local adaptation to diverse climate variable. We identify a set of climate-associated single nucleotide polymorphisms (SNPs), insertions-deletions (Indels) and structural variations (SVs), in particular numerous adaptive non-coding variants distributed across the genome of P. koreana. We incorporate these variants into an environmental modelling scheme to predict spatiotemporal responses of P. koreana to future climate change. Our results highlight the insights that the integration of genomic and climate data can shed on the future evolutionary adaptive capacities of a species to changing environmental conditions.

evolutionary biology↗

Conserved genomic landscapes of differentiation across Populus speciation continuum

Speciation, the continuous process by which new species form, is often investigated by looking at the variation of nucleotide diversity and differentiation across the genome (hereafter genomic landscapes). A key challenge lies in how to determine the main evolutionary forces at play shaping these patterns. One promising strategy, albeit little used to date, is to comparatively investigate these genomic landscapes as a progression through time by using a series of species pairs along a divergence gradient. Here, we resequenced 201 whole-genomes from eight closely related Populus species, with pairs of species at different stages along the divergence gradient to learn more about speciation processes. Using population structure and ancestry analyses, we document extensive introgression between some species pairs, especially those with parapatric distributions. We further investigate genomic landscapes, focusing on within-species (nucleotide diversity and recombination rate) and among-species (relative and absolute divergence) summary statistics of diversity and divergence. We observe highly conserved patterns of genomic divergence across species pairs. Independent of the stage across the divergence gradient, we find support for signatures of linked selection (i.e., the interaction between natural selection and genetic linkage) in shaping these genomic landscapes, along with gene flow and standing genetic variation. We highlight the importance of investigating genomic patterns on multiple species across a divergence gradient and discuss prospects to better understand the evolutionary forces shaping the genomic landscapes of diversity and differentiation.

evolutionary biology↗

GIGANTEA gene expression influence leaf senescence in Populus in two different ways

GIGANTEA (GI) genes have a central role in plant development and influence several processes such as light signaling, circadian rhythm and abiotic stress tolerance. Hybrid aspen T89 (Populus tremula x tremuloides) trees with low GI expression through RNAi have a severely compromised growth. In order to study the effect of reduced GI expression on leaf traits with special emphasis on leaf senescence, we grafted GI-RNAi scions onto wild type (WT) rootstocks and managed to restore scions growth. The RNAi line had distorted leaf shape and reduced photosynthesis, probably caused by modulating phloem or stomatal function, increased starch accumulation, higher carbon-to-nitrogen (C/N) ratio and a reduced capacity to withstand moderate light stress. GI-RNAi also induced senescence under long day (LD) and moderate light conditions. Furthermore, the GI-RNAi lines were affected in their capacity to respond to "autumn environmental cues" inducing senescence, a type of leaf senescence with characteristics different from senescence induced directly by stress under LD conditions. Whereas Overexpression of GI delayed senescence. The two different effects on leaf senescence were not affected by the expression of FT (Flowering locus T), were "local" - they followed the genotype of the branch independent on the position in the tree - and trees with modified gene expression grown in the field were affected in a similar way as under controlled conditions. Taken together, GI plays a central role to sense the environmental changes during autumn and determine the appropriate timing for leaf senescence in Populus. One sentence summaryLeaf senescence is a complex process that is not well understood, but this paper shows that changing the expression of one gene could influence leaf senescence in Populus trees in two separate ways.

plant biology↗

Adaptive introgression and standing genetic variation, two facilitators of adaptation to high latitudes in European aspen (Populus tremula L.)

Understanding local adaptation in plants from a genomic perspective has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole genome re-sequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum (LGM), we detected an adaptive introgression event in a genome region of [~]500kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin - probably Russian - of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results therefore emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.

evolutionary biology↗

Barriers to gene flow play an important role in miantaining reproductive isolation between two closely related Populus (Salicaceae) species

In most species, natural selection plays a key role in genomic heterogeneous divergence. Additionally, barriers to gene flow, such as chromosomal rearrangements or gene incompatibilities, can cause genome heterogeneity. We used genome-wide re-sequencing data from 27 Populus alba and 28 P. adenopoda individuals to explore the causes of genomic heterogeneous differentiation in these two closely related species. In highly differentiated regions, neutrality tests (Tajimas D and Fay & Wus H) revealed no difference while the absolute divergence (dxy) were significantly higher than genome background, which indicates that natural selection did not play a major role but barriers to gene flow play an important role in generating genomic heterogeneous divergence and reproductive isolation. The two species diverged [~]5-10 million years ago (Mya), when the Qinghai-Tibet Plateau reached a certain height and the inland climate of the Asian continent became arid. We further found some genes that are related to reproduction.

evolutionary biology↗

Quantifying adaptive evolution and the effects of natural selection across the Norway spruce genome

Detecting natural selection is one of the major goals of evolutionary genomics. Here, we sequence whole genomes of 34 Picea abies individuals and quantify the amount of selection across the genome. Using an estimate of the distribution of fitness effects, we show that negative selection is very limited in coding regions, while positive selection is rare in coding regions but very strong in non-coding regions, suggesting the great importance of regulatory changes in evolution of Norway spruce. Additionally, we found a positive correlation between adaptive rate with recombination rate and a negative correlation between adaptive rate and gene density, suggesting a widespread influence from Hill-Robertson interference to efficiency of protein adaptation in P. abies. Finally, the distinct population statistics between genomic regions under either positive or balancing selection with that under neutral regions indicated impact from selection to genomic architecture of Norway spruce. Further gene ontology enrichment analysis for genes located in regions identified as undergoing either positive or long-term balancing selection also highlighted specific molecular functions and biological processes in that appear to be targets of selection in Norway spruce.

evolutionary biology↗

The genetic basis of adaptation in phenology in an introduced population of Black Cottonwood (Populus trichocarpa, Torr. & Gray)

O_LIEntering and exiting winter dormancy presents important trade-offs between growth and survival at northern latitudes and many forest trees display local adaptation across latitude. Transfers of a species outside its native range introduce the species to novel combinations of environmental conditions potentially requiring different combinations of alleles to optimize growth. C_LIO_LIWe performed genome wide association analyses and a selection scan in a P. trichocarpa mapping population derived from crossings between clones collected across the native range and introduced into Sweden. GWAS analyses were performed using phenotypic data collected across two field seasons and in a controlled phytotron experiment. C_LIO_LIWe uncovered 629 putative candidate genes associated with spring and autumn phenology traits as well as with growth. Many regions harboring variation significantly associated with the initiation of leaf shed and leaf autumn coloring appeared to have been evolving under positive selection in the native environments of P. trichocarpa. C_LIO_LIA comparison between the candidate genes identified with results from earlier GWAS analyses performed in the native environment found a smaller overlap for spring phenology traits than for autumn phenology traits, aligning well with earlier observations that spring phenology transitions have a more complex genetic basis that autumn phenology transitions. C_LI

evolutionary biology↗

Quantitative genetic architecture of adaptive phenology traits in the deciduous tree, Populus trichocarpa (Torr. & Gray).

In a warming climate, the ability to accurately predict and track shifting environmental conditions will be fundamental for plant survival. Environmental cues define the transitions between growth and dormancy as plants synchronise development with favourable environmental conditions, however these cues are predicted to change under future climate projections which may have profound impacts on tree survival and growth. Here, we use a quantitative genetic approach to estimate the genetic basis of spring and autumn phenology in Populus trichocarpa to determine this species capacity for climate adaptation. We measured bud burst, leaf coloration, and leaf senescence traits across two years (2017-2018) and combine these observations with measures of lifetime growth to determine how genetic correlations between phenology and growth may facilitate or constrain adaptation. Timing of transitions differed between years, although we found strong cross year genetic correlations in all traits, suggesting that genotypes respond in consistent ways to seasonal cues. Spring and autumn phenology were correlated with lifetime growth, where genotypes that burst leaves early and shed them late had the highest lifetime growth. We also identified substantial heritable variation in the timing of all phenological transitions (h2 = 0.5-0.8) and in lifetime growth (h2 = 0.8). The combination of abundant additive variation and favourable genetic correlations in phenology traits suggests that cultivated varieties of P. trichocarpa have the capability to create populations which may adapt their phenology to climatic changes without negative impacts on growth.

genetics↗

Integrating genome-wide association mapping of additive and dominance genetic effects to improve genomic prediction accuracy in Eucalyptus

Genome-wide association studies (GWAS) is a powerful and widely used approach to decipher the genetic control of complex traits. A major challenge for dissecting quantitative traits in forest trees is statistical power. In this study, we use a population consisting of 1123 samples from two successive generations that have been phenotyped for growth and wood property traits and genotyped using the EuChip60K chip, yielding 37,832 informative SNPs. We use multi-locus GWAS models to assess both additive and dominance effects to identify markers associated with growth and wood property traits in the eucalypt hybrids. Additive and dominance association models identified 78 and 82 significant SNPs across all traits, respectively, which captured between 39 and 86% of the genomic-based heritability. We also used SNPs identified from the GWAS and SNPs using less stringent significance thresholds to evaluate predictive abilities in a genomic selection framework. Genomic selection models based on the top 1% SNPs captured a substantially greater proportion of the genetic variance of traits compared to when all SNPs were used for model training. The prediction ability of estimated breeding values was significantly improved for all traits using either the top 1% SNPs or SNPs identified using a relaxed p-value threshold (p<10-3). This study highlights the added value of also considering dominance effects for identifying genomic regions controlling growth traits in trees. Moreover, integrating GWAS results into genomic selection method provides enhanced power relative to discrete associations for identifying genomic variation potentially useful in tree breeding.

genetics↗

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Increasing our understanding of how various evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, the genome-wide patterns of within- and between-species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole-genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories, investigate patterns of diversity and divergence, infer their genealogical relationships and estimate the extent of ancient introgression across the genome. Our results show substantial variation in these patterns along the genomes although this variation is not randomly distributed but is strongly predicted by the local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long-term balancing selection are also crucial components in shaping patterns of genome-wide variation during the speciation process.

evolutionary biology↗

Demography and natural selection have shaped genome-wide variation in the widely distributed conifer Norway Spruce (Picea abies)

Under the neutral theory, species with larger effective population sizes are expected to harbour higher genetic diversity. However, across a wide variety of organisms, the range of genetic diversity is orders of magnitude more narrow than the range of effective population size. This observation has become known as Lewontins paradox and although aspects of this phenomenon have been extensively studied, the underlying causes for the paradox remain unclear. Norway spruce (Picea abies) is a widely distributed conifer species across the northern hemisphere and it consequently plays a major role in European forestry. Here, we use whole-genome re-sequencing data from 35 individuals to perform population genomic analyses in P. abies in an effort to understand what drives genome-wide patterns of variation in this species. Despite having a very wide geographic distribution and an enormous current population size, our analyses find that genetic diversity of P.abies is low across a number of populations (p=0.005-0.006). To assess the reasons for the low levels of genetic diversity, we infer the demographic history of the species and find that it is characterised by several re-occurring bottlenecks with concomitant decreases in effective population size can, at least partly, provide an explanation for low polymorphism we observe in P. abies. Further analyses suggest that recurrent natural selection, both purifying and positive selection, can also contribute to the loss of genetic diversity in Norway spruce by reducing genetic diversity at linked sites. Finally, the overall low mutation rates seen in conifers can also help explain the low genetic diversity maintained in Norway spruce.

evolutionary biology↗

Variant calling using NGS and sequence capture data for population and evolutionary genomic inferences in Norway Spruce (Picea abies)

Advances in next-generation sequencing methods and the development of new statistical and computational methods have opened up possibilities made for large-scale, high quality genotyping in most organisms. Conifer genomes are large and are known to contain a high fraction of repetitive elements and this complex genome structure has bearings for approaches that aim to use next-generation sequencing methods for genotyping. In this chapter we provide a detailed description of a workflow for variant calling using next-generation sequencing in Norway spruce (Picea abies). The workflow that starts with raw sequencing reads and proceeds through read mapping to variant calling and variant filtering. We illustrate the pipeline using data derived from both whole-genome resequencing data and reduced-representation sequencing. We highlight possible problems and pitfalls of using next-generation sequencing data for genotyping stemming from the complex genome structure of conifers and how those issues can be mitigated or eliminated.

bioinformatics↗

Constructing a high-density linkage map to infer the genomic landscape of recombination rate variation in European Aspen (Populus tremula)

The rate of meiotic recombination is one of the central factors determining levels of linkage disequilibrium and the efficiency of natural selection, and many organisms show a positive correlation between local rates of recombination and levels of nucleotide diversity indicating that linked selection is an important factor determining genome-wide levels of nucleotide diversity. Several methods for estimating recombination rates from segregating polymorphisms in natural populations have recently been developed. These methods have been extensively used in part because they are relatively simple to implement even in many non-model organisms, but also because they potentially offer higher resolution than traditional map-based methods. However, thorough comparisons of LD and map-based estimates of recombination are not readily available in plants. Here we present a new, high-resolution linkage map for Populus tremula and use this to estimate variation in recombination rates across the P. tremula genome. We compare these results to recombination rates estimated based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identify a number of genomic regions with very high recombination rates that the map-based method fail to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome.

evolutionary biology↗

Association mapping identified novel candidate loci affecting wood formation in Norway spruce

[tpltrtarr] Norway spruce (Picea abies) is an important boreal forest tree species of significant ecological and economic importance. Hence there is a strong imperative to dissect the genetics controlling important wood quality traits in the species.\n[tpltrtarr]We performed a functional genome-wide association mapping of 17 wood traits in Norway spruce using 178101 single-nucleotide polymorphisms (SNPs) generated from exome genotyping of 517 mother trees. The wood traits were defined using functional modelling of wood properties across annual growth rings.\n[tpltrtarr]Association mapping was performed using a multilocus LASSO penalized regression method and we detected a total of 51 significant SNPs from 39 candidate genes that are involved in wood formation.\n[tpltrtarr]Our study represents the first functional multi-locus genome-wide association mapping (AM) in Norway spruce. The results advance our understanding of the genetics influencing wood traits, identify novel candidate genes for further functional studies and support current Norway spruce breeding efforts.

genetics↗