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  • 1. Baison, John
    et al.
    Vidalis, Amaryllis
    Zhou, Linghua
    Chen, Zhi-Qiang
    Li, Zitong
    Sillanpaeae, Mikko J.
    Bernhardsson, Carolina
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Scofield, Douglas
    Forsberg, Nils
    Grahn, Thomas
    Olsson, Lars
    Karlsson, Bo
    Wu, Harry
    Ingvarsson, Pär
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Lundqvist, Sven-Olof
    Niittylae, Totte
    Garcia-Gil, M. Rosario
    Genome-wide association study identified novel candidate loci affecting wood formation in Norway spruce2019In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313XArticle in journal (Refereed)
    Abstract [en]

    Norway spruce is a boreal forest tree species of significant ecological and economic importance. Hence there is a strong imperative to dissect the genetics underlying important wood quality traits in the species. We performed a functional genome-wide association study (GWAS) of 17 wood traits in Norway spruce using 178 101 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. We applied a Least Absolute Shrinkage and Selection Operator (LASSO-based) association mapping method using a functional multilocus mapping approach that utilizes latent traits, with a stability selection probability method as the hypothesis testing approach to determine a significant quantitative trait locus. The analysis provided 52 significant SNPs from 39 candidate genes, including genes previously implicated in wood formation and tree growth in spruce and other species. Our study represents a multilocus GWAS for complex wood traits in Norway spruce. The results advance our understanding of the genetics influencing wood traits and identifies candidate genes for future functional studies.

  • 2. Barker, Hilary L.
    et al.
    Riehl, Jennifer F.
    Bernhardsson, Carolina
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Rubert-Nason, Kennedy F.
    Holeski, Liza M.
    Ingvarsson, Pär K.
    Lindroth, Richard L.
    Linking plant genes to insect communities: Identifying the genetic bases of plant traits and community composition2019In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294XArticle in journal (Refereed)
    Abstract [en]

    Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Thus far, research has shown that plant genetics can underlie variation in the composition of associated communities (e.g., insects, lichen and endophytes), and those communities can therefore be considered as extended phenotypes. This work, however, has been conducted primarily at the plant genotype level and has not identified the key underlying genes. To address this gap, we used genome‐wide association mapping with a population of 445 aspen (Populus tremuloides) genets to identify the genes governing variation in plant traits (defence chemistry, bud phenology, leaf morphology, growth) and insect community composition. We found 49 significant SNP associations in 13 Populus genes that are correlated with chemical defence compounds and insect community traits. Most notably, we identified an early nodulin‐like protein that was associated with insect community diversity and the abundance of interacting foundation species (ants and aphids). These findings support the concept that particular plant traits are the mechanistic link between plant genes and the composition of associated insect communities. In putting the “genes” into “genes to ecosystems ecology”, this work enhances understanding of the molecular genetic mechanisms that underlie plant–insect associations and the consequences thereof for the structure of ecological communities.

  • 3.
    Bernhardsson, Carolina
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Molecular population genetics of inducible defense genes in Populus tremula2012Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Plant-herbivore interactions are among the most common of ecological interactions. It is therefore not surprising that plants have evolved multiple mechanisms to defend themselves, using both constitutive chemical and physical barriers and by induced responses which are only expressed after herbivory has occurred. Herbivores, on the other hand, respond to these plant defenses by evolving counter-adaptations which makes defenses less effective or even useless. Adaptation can occur at different geographical scales, with varying coevolutionary interactions across a spatially heterogenous landscape. By looking at the underlying genes responsible for these defensive traits and herbivore related phenotypic traits, it is possible to investigate the coevolutionary history of these plant- herbivore interactions. Here I use molecular population genetic tools to investigate the evolutionary history of several inducible defense genes in European Aspen (Populus tremula) in Sweden. Two genes, belonging to the Polyphenol oxidase gene-family (PPO1 and PPO2), show skews in their site frequency spectrum together with patterns of diversity and divergence from an outgroup which correspond to signatures of adaptive evolution (Paper II). 71 single nucleotide polymorphisms (SNPs) from seven inducible defense genes (PPO1-PPO3, TI2-TI5) show elevated levels of population differentiation compared to control genes (genes not involved in plant defense), and 10 of these defense SNPs show strong signatures of natural selection (Paper III). These 71 defense SNPs also divides a sample of Swedish P. tremula trees into three distinct geographical groups, corresponding to a Southern, Central and Northern cluster, a patterns that is not present in control SNPs (Paper III). The same geographical pattern, with a distinct Northern cluster, is also observed in several phenotypic traits related to herbivory in our common garden in Sävar (Paper IV). These phenotypic traits show patterns of apparent local maladaptation of the herbivore community to the host population which could indicate the presence of “information coevolution” between plants and herbivores (Paper IV). 15 unique defense SNPs also show significant associations to eight phenotypic traits but the causal effects of these SNP associations may be confounded by the geographic structure found in both the underlying genes and in the phenotypic traits. The co-occurrence of population structure in both defense genes and herbivore community traits may be the result from historical events during the post-glacial recolonization of Sweden.

  • 4.
    Bernhardsson, Carolina
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ingvarsson, Pär
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Geographic structure and adaptive population differentiation in herbivore defence genes in European aspen (Populus tremula L., Salicaceae)2012In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 21, no 9, p. 2197-2207Article in journal (Refereed)
    Abstract [en]

    When a phenotypic trait is subjected to spatially variable selection and local adaptation, the underlying genes controlling the trait are also expected to show strong patterns of genetic differentiation since alternative alleles are favored in different geographical locations. Here we study 71 SNPs from seven genes associated with inducible defense responses in a sample of P. tremula collected from across Sweden. Four of these genes (PPO2, TI2, TI4 and TI5) show substantial population differentiation and a PCA conducted on the defense SNPs divides the Swedish population into three distinct clusters. Several defense SNPs show latitudinal clines, although these were not robust to multiple testing. However, five SNPs (located within TI4 and TI5) show strong longitudinal clines that remain significant after multiple test correction. Genetic geographical variation, supporting local adaptation, has earlier been confirmed in genes involved in the photoperiod pathway in P. tremula, but this is, to our knowledge, one of the first times that geographic variation has been found in genes involved in plant defense against antagonists.

  • 5.
    Bernhardsson, Carolina
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Ingvarsson, Pär K
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Molecular population genetics of elicitor-induced resistance genes in European aspen (Populus tremula L., Salicaceae)2011In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 9, p. e24867-Article in journal (Refereed)
    Abstract [en]

    Owing to their long life span and ecological dominance in many communities, forest trees are subject to attack from a diverse array of herbivores throughout their range, and have therefore developed a large number of both constitutive and inducible defenses. We used molecular population genetics methods to examine the evolution of eight genes in European aspen, Populus tremula, that are all associated with defensive responses against pests and/or pathogens, and have earlier been shown to become strongly up-regulated in poplars as a response to wounding and insect herbivory. Our results show that the majority of these defense genes show patterns of intraspecific polymorphism and site-frequency spectra that are consistent with a neutral model of evolution. However, two of the genes, both belonging to a small gene family of polyphenol oxidases, show multiple deviations from the neutral model. The gene PPO1 has a 600 bp region with a highly elevated K(A)/K(S) ratio and reduced synonymous diversity. PPO1 also shows a skew toward intermediate frequency variants in the SFS, and a pronounced fixation of non-synonymous mutations, all pointing to the fact that PPO1 has been subjected to recurrent selective sweeps. The gene PPO2 shows a marked excess of high frequency, derived variants and shows many of the same trends as PPO1 does, even though the pattern is less pronounced, suggesting that PPO2 might have been the target of a recent selective sweep. Our results supports data from both Populus and other species which have found that the the majority of defense-associated genes show few signs of selection but that a number of genes involved in mediating defense against herbivores show signs of adaptive evolution.

  • 6.
    Bernhardsson, Carolina
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Robinson, Kathryn M.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Abreu, Ilka N.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Albrectsen, Benedicte R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Univ Copenhagen, Sect Plant Biochem, Dept Plant & Environm Sci, DK-1871 Frederiksberg, Denmark.
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Geographic structure in metabolome and herbivore community co-occurs with genetic structure in plant defence genes2013In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 16, no 6, p. 791-798Article in journal (Refereed)
    Abstract [en]

    Plantherbivore interactions vary across the landscape and have been hypothesised to promote local adaption in plants to the prevailing herbivore regime. Herbivores that feed on European aspen (Populus tremula) change across regional scales and selection on host defence genes may thus change at comparable scales. We have previously observed strong population differentiation in a set of inducible defence genes in Swedish P. tremula. Here, we study the geographic patterns of abundance and diversity of herbivorous insects, the untargeted metabolome of the foliage and genetic variation in a set of wound-induced genes and show that the geographic structure co-occurs in all three data sets. In response to this structure, we observe local maladaptation of herbivores, with fewer herbivores on local trees than on trees originated from more distant localities. Finally, we also identify 28 significant associations between single nucleotide polymorphisms SNPs from defence genes and a number of the herbivore traits and metabolic profiles.

  • 7.
    Bernhardsson, Carolina
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Robinson, Kathryn M.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Abreu, Ilka N.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Albrectsen, Benedicte R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Population differentiation in arthropod community structure and phenotypic association with inducible defense genes in European Aspen (Populus tremula L., salicaceae)Manuscript (preprint) (Other academic)
    Abstract [en]

    Plant-herbivore interactions are known to vary across a landscape due to both variation in abiotic and biotic factors. Such spatial variation tends to promoting local adaption of plants to the prevailing herbivore regime. Here we use data from a common garden to look for patterns across populations in the abundance and diversity of herbivorous insects. We also screen for variation in the untargeted metabolome of the foliage of a subset of the same trees. We also search for phenotypic associations between genetic variation in a number of wound-induced genes and phenotypic variation in herbivore abundance, diversity and in metabolomes. We observe significant genetic variation in a number of herbivore-related traits but low correlations between traits. We do observe substantial genetic structure in both herbivore community structure and in metabolic profiles and this structure is aligned with genetic structure we have previously documented for a set of defense genes. We also identify a number of significant associations between SNPs from wound-induced defense genes and a number of the herbivore traits and metabolic profiles. However, these associations are likely not causal, but are rather caused by the underlying population structure we observe. These results highlight to the importance of historical processes and the need to better understand both the current-day geographic distribution of different herbivore species as well as the post-glacial colonization history of both plants and herbivores.

  • 8.
    Bernhardsson, Carolina
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Science, Umeå, Sweden; Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Science, Uppsala, Sweden.
    Vidalis, Amaryllis
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Population Genetics, Center of Life and Food Sciences Weihenstephan, Technische Universität München.
    Wang, Xi
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Science, Uppsala, Sweden.
    Scofield, Douglas
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Uppsala Multidisciplinary Center for Advanced Computational Science; Department of Ecology and Genetics: Evolutionary Biology, Uppsala University, Uppsala, Sweden.
    Schiffthaler, Bastian
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Baison, John
    Street, Nathaniel
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Garcia-Gil, M. Rosario
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Science, Uppsala, Sweden.
    An Ultra-Dense Haploid Genetic Map for Evaluating the Highly Fragmented Genome Assembly of Norway Spruce (Picea abies)2019In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 9, no 5, p. 1623-1632Article in journal (Refereed)
    Abstract [en]

    Norway spruce (Picea abies (L.) Karst.) is a conifer species of substanital economic and ecological importance. In common with most conifers, the P. abies genome is very large (similar to 20 Gbp) and contains a high fraction of repetitive DNA. The current P. abies genome assembly (v1.0) covers approximately 60% of the total genome size but is highly fragmented, consisting of >10 million scaffolds. The genome annotation contains 66,632 gene models that are at least partially validated (), however, the fragmented nature of the assembly means that there is currently little information available on how these genes are physically distributed over the 12 P. abies chromosomes. By creating an ultra-dense genetic linkage map, we anchored and ordered scaffolds into linkage groups, which complements the fine-scale information available in assembly contigs. Our ultra-dense haploid consensus genetic map consists of 21,056 markers derived from 14,336 scaffolds that contain 17,079 gene models (25.6% of the validated gene models) that we have anchored to the 12 linkage groups. We used data from three independent component maps, as well as comparisons with previously published Picea maps to evaluate the accuracy and marker ordering of the linkage groups. We demonstrate that approximately 3.8% of the anchored scaffolds and 1.6% of the gene models covered by the consensus map have likely assembly errors as they contain genetic markers that map to different regions within or between linkage groups. We further evaluate the utility of the genetic map for the conifer research community by using an independent data set of unrelated individuals to assess genome-wide variation in genetic diversity using the genomic regions anchored to linkage groups. The results show that our map is sufficiently dense to enable detailed evolutionary analyses across the P. abies genome.

  • 9.
    Hall, David
    et al.
    Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
    Tegström, Carolina
    Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
    Ingvarsson, Pär K
    Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
    Using association mapping to dissect the genetic basis of complex traits in plants2010In: Briefings in Functional Genomics & Proteomics, ISSN 1473-9550, E-ISSN 1477-4062, Vol. 9, no 2, p. 157-165Article in journal (Refereed)
    Abstract [en]

    Association or linkage disequilibrium mapping has become a very popular method for dissecting the genetic basis of complex traits in plants. The benefits of association mapping, compared with traditional quantitative trait locus mapping, is, for example, a relatively detailed mapping resolution and that it is far less time consuming since no mapping populations need to be generated. The surge of interest in association mapping has been fueled by recent developments in genomics that allows for rapid identification and scoring of genetic markers which has traditionally limited mapping experiments. With the decreasing cost of genotyping future emphasis will likely focus on phenotyping, which can be both costly and time consuming but which is crucial for obtaining reliable results in association mapping studies. In addition, association mapping studies are prone to the identification of false positives, especially if the experimental design is not rigorously controlled. For example, population structure has long been known to induce many false positives and accounting for population structure has become one of the main issues when implementing association mapping in plants. Also, with increasing numbers of genetic markers used, the problem becomes separating true from false positive and this highlights the need for independent validation of identified association. With these caveats in mind, association mapping nevertheless shows great promise for helping us understand the genetic basis of complex traits of both economic and ecological importance.

  • 10.
    Johansson, Anna-Mia
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Centre for Molecular Pathogenesis (UCMP) (Faculty of Science and Technology).
    Stenberg, Per
    Umeå University, Faculty of Science and Technology, Umeå Centre for Molecular Pathogenesis (UCMP) (Faculty of Science and Technology).
    Bernhardsson, Carolina
    Umeå University, Faculty of Science and Technology, Umeå Centre for Molecular Pathogenesis (UCMP) (Faculty of Science and Technology).
    Larsson, Jan
    Umeå University, Faculty of Science and Technology, Umeå Centre for Molecular Pathogenesis (UCMP) (Faculty of Science and Technology).
    Painting of fourth and chromosome-wide regulation of the 4th chromosome in Drosophila melanogaster.2007In: EMBO J, ISSN 0261-4189, Vol. 26, no 9, p. 2307-2316Article in journal (Refereed)
    Abstract [en]

    Drosophila melanogaster exhibits two expression-regulating systems that target whole, specific chromosomes: the dosage compensation system whereby the male-specific lethal complex doubles transcription of genes on the male X-chromosome and the chromosome 4-specific protein Painting of fourth, POF. POF is the first example of an autosome-specific protein and its presence raises the question of the universality of chromosome-specific regulation. Here we show that POF and heterochromatin protein 1 (HP1) are involved in the global regulation of the 4th chromosome. Contrary to previous conclusions, Pof is not essential for survival of diplo-4th karyotype flies. However, Pof is essential for survival of haplo-4th individuals and expression of chromosome 4 genes in diplo-4th individuals is decreased in the absence of Pof. Mapping of POF using chromatin immunoprecipitation suggested that it binds within genes. Furthermore, we show that POF binding is dependent on heterochromatin and that POF and HP1 bind interdependently to the 4th chromosome. We propose a balancing mechanism involving POF and HP1 that provides a feedback system for fine-tuning expression status of genes on the 4th chromosome.

  • 11.
    Schiffthaler, Bastian
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Bernhardsson, Carolina
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Ingvarsson, Par K.
    Street, Nathaniel R.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    BatchMap: A parallel implementation of the OneMap R package for fast computation of F-1 linkage maps in outcrossing species2017In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 12, no 12, article id e0189256Article in journal (Refereed)
    Abstract [en]

    With the rapid advancement of high throughput sequencing, large numbers of genetic markers can be readily and cheaply acquired, but most current software packages for genetic map construction cannot handle such dense input. Modern computer architectures and server farms represent untapped resources that can be used to enable higher marker densities to be processed in tractable time. Here we present a pipeline using a modified version of OneMap that parallelizes over bottleneck functions and achieves substantial speedups for producing a high density linkage map (N = 20,000). Using simulated data we show that the outcome is as accurate as the traditional pipeline. We further demonstrate that there is a direct relationship between the number of markers used and the level of deviation between true and estimated order, which in turn impacts the final size of a genetic map.

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