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  • 1.
    Ahmed, Engy
    et al.
    Stockholm University, Faculty of Science, Department of Geological Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Parducci, Laura
    Unneberg, Per
    Ågren, Rasmus
    Schenk, Frederik
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Rattray, Jayne E.
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Han, Lu
    Muschitiello, Francesco
    Stockholm University, Faculty of Science, Department of Geological Sciences. Columbia University, USA.
    Pedersen, Mikkel W.
    Smittenberg, Rienk H.
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Afrifa Yamoah, Kweku
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Wohlfarth, Barbara
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Archaeal community changes in Lateglacial lake sediments: Evidence from ancient DNA2018In: Quaternary Science Reviews, ISSN 0277-3791, E-ISSN 1873-457X, Vol. 181, p. 19-29Article in journal (Refereed)
    Abstract [en]

    The Lateglacial/early Holocene sediments from the ancient lake at Hasseldala Port, southern Sweden provide an important archive for the environmental and climatic shifts at the end of the last ice age and the transition into the present Interglacial. The existing multi-proxy data set highlights the complex interplay of physical and ecological changes in response to climatic shifts and lake status changes. Yet, it remains unclear how microorganisms, such as Archaea, which do not leave microscopic features in the sedimentary record, were affected by these climatic shifts. Here we present the metagenomic data set of Hasseldala Port with a special focus on the abundance and biodiversity of Archaea. This allows reconstructing for the first time the temporal succession of major Archaea groups between 13.9 and 10.8 ka BP by using ancient environmental DNA metagenomics and fossil archaeal cell membrane lipids. We then evaluate to which extent these findings reflect physical changes of the lake system, due to changes in lake-water summer temperature and seasonal lake-ice cover. We show that variations in archaeal composition and diversity were related to a variety of factors (e.g., changes in lake water temperature, duration of lake ice cover, rapid sediment infilling), which influenced bottom water conditions and the sediment-water interface. Methanogenic Archaea dominated during the Allerod and Younger Dryas pollen zones, when the ancient lake was likely stratified and anoxic for large parts of the year. The increase in archaeal diversity at the Younger Dryas/Holocene transition is explained by sediment infilling and formation of a mire/peatbog.

  • 2.
    Bachmann, Jörg A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Lafon-Placette, Clément
    Köhler, Claudia
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)2021In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 127, p. 124-134Article in journal (Refereed)
    Abstract [en]

    Polyploidy, or whole-genome duplication, is a common speciation mechanism in plants. An important barrier to polyploid establishment is a lack of compatible mates. Because self-compatibility alleviates this problem, it has long been hypothesized that there should be an association between polyploidy and self-compatibility (SC), but empirical support for this prediction is mixed. Here, we investigate whether the molecular makeup of the Brassicaceae self-incompatibility (SI) system, and specifically dominance relationships among S-haplotypes mediated by small RNAs, could facilitate loss of SI in allopolyploid crucifers. We focus on the allotetraploid species Capsella bursa-pastoris, which formed similar to 300 kya by hybridization and whole-genome duplication involving progenitors from the lineages of Capsella orientalis and Capsella grandiflora. We conduct targeted long-read sequencing to assemble and analyze eight full-length S-locus haplotypes, representing both homeologous subgenomes of C. bursa-pastoris. We further analyze small RNA (sRNA) sequencing data from flower buds to identify candidate dominance modifiers. We find that C. orientalis-derived S-haplotypes of C. bursa-pastoris harbor truncated versions of the male SI specificity gene SCR and express a conserved sRNA-based candidate dominance modifier with a target in the C. grandiflora-derived S-haplotype. These results suggest that pollen-level dominance may have facilitated loss of SI in C. bursa-pastoris. Finally, we demonstrate that spontaneous somatic tetraploidization after a wide cross between C. orientalis and C. grandiflora can result in production of self-compatible tetraploid offspring. We discuss the implications of this finding on the mode of formation of this widespread weed.

  • 3.
    Bachmann, Jörg A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genete, Mathieu
    Ferreira de Carvalho, Julie
    Castric, Vincent
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Evolutionary stability of genetic dominance in the Brassicaceae self-incompatibility systemManuscript (preprint) (Other academic)
    Abstract [en]

    The question of whether dominance-recessivity relationships between associated alleles in a diploid genotype can evolve independently from the activity of the gene products encoded has been a hot topic in evolutionary genetics throughout the 20th century. In hermaphroditic plants of the Brassicaceae family, the self-incompatibility locus (S-locus) confers the ability to recognize and reject self-pollen. Dominance relationships between self-incompatibility alleles (S-alleles) in pollen are governed by small RNA (sRNA) transcriptional regulators produced by dominant S-alleles and their target sites on recessive S-alleles. These regulators and their target sites segregate together with but are distinct from the genes encoding self-recognition specificities themselves, providing the opportunity for dominance to evolve independently from the recognition specificities. Dominance interactions between the many segregating S-alleles have been described in the distantly related Arabidopsis and Brassica, but little is known about the evolutionary stability of the dominance networks given that divergent sets of S-alleles are segregating in these two genera. In this study, we take advantage of the extensive trans-specific sharing of S-haplotypes between the self-incompatible species Capsella grandiflora and Arabidopsis halleri to investigate the conservation of S-locus dominance relationships across their approximately 8 million years of divergence. For this purpose, we use a combination of controlled crosses and full-length long-read sequencing of S-haplotypes. We find that the dominance network among six C. grandiflora S-alleles has a largely parallel structure to that among their orthologous S-alleles in A. halleri. We test the theoretical prediction that dominant S-alleles should be found at lower population frequencies using a large sample of a natural C. grandiflora population. Finally, we test whether dominant C. grandiflora S-alleles show increased accumulation of repeats (TEs) than recessive S-alleles, as expected due to their lower chance of recombination and lower effective population sizes. Our results contribute to an improved understanding of the maintenance of dominance relationships at loci under balancing selection.

  • 4.
    Bachmann, Jörg A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Désamore, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Lafon-Placette, Clement
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Callot, Caroline
    Marande, William
    Neuffer, Barbara
    Bergès, Hélène
    Köhler, Claudia
    Castric, Vincent
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genetic basis and timing of a major mating system shift in Capsella2019In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 224, no 1, p. 505-517Article in journal (Refereed)
    Abstract [en]

    A crucial step in the transition from outcrossing to self-fertilization is the loss of genetic self-incompatibility (SI). In the Brassicaceae, SI involves the interaction of female and male specificity components, encoded by the genes SRK and SCR at the self-incompatibility locus (S-locus). Theory predicts that S-linked mutations, and especially dominant mutations in SCR, are likely to contribute to loss of SI. However, few studies have investigated the contribution of dominant mutations to loss of SI in wild plant species. Here, we investigate the genetic basis of loss of SI in the self-fertilizing crucifer species Capsella orientalis, by combining genetic mapping, long-read sequencing of complete S-haplotypes, gene expression analyses and controlled crosses. We show that loss of SI in C. orientalis occurred S-locus. We identify a fixed frameshift deletion in the male specificity gene SCR and confirm loss of male SI specificity. We further identify an S-linked small RNA that is predicted to cause dominance of self-compatibility. Our results agree with predictions on the contribution of dominant S-linked mutations to loss of SI, and thus provide new insights into the molecular basis of mating system transitions.

  • 5.
    Bachmann, Jörg A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Targeted Long-Read Sequencing of a Locus Under Long-Term Balancing Selection in Capsella2018In: G3: Genes, Genomes, Genetics, E-ISSN 2160-1836, Vol. 8, no 4, p. 1327-1333Article in journal (Refereed)
    Abstract [en]

    Rapid advances in short-read DNA sequencing technologies have revolutionized population genomic studies, but there are genomic regions where this technology reaches its limits. Limitations mostly arise due to the difficulties in assembly or alignment to genomic regions of high sequence divergence and high repeat content, which are typical characteristics for loci under strong long-term balancing selection. Studying genetic diversity at such loci therefore remains challenging. Here, we investigate the feasibility and error rates associated with targeted long-read sequencing of a locus under balancing selection. For this purpose, we generated bacterial artificial chromosomes (BACs) containing the Brassicaceae S-locus, a region under strong negative frequency-dependent selection which has previously proven difficult to assemble in its entirety using short reads. We sequence S-locus BACs with single-molecule long-read sequencing technology and conduct de novo assembly of these S-locus haplotypes. By comparing repeated assemblies resulting from independent long-read sequencing runs on the same BAC clone we do not detect any structural errors, suggesting that reliable assemblies are generated, but we estimate an indel error rate of 5.7x10(-5). A similar error rate was estimated based on comparison of Illumina short-read sequences and BAC assemblies. Our results show that, until de novo assembly of multiple individuals using long-read sequencing becomes feasible, targeted long-read sequencing of loci under balancing selection is a viable option with low error rates for single nucleotide polymorphisms or structural variation. We further find that short-read sequencing is a valuable complement, allowing correction of the relatively high rate of indel errors that result from this approach.

  • 6. Berdan, Emma L.
    et al.
    Blanckaert, Alexandre
    Butlin, Roger K.
    Flatt, Thomas
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Wielstra, Ben
    Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals2022In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 377, no 1856, article id 20210199Article in journal (Refereed)
    Abstract [en]

    Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One outcome is the formation of maladaptive balanced lethal systems, where only heterozygotes remain viable and reproduce. We investigated the conditions under which these different outcomes occur, assuming a scenario of introgression after divergence. We found that AOD aided the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism was easily destabilized by further mutation accumulation, which was often asymmetric, disrupting the quasi-equilibrium state. Mechanisms that accelerated degeneration tended to amplify asymmetric mutation accumulation between the supergene arrangements and vice-versa. As the evolution of balanced lethal systems requires symmetric degeneration of both arrangements, this leaves only restricted conditions for their evolution, namely small population sizes and low rates of gene conversion. The dichotomy between the persistence of polymorphism and degeneration of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

  • 7.
    Berdan, Emma L.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Blanckaert, Alexandre
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Suh, Alexander
    Westram, Anja M.
    Fragata, Inês
    Unboxing mutations: Connecting mutation types with evolutionary consequences2021In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 30, no 12, p. 2710-2723Article in journal (Refereed)
    Abstract [en]

    A key step in understanding the genetic basis of different evolutionary outcomes (e.g., adaptation) is to determine the roles played by different mutation types (e.g., SNPs, translocations and inversions). To do this we must simultaneously consider different mutation types in an evolutionary framework. Here, we propose a research framework that directly utilizes the most important characteristics of mutations, their population genetic effects, to determine their relative evolutionary significance in a given scenario. We review known population genetic effects of different mutation types and show how these may be connected to different evolutionary outcomes. We provide examples of how to implement this framework and pinpoint areas where more data, theory and synthesis are needed. Linking experimental and theoretical approaches to examine different mutation types simultaneously is a critical step towards understanding their evolutionary significance.

  • 8. Birkeland, Siri
    et al.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). University of Oslo, Norway.
    Brysting, Anne Krag
    Gustafsson, A. Lovisa S.
    Hvidsten, Torgeir Rhoden
    Brochmann, Christian
    Nowak, Michael D.
    What can cold-induced transcriptomes of Arctic Brassicaceae tell us about the evolution of cold tolerance?2022In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 31, no 16, p. 4271-4285Article in journal (Refereed)
    Abstract [en]

    Little is known about the evolution of cold tolerance in polar plant species and how they differ from temperate relatives. To gain insight into their biology and the evolution of cold tolerance, we compared the molecular basis of cold response in three Arctic Brassicaceae species. We conducted a comparative time series experiment to examine transcriptional responses to low temperature. RNA was sampled at 22°C, and after 3, 6, and 24 at 2°C. We then identified sets of genes that were differentially expressed in response to cold and compared them between species, as well as to published data from the temperate Arabidopsis thaliana. Most differentially expressed genes were species-specific, but a significant portion of the cold response was also shared among species. Among thousands of differentially expressed genes, ~200 were shared among the three Arctic species and A. thaliana, while ~100 were exclusively shared among the three Arctic species. Our results show that cold response differs markedly between Arctic Brassicaceae species, but probably builds on a conserved basis found across the family. They also confirm that highly polygenic traits such as cold tolerance may show little repeatability in their patterns of adaptation. 

  • 9. Bohutínská, Magdalena
    et al.
    Vlček, Jakub
    Yair, Sivan
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Konečná, Veronika
    Fracassetti, Marco
    Stockholm University, Science for Life Laboratory (SciLifeLab). Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Kolář, Filip
    Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives2021In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 118, no 21, article id e2022713118Article in journal (Refereed)
    Abstract [en]

    Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.

  • 10. Dong, Yang
    et al.
    Majda, Mateusz
    Šimura, Jan
    Horvath, Robert
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Srivastava, Anjil K.
    Łangowski, Łukasz
    Eldridge, Tilly
    Stacey, Nicola
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Sadanandom, Ari
    Ljung, Karin
    Smith, Richard S.
    Østergaard, Lars
    HEARTBREAK Controls Post-translational Modification of INDEHISCENT to Regulate Fruit Morphology in Capsella2020In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 30, no 19, p. 3880-3888Article in journal (Refereed)
    Abstract [en]

    Morphological variation is the basis of natural diversity and adaptation. For example, angiosperms (flowering plants) evolved during the Cretaceous period more than 100 mya and quickly colonized terrestrial habitats [1]. A major reason for their astonishing success was the formation of fruits, which exist in a myriad of different shapes and sizes [2]. Evolution of organ shape is fueled by variation in expression patterns of regulatory genes causing changes in anisotropic cell expansion and division patterns [3-5]. However, the molecular mechanisms that alter the polarity of growth to generate novel shapes are largely unknown. The heart-shaped fruits produced by members of the Capsella genus comprise an anatomical novelty, making it particularly well suited for studies on morphological diversification [6-8]. Here, we show that post-translational modification of regulatory proteins provides a critical step in organ-shape formation. Our data reveal that the SUMO protease, HEARTBREAK (HTB), from Capsella rubella controls the activity of the key regulator of fruit development, INDEHISCENT (CrIND in C. rubella), via de-SUMOylation. This post-translational modification initiates a transduction pathway required to ensure precisely localized auxin biosynthesis, thereby facilitating anisotropic cell expansion to ultimately form the heart-shaped Capsella fruit. Therefore, although variation in the expression of key regulatory genes is known to be a primary driver in morphological evolution, our work demonstrates how other processes-such as post-translational modification of one such regulator-affects organ morphology.

  • 11. Douglas, Gavin M.
    et al.
    Gos, Gesseca
    Steige, Kim A.
    Salcedo, Adriana
    Holm, Karl
    Josephs, Emily B.
    Arunkumar, Ramesh
    Agren, J. Arvid
    Hazzouri, Khaled M.
    Wang, Wei
    Platts, Adrian E.
    Williamson, Robert J.
    Neuffer, Barbara
    Lascoux, Martin
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Uppsala University, Sweden.
    Wright, Stephen I.
    Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris2015In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 112, no 9, p. 2806-2811Article in journal (Refereed)
    Abstract [en]

    Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000-300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that non-functionalization can receive a head start through a legacy of deleterious variants and differential expression originating in parental diploid populations.

  • 12. Dziasek, Katarzyna
    et al.
    Simon, Lauriane
    Lafon-Placette, Clément
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Wärdig, Cecilia
    Santos-González, Juan
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Köhler, Claudia
    Hybrid seed incompatibility in Capsella is connected to chromatin condensation defects in the endosperm2021In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 17, no 2, article id e1009370Article in journal (Refereed)
    Abstract [en]

    Hybridization of closely related plant species is frequently connected to endosperm arrest and seed failure, for reasons that remain to be identified. In this study, we investigated the molecular events accompanying seed failure in hybrids of the closely related species pair Capsella rubella and C. grandiflora. Mapping of QTL for the underlying cause of hybrid incompatibility in Capsella identified three QTL that were close to pericentromeric regions. We investigated whether there are specific changes in heterochromatin associated with interspecific hybridizations and found a strong reduction of chromatin condensation in the endosperm, connected with a strong loss of CHG and CHH methylation and random loss of a single chromosome. Consistent with reduced DNA methylation in the hybrid endosperm, we found a disproportionate deregulation of genes located close to pericentromeric regions, suggesting that reduced DNA methylation allows access of transcription factors to targets located in heterochromatic regions. Since the identified QTL were also associated with pericentromeric regions, we propose that relaxation of heterochromatin in response to interspecies hybridization exposes and activates loci leading to hybrid seed failure.

  • 13.
    Gutiérrez-Valencia, Juanita
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Berdan, Emma L.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Bunikis, Ignas
    Soler, Lucile
    Dainat, Jacques
    Kutschera, Verena E.
    Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Losvik, Aleksandra
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Désamoré, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Hughes, P. William
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Foroozani, Alireza
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Pesquet, Edouard
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Abdelaziz, Mohamed
    Pettersson, Olga Vinnere
    Nystedt, Björn
    Brennan, Adrian C.
    Arroyo, Juan
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level2022In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 32, no 20, p. 4360-4371, 4371.e1-4371.e6Article in journal (Refereed)
    Abstract [en]

    Supergenes govern multi-trait-balanced polymorphisms in a wide range of systems; however, our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown whether hemizygosity is pervasive among distyly S-loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. Here, we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes, provide a counterexample to classic inversion-based supergenes, and shed new light on the origin and maintenance of an iconic floral polymorphism.

  • 14.
    Gutiérrez-Valencia, Juanita
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Horvath, Robert
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Désamore, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Drouzas, Andreas D.
    Friberg, Magne
    Kolář, Filip
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genomic Signatures of Sexual Selection on Pollen-Expressed Genes in Arabis alpina2022In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 39, no 1, article id msab349Article in journal (Refereed)
    Abstract [en]

    Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.

  • 15.
    Gutiérrez-Valencia, Juanita
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Hughes, P. William
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Berdan, Emma L.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    The Genomic Architecture and Evolutionary Fates of Supergenes2021In: Genome Biology and Evolution, E-ISSN 1759-6653, Vol. 13, no 5, article id evab057Article, review/survey (Refereed)
    Abstract [en]

    Supergenes are genomic regions containing sets of tightly linked loci that control multi-trait phenotypic polymorphisms under balancing selection. Recent advances in genomics have uncovered significant variation in both the genomic architecture as well as the mode of origin of supergenes across diverse organismal systems. Although the role of genomic architecture for the origin of supergenes has been much discussed, differences in the genomic architecture also subsequently affect the evolutionary trajectory of supergenes and the rate of degeneration of supergene haplotypes. In this review, we synthesize recent genomic work and historical models of supergene evolution, highlighting how the genomic architecture of supergenes affects their evolutionary fate. We discuss how recent findings on classic supergenes involved in governing ant colony social form, mimicry in butterflies, and heterostyly in flowering plants relate to theoretical expectations. Furthermore, we use forward simulations to demonstrate that differences in genomic architecture affect the degeneration of supergenes. Finally, we discuss implications of the evolution of supergene haplotypes for the long-term fate of balanced polymorphisms governed by supergenes.

  • 16.
    Gutiérrez-Valencia, Juanita
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Zervakis, Panagiotis-Ioannis
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Losvik, Aleksandra
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Mehrabi, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Bunikis, Ignas
    Soler, Lucile
    Hughes, P. William
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Désamoré, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Abdelaziz, Mohamed
    Vinnere Pettersson, Olga
    Nystedt, Björn
    Arroyo, Juan
    Slotte, Tanja
    Genomic analyses of the breakdown of distyly in Linum trigynumManuscript (preprint) (Other academic)
  • 17.
    Gutiérrez-Valencia, Juanita
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Zervakis, Panagiotis-Ioannis
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Postel, Zoé
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Fracassetti, Marco
    Stockholm University, Science for Life Laboratory (SciLifeLab). Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Losvik, Aleksandra
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Mehrabi, Sara
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Bunikis, Ignas
    Soler, Lucile
    Hughes, P. William
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Désamoré, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Abdelaziz, Mohamed
    Pettersson, Olga Vinnere
    Arroyo, Juan
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genetic Causes and Genomic Consequences of Breakdown of Distyly in Linum trigynum2024In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 41, no 5, article id msae087Article in journal (Refereed)
    Abstract [en]

    Distyly is an iconic floral polymorphism governed by a supergene, which promotes efficient pollen transfer and outcrossing through reciprocal differences in the position of sexual organs in flowers, often coupled with heteromorphic self-incompatibility. Distyly has evolved convergently in multiple flowering plant lineages, but has also broken down repeatedly, often resulting in homostylous, self-compatible populations with elevated rates of self-fertilization. Here, we aimed to study the genetic causes and genomic consequences of the shift to homostyly in Linum trigynum, which is closely related to distylous Linum tenue. Building on a high-quality genome assembly, we show that L. trigynum harbors a genomic region homologous to the dominant haplotype of the distyly supergene conferring long stamens and short styles in L. tenue, suggesting that loss of distyly first occurred in a short-styled individual. In contrast to homostylous Primula and FagopyrumL. trigynum harbors no fixed loss-of-function mutations in coding sequences of S-linked distyly candidate genes. Instead, floral gene expression analyses and controlled crosses suggest that mutations downregulating the S-linked LtWDR-44 candidate gene for male self-incompatibility and/or anther height could underlie homostyly and self-compatibility in L. trigynum. Population genomic analyses of 224 whole-genome sequences further demonstrate that L. trigynum is highly self-fertilizing, exhibits significantly lower genetic diversity genome-wide, and is experiencing relaxed purifying selection and less frequent positive selection on nonsynonymous mutations relative to L. tenue. Our analyses shed light on the loss of distyly in L. trigynum, and advance our understanding of a common evolutionary transition in flowering plants.

  • 18. Hatorangan, Marcelinus R.
    et al.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Kohler, Claudia
    Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae2016In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 28, no 8, p. 1815-1827Article in journal (Refereed)
    Abstract [en]

    Genomic imprinting is an epigenetic phenomenon occurring in mammals and flowering plants that causes genes to adopt a parent-of-origin-specific mode of expression. While the imprinting status of genes is well conserved in mammals, clear estimates for the degree of conservation were lacking in plants. We therefore analyzed the genome-wide imprinting status of Capsella rubella, which shared a common recent ancestor with Arabidopsis thaliana similar to 10 to 14 million years ago. However, only similar to 14% of maternally expressed genes (MEGs) and similar to 29% of paternally expressed genes (PEGs) in C. rubella were commonly imprinted in both species, revealing that genomic imprinting is a rapidly evolving phenomenon in plants. Nevertheless, conserved PEGs exhibited signs of selection, suggesting that a subset of imprinted genes play an important functional role and are therefore maintained in plants. Like in Arabidopsis, PEGs in C. rubella are frequently associated with the presence of transposable elements that preferentially belong to helitron and MuDR families. Our data further reveal that MEGs and PEGs differ in their targeting by 24-nucleotide small RNAs and asymmetric DNA methylation, suggesting different mechanisms establishing DNA methylation at MEGs and PEGs.

  • 19.
    Horvath, Robert
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Josephs, Emily B.
    Pesquet, Edouard
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Stinchcombe, John R.
    Wright, Stephen I.
    Scofield, Douglas
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Selection on accessible chromatin regions in Capsella grandifloraManuscript (preprint) (Other academic)
  • 20.
    Horvath, Robert
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Josephs, Emily B.
    Pesquet, Edouard
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Stinchcombe, John R.
    Wright, Stephen
    Scofield, Douglas
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Selection on Accessible Chromatin Regions in Capsella grandiflora2021In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 38, no 12, p. 5563-5575Article in journal (Refereed)
    Abstract [en]

    Accurate estimates of genome-wide rates and fitness effects of new mutations are essential for an improved understanding of molecular evolutionary processes. Although eukaryotic genomes generally contain a large noncoding fraction, functional noncoding regions and fitness effects of mutations in such regions are still incompletely characterized. A promising approach to characterize functional noncoding regions relies on identifying accessible chromatin regions (ACRs) tightly associated with regulatory DNA. Here, we applied this approach to identify and estimate selection on ACRs in Capsella grandiflora, a crucifer species ideal for population genomic quantification of selection due to its favorable population demography. We describe a population-wide ACR distribution based on ATAC-seq data for leaf samples of 16 individuals from a natural population. We use population genomic methods to estimate fitness effects and proportions of positively selected fixations (alpha) in ACRs and find that intergenic ACRs harbor a considerable fraction of weakly deleterious new mutations, as well as a significantly higher proportion of strongly deleterious mutations than comparable inaccessible intergenic regions. ACRs are enriched for expression quantitative trait loci (eQTL) and depleted of transposable element insertions, as expected if intergenic ACRs are under selection because they harbor regulatory regions. By integrating empirical identification of intergenic ACRs with analyses of eQTL and population genomic analyses of selection, we demonstrate that intergenic regulatory regions are an important source of nearly neutral mutations. These results improve our understanding of selection on noncoding regions and the role of nearly neutral mutations for evolutionary processes in outcrossing Brassicaceae species.

  • 21.
    Horvath, Robert
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Takuno, Shohei
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Single-cell expression noise and gene-body methylation in Arabidopsis thaliana2019In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 123, no 2, p. 81-91Article in journal (Refereed)
    Abstract [en]

    Gene-body methylation (gbM) refers to an increased level of methylated cytosines specifically in a CG sequence context within genes. gbM is found in plant genes with intermediate expression level, which evolve slowly, and is often broadly conserved across millions of years of evolution. Intriguingly however, some plants lack gbM, and thus it remains unclear whether gbM has a function. In animals, there is support for a role of gbM in reducing erroneous transcription and transcription noise, but so far most studies in plants have tested for an effect of gbM on expression level, not noise. Here, we therefore tested whether gbM was associated with reduced expression noise in Arabidopsis thaliana, using single-cell transcriptome sequencing data from root quiescent centre cells. We find that gbM genes have lower expression noise levels than unmethylated genes. However, an analysis of covariance revealed that, if other genomic features are taken into account, this association disappears. Nonetheless, gbM genes were more consistently expressed across single-cell samples, supporting previous inference that gbM genes are constitutively expressed. Finally, we observed that fewer RNAseq reads map to introns of gbM genes than to introns of unmethylated genes, which indicates that gbM might be involved in reducing erroneous transcription by reducing intron retention.

  • 22.
    Horvath, Robert
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    The Role of Small RNA-Based Epigenetic Silencing for Purifying Selection on Transposable Elements in Capsella grandiflora2017In: Genome Biology and Evolution, E-ISSN 1759-6653, Vol. 9, no 10, p. 2911-2920Article in journal (Refereed)
    Abstract [en]

    To avoid negative effects of transposable element (TE) proliferation, plants epigenetically silence TEs using a number of mechanisms, including RNA-directed DNA methylation. These epigenetic modifications can extend outside the boundaries of TE insertions and lead to silencing of nearby genes, resulting in a trade-off between TE silencing and interference with nearby gene regulation. Therefore, purifying selection is expected to remove silenced TE insertions near genes more efficiently and prevent their accumulation within a population. To explore how effects of TE silencing on gene regulation shapes purifying selection on TEs, we analyzed whole genome sequencing data from 166 individuals of a large population of the outcrossing species Capsella grandiflora. We found that most TEs are rare, and in chromosome arms, silenced TEs are exposed to stronger purifying selection than those that are not silenced by 24-nucleotide small RNAs, especially with increasing proximity to genes. An age-of-allele test of neutrality on a subset of TEs supports our inference of purifying selection on silenced TEs, suggesting that our results are robust to varying transposition rates. Our results provide new insights into the processes affecting the accumulation of TEs in an outcrossing species and support the view that epigenetic silencing of TEs results in a trade-off between preventing TE proliferation and interference with nearby gene regulation. We also suggest that in the centromeric and pericentromeric regions, the negative aspects of epigenetic TE silencing are missing.

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  • 23. Koenig, Daniel
    et al.
    Hagmann, Jörg
    Li, Rachel
    Bemm, Felix
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Nueffer, Barbara
    Wright, Stephen
    Weigel, Detlef
    Long-term balancing selection drives evolution of immunity genes in Capsella2019In: eLIFE, E-ISSN 2050-084X, Vol. 8, article id e43606Article in journal (Refereed)
    Abstract [en]

    Genetic drift is expected to remove polymorphism from populations over long periods of time, with the rate of polymorphism loss being accelerated when species experience strong reductions in population size. Adaptive forces that maintain genetic variation in populations, or balancing selection, might counteract this process. To understand the extent to which natural selection can drive the retention of genetic diversity, we document genomic variability after two parallel species-wide bottlenecks in the genus Capsella. We find that ancestral variation preferentially persists at immunity related loci, and that the same collection of alleles has been maintained in different lineages that have been separated for several million years. By reconstructing the evolution of the disease-related locus MLO2b, we find that divergence between ancient haplotypes can be obscured by referenced based re-sequencing methods, and that trans-specific alleles can encode substantially diverged protein sequences. Our data point to long-term balancing selection as an important factor shaping the genetics of immune systems in plants and as the predominant driver of genomic variability after a population bottleneck.

  • 24.
    Laenen, Benjamin
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Nowak, Michael D.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Toräng, Per
    Wunder, Jörg
    Wötzel, Stefan
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Kourmpetis, Yiannis
    Odong, Thomas
    Drouzas, Andreas D.
    Bink, Marco C. A. M.
    Ågren, Jon
    Coupland, George
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina2018In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 4, p. 816-821Article in journal (Refereed)
    Abstract [en]

    Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

  • 25. Lafon-Placette, Clément
    et al.
    Hatorangan, Marcelinus R.
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Cornille, Amandine
    Lascoux, Martin
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Köhler, Claudia
    Paternally expressed imprinted genes associate with hybridization barriers in Capsella2018In: Nature plants, ISSN 2055-026X, Vol. 4, no 6, p. 352-357Article in journal (Refereed)
    Abstract [en]

    Hybrid seed lethality is a widespread type of reproductive barrier among angiosperm taxa(1,2) that contributes to species divergence by preventing gene flow between natural populations(3,4). Besides its ecological importance, it is an important obstacle to plant breeding strategies(5). Hybrid seed lethality is mostly due to a failure of the nourishing endosperm tissue, resulting in embryo arrest(3,6,7). The cause of this failure is a parental dosage imbalance in the endosperm that can be a consequence of either differences in parental ploidy levels or differences in the 'effective ploidy', also known as the endosperm balance number (EBN)(8,9). Hybrid seed defects exhibit a parent-of-origin pattern(3,6,7), suggesting that differences in number or expression strength of parent-of-origin-specific imprinted genes underpin, as the primary or the secondary cause, the molecular basis of the EBN7,10. Here, we have tested this concept in the genus Capsella and show that the effective ploidy of three Capsella species correlates with the number and expression level of paternally expressed genes (PEGs). Importantly, the number of PEGs and the effective ploidy decrease with the selfing history of a species: the obligate outbreeder Capsella grandiflora had the highest effective ploidy, followed by the recent selfer Capsella rubella and the ancient selfer Capsella orientalis. PEGs were associated with the presence of transposable elements and their silencing mark, DNA methylation in CHH context (where H denotes any base except C). This suggests that transposable elements have driven the imprintome divergence between Capsella species. Together, we propose that variation in transposable element insertions, the resulting differences in PEG number and divergence in their expression level form one component of the effective ploidy variation between species of different breeding system histories, and, as a consequence, allow the establishment of endosperm-based hybridization barriers.

  • 26. Mattila, Tiina M.
    et al.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Horvath, Robert
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Hämälä, Tuomas
    Savolainen, Outi
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Impact of demography on linked selection in two outcrossing Brassicaceae species2019In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 9, no 17, p. 9532-9545Article in journal (Refereed)
    Abstract [en]

    Genetic diversity is shaped by mutation, genetic drift, gene flow, recombination, and selection. The dynamics and interactions of these forces shape genetic diversity across different parts of the genome, between populations and species. Here, we have studied the effects of linked selection on nucleotide diversity in outcrossing populations of two Brassicaceae species, Arabidopsis lyrata and Capsella grandiflora, with contrasting demographic history. In agreement with previous estimates, we found evidence for a modest population size expansion thousands of generations ago, as well as efficient purifying selection in C. grandiflora. In contrast, the A. lyrata population exhibited evidence for very recent strong population size decline and weaker efficacy of purifying selection. Using multiple regression analyses with recombination rate and other genomic covariates as explanatory variables, we can explain 47% of the variance in neutral diversity in the C. grandiflora population, while in the A. lyrata population, only 11% of the variance was explained by the model. Recombination rate had a significant positive effect on neutral diversity in both species, suggesting that selection at linked sites has an effect on patterns of neutral variation. In line with this finding, we also found reduced neutral diversity in the vicinity of genes in the C. grandiflora population. However, in A. lyrata no such reduction in diversity was evident, a finding that is consistent with expectations of the impact of a recent bottleneck on patterns of neutral diversity near genes. This study thus empirically demonstrates how differences in demographic history modulate the impact of selection at linked sites in natural populations.

  • 27. Monnahan, Patrick
    et al.
    Kolar, Filip
    Baduel, Pierre
    Sailer, Christian
    Koch, Jordan
    Horvath, Robert
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Schmickl, Roswitha
    Paajanen, Pirita
    Šrámková, Gabriela
    Bohutínská, Magdalena
    Arnold, Brian
    Weisman, Caroline M.
    Marhold, Karol
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Bomblies, Kirsten
    Yant, Levi
    Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa2019In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 3, no 3, p. 457-468Article in journal (Refereed)
    Abstract [en]

    Ploidy-variable species allow direct inference of the effects of chromosome copy number on fundamental evolutionary processes. While an abundance of theoretical work suggests polyploidy should leave distinct population genomic signatures, empirical data remains sparse. We sequenced similar to 300 individuals from 39 populations of Arabidopsis arenosa, a naturally diploidautotetraploid species. We find that the impacts of polyploidy on population genomic processes are subtle yet pervasive, such as reduced efficiency of purifying selection, differences in linked selection and rampant gene flow from diploids. Initial masking of deleterious mutations, faster rates of nucleotide substitution and interploidy introgression likely conspire to shape the evolutionary potential of polyploids.

  • 28. Nowak, Michael D.
    et al.
    Birkeland, Siri
    Mandákova, Terezie
    Roy Choudhury, Rimjhim
    Guo, Xinyi
    Gustafsson, Anna Lovisa S.
    Gizaw, Abel
    Schrøder-Nielsen, Audun
    Fracassetti, Marco
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Brysting, Anne K.
    Rieseberg, Loren
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Parisod, Christian
    Lysak, Martin A.
    Brochmann, Christian
    The genome of Draba nivalis shows signatures of adaptation to the extreme environmental stresses of the Arctic2021In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, no 3, p. 661-676Article in journal (Refereed)
    Abstract [en]

    The Arctic is one of the most extreme terrestrial environments on the planet. Here, we present the first chromosome-scale genome assembly of a plant adapted to the high Arctic, Draba nivalis (Brassicaceae), an attractive model species for studying plant adaptation to the stresses imposed by this harsh environment. We used an iterative scaffolding strategy with data from short-reads, single-molecule long reads, proximity ligation data, and a genetic map to produce a 302 Mb assembly that is highly contiguous with 91.6% assembled into eight chromosomes (the base chromosome number). To identify candidate genes and gene families that may have facilitated adaptation to Arctic environmental stresses, we performed comparative genomic analyses with nine non-Arctic Brassicaceae species. We show that the D. nivalis genome contains expanded suites of genes associated with drought and cold stress (e.g., related to the maintenance of oxidation-reduction homeostasis, meiosis, and signaling pathways). The expansions of gene families associated with these functions appear to be driven in part by the activity of transposable elements. Tests of positive selection identify suites of candidate genes associated with meiosis and photoperiodism, as well as cold, drought, and oxidative stress responses. Our results reveal a multifaceted landscape of stress adaptation in the D. nivalis genome, offering avenues for the continued development of this species as an Arctic model plant.

  • 29. Olmedo-Vicente, Erika
    et al.
    Desamore, Aurelie
    Stockholm Univ, Dept Ecol Environm & Plant Sci, Sci Life Lab, Stockholm, Sweden.
    Simon-Porcar, Violeta I.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Arroyo, Juan
    Development of microsatellite markers for sister species Linum suffruticosum and Linum tenuifolium in their overlapping ranges2023In: Molecular Biology Reports, ISSN 0301-4851, E-ISSN 1573-4978, Vol. 50, no 9, p. 7927-7933Article in journal (Refereed)
    Abstract [en]

    Background Microsatellite markers were developed for distylous Linum suffruticosum and tested in the monomorphic sister species Linum tenuifolium. These species are perennial herbs endemic to the western and northwestern Mediterranean, respectively, with a partially overlapping distribution area.Methods and resultsWe developed 12 microsatellite markers for L. suffruticosum using next generation sequencing, and assessed their polymorphism and genetic diversity in 152 individuals from seven natural populations. The markers displayed high polymorphism, with two to 16 alleles per locus and population, and average observed and expected heterozygosities of 0.833 and 0.692, respectively. All loci amplified successfully in the sister species L. tenuifolium, and 150 individuals from seven populations were also screened. The polymorphism exhibited was high, with two to ten alleles per locus and population, and average observed and expected heterozygosities of 0.77 and 0.62, respectively.

    Conclusions The microsatellite markers identified in L. suffruticosum and tested in L. tenuifolium are a powerful tool to facilitate future investigations of the population genetics, mating patterns and hybridization between both Linum species in their contact zone.

  • 30. Parducci, Laura
    et al.
    Greve Alsos, Inger
    Unneberg, Per
    Pedersen, Mikkel W.
    Han, Lu
    Lammers, Youri
    Salonen, J. Sakari
    Väliranta, Minna M.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Wohlfarth, Barbara
    Stockholm University, Faculty of Science, Department of Geological Sciences.
    Shotgun Environmental DNA, Pollen, and Macrofossil Analysis of Lateglacial Lake Sediments From Southern Sweden2019In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 7, article id 189Article in journal (Refereed)
    Abstract [en]

    The lake sediments of Hasseldala Port in south-east Sweden provide an archive of local and regional environmental conditions similar to 14.5-9.5 ka BP (thousand years before present) and allow testing DNA sequencing techniques to reconstruct past vegetation changes. We combined shotgun sequencing with plant micro- and macrofossil analyses to investigate sediments dating to the Allerod (14.1-12.7 ka BP), Younger Dryas (12.7-11.7 ka BP), and Preboreal (<11.7 ka BP). Number of reads and taxa were not associated with sample age or organic content. This suggests that, beyond the initial rapid degradation, DNA is still present. The proportion of recovered plant DNA was low, but allowed identifying an important number of plant taxa, thus adding valid information on the composition of the local vegetation. Importantly, DNA provides a stronger signal of plant community changes than plant micro- and plant macrofossil analyses alone, since a larger number of new taxa were recorded in Younger Dryas samples. A comparison between the three proxies highlights differences and similarities and supports earlier findings that plants growing close to or within a lake are recorded by DNA. Plant macrofossil remains moreover show that tree birch was present close to the ancient lake since the Allerod; together with the DNA results, this indicates that boreal to subarctic climatic conditions also prevailed during the cold Younger Dryas interval. Increasing DNA reference libraries and enrichment strategies prior to sequencing are necessary to improve the potential and accuracy of plant identification using the shotgun metagenomic approach.

  • 31.
    Plue, Jan
    et al.
    Stockholm University, Faculty of Science, Department of Physical Geography. Södertörn University, Sweden.
    Kimberley, Adam
    Stockholm University, Faculty of Science, Department of Physical Geography.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Interspecific variation in ploidy as a key plant trait outlining local extinction risks and community patterns in fragmented landscapes2018In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 32, no 8, p. 2095-2106Article in journal (Refereed)
    Abstract [en]

    1. Polyploidy is associated with a plethora of phenotypic and genetic changes yielding transformative effects on species' life-history and ecology. These biological attributes can contribute to the success of species on ecological timescales, as observed in the invasion success or rapid environmental and climatic adaptation of polyploids. However, to date there has been a distinct lack of empirical evidence linking species' local extinction risk, species distributions and community structure in fragmented landscapes with interspecific variation in ploidy. 2. We aimed to investigate the relationship between levels of habitat fragmentation and patterns in both diversity and the frequency of species with different ploidy levels. We included additional persistence-and dispersal related life-history traits, to establish the relative importance of ploidy in determining species richness and frequencies following habitat fragmentation. We therefore collected plant community presence-absence data and landscape data from grassland fragments from south-central Sweden. 3. Community-level analysis uncovered that interspecific variation in ploidy proved the strongest predictor of plant community species richness and turn-over across grassland fragments. Local extinction risk decreased as ploidy increased, with diploids most prone to local extinction. 4. In the species-level analysis, ploidy outweighed the combined explanatory power of commonly used life-history traits such as clonality, dispersal mechanism and mating system; key predictors of plant species distributions across fragmented landscapes. 5. Ploidy appears to capture parallel variation in a series of advantageous genetic and life-history mechanisms which operate on ecological timescales, emerging as the strongest predictor of local extinction risk even after accounting for variation in other crucial life-history traits. Our results therefore highlight the importance of genomic traits such as ploidy and total chromosome number as valuable factors explaining and predicting local extinction risk in fragmented landscapes.

  • 32. Rebernig, Carolin A.
    et al.
    Lafon-Placette, Clement
    Hatorangan, Marcelinus R.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Kohler, Claudia
    Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm2015In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 11, no 6, article id e1005295Article in journal (Refereed)
    Abstract [en]

    The transition to selfing in Capsella rubella accompanies its recent divergence from the ancestral outcrossing C. grandiflora species about 100,000 years ago. Whether the change in mating system was accompanied by the evolution of additional reproductive barriers that enforced species divergence remained unknown. Here, we show that C. rubella and C. grandiflora are reproductively separated by an endosperm-based, non-reciprocal postzygotic hybridization barrier. While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors resulted in complete seed abortion caused by endosperm cellularization failure, the reciprocal hybridization resulted in the formation of small seeds with precociously cellularized endosperm. Strikingly, the transcriptomic response of both hybridizations mimicked respectively the response of paternal and maternal excess hybridizations in Arabidopsis thaliana, suggesting unbalanced genome strength causes hybridization failure in both species. These results provide strong support for the theory that crosses between plants of different mating systems will be unbalanced, with the outcrosser behaving like a plant of increased ploidy, evoking a response that resembles an interploidy-type seed failure. Seed incompatilibity of C. rubella pollinated by C. grandiflora followed the Bateson-Dobzhansky-Muller model, involving negative genetic interaction of multiple paternal C. grandiflora loci with at least one maternal C. rubella locus. Given that both species only recently diverged, our data suggest that a fast evolving mechanism underlies the post-zygotic hybridization barrier(s) separating both species.

  • 33.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    The impact of linked selection on plant genomic variation2014In: Briefings in Functional Genomics & Proteomics, ISSN 2041-2649, E-ISSN 2041-2657, Vol. 13, no 4, p. 268-275Article in journal (Refereed)
    Abstract [en]

    Understanding the forces that shape patterns of genetic variation across the genome is a major aim in evolutionary genetics. An emerging insight from analyses of genome-wide polymorphism and divergence data is that selection on linked sites can have an important impact on neutral genetic variation. However, in contrast to Drosophila, which exhibits a signature of recurrent hitchhiking, many plant genomes studied so far seem to mainly be affected by background selection. Moreover, many plants do not exhibit classic signatures of linked selection, such as a correlation between recombination rate and neutral diversity. In this review, I discuss the impact of genome architecture and mating system on the expected signature of linked selection in plants and review empirical evidence for linked selection, with a focus on plant model systems. Finally, I discuss the implications of linked selection for inference of demographic history in plants.

  • 34.
    Steige, Kim A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Reimegård, Johan
    Scofield, Douglas G.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Genomic analysis reveals major determinants of cis-regulatory variation in Capsella grandiflora2017In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 114, no 5, p. 1087-1092Article in journal (Refereed)
    Abstract [en]

    Understanding the causes of cis-regulatory variation is a long-standing aim in evolutionary biology. Although cis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standing cis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants, and selective forces shaping cis-regulatory variation in the outcrossing plant Capsella grandiflora. We first identified a set of 1,010 genes with common cis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with common cis-regulatory variation (i) are underweaker purifying selection and (ii) undergo less frequent positive selection than other genes. We further identified genomic determinants of cis-regulatory variation. Gene body methylation (gbM) was a major factor constraining cis-regulatory variation, whereas presence of nearby transposable elements (TEs) and tissue specificity of expression increased the odds of ASE. Our results suggest that most common cis-regulatory variation in C. grandiflora is under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance of cis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide evidence for a link between gbM and cis-regulatory constraint, possibly reflecting greater dosage sensitivity of body-methylated genes. Given the extensive conservation of gbM in flowering plants, this suggests that gbM could be an important predictor of cis-regulatory variation in a wide range of plant species.

  • 35. Steige, Kim A.
    et al.
    Reimegard, Johan
    Koenig, Daniel
    Scofield, Douglas G.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Cis-Regulatory Changes Associated with a Recent Mating System Shift and Floral Adaptation in Capsella2015In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 10, p. 2501-2514Article in journal (Refereed)
    Abstract [en]

    The selfing syndrome constitutes a suite of floral and reproductive trait changes that have evolved repeatedly across many evolutionary lineages in response to the shift to selfing. Convergent evolution of the selfing syndrome suggests that these changes are adaptive, yet our understanding of the detailed molecular genetic basis of the selfing syndrome remains limited. Here, we investigate the role of cis-regulatory changes during the recent evolution of the selfing syndrome in Capsella rubella, which split from the outcrosser Capsella grandiflora less than 200 ka. We assess allele-specific expression (ASE) in leaves and flower buds at a total of 18,452 genes in three interspecific F1 C. grandiflora x C. rubella hybrids. Using a hierarchical Bayesian approach that accounts for technical variation using genomic reads, we find evidence for extensive cis-regulatory changes. On average, 44% of the assayed genes show evidence of ASE; however, only 6% show strong allelic expression biases. Flower buds, but not leaves, show an enrichment of cis-regulatory changes in genomic regions responsible for floral and reproductive trait divergence between C. rubella and C. grandiflora. We further detected an excess of heterozygous transposable element (TE) insertions near genes with ASE, and TE insertions targeted by uniquely mapping 24-nt small RNAs were associated with reduced expression of nearby genes. Our results suggest that cis-regulatory changes have been important during the recent adaptive floral evolution in Capsella and that differences in TE dynamics between selfing and outcrossing species could be important for rapid regulatory divergence in association with mating system shifts.

  • 36.
    Steige, Kim A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Genomic legacies of the progenitors and the evolutionary consequences of allopolyploidy2016In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 30, p. 88-93Article, review/survey (Refereed)
    Abstract [en]

    The formation of an allopolyploid species involves the merger of genomes with separate evolutionary histories and thereby different genomic legacies. Contrary to expectations from theory, genes from one are often lost preferentially in allopolyploids - there is biased fractionation. Here, we provide an overview of two ways in which the genomic legacies of the progenitors may impact the fate of duplicated genes in allopolyploids. Specifically, we discuss the role of homeolog expression biases in setting the stage for biased fractionation, and the evidence for transposable element silencing as a possible mechanism for homeolog expression biases. Finally, we highlight how differences between the progenitors with respect to accumulation of deleterious variation may affect trajectories of duplicate gene evolution in allopolyploids.

  • 37.
    Yang, Xuyue
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Fors, Lisa
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Theopold, Ulrich
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Binzer-Panchal, Mahesh
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Hambäck, Peter A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Differential expression of immune genes between two closely related beetle species with different immunocompetence following attack by Asecodes parviclava2020In: Genome Biology and Evolution, E-ISSN 1759-6653, Vol. 12, no 5, p. 522-534Article in journal (Refereed)
    Abstract [en]

    Endoparasitoid wasps are important natural enemies of many insect species and are major selective forces on the host immune system. Despite increased interest in insect antiparasitoid immunity, there is sparse information on the evolutionary dynamics of biological pathways and gene regulation involved in host immune defense outside Drosophila species. We de novo assembled transcriptomes from two beetle species and used time-course differential expression analysis to investigate gene expression differences in closely related species Galerucella pusilla and G. calmariensis that are, respectively, resistant and susceptible against parasitoid infection by Asecodes paividava parasitoids. Approximately 271 million and 224 million paired-ended reads were assembled and filtered to form 52,563 and 59,781 transcripts for G. pusilla and G. calmariensis, respectively. In the whole-transcriptome level, an enrichment of functional categories related to energy production, biosynthetic process, and metabolic process was exhibited in both species. The main difference between species appears to be immune response and wound healing process mounted by G. pusilla larvae. Using reciprocal BLAST against the Drosophila melanogaster proteome, 120 and 121 immune-related genes were identified in G. pusilla and G. calmariensis, respectively. More immune genes were differentially expressed in G. pusilla than in G. calmariensis, in particular genes involved in signaling, hematopoiesis, and melanization. In contrast, only one gene was differentially expressed in G. calmariensis. Our study characterizes important genes and pathways involved in different immune functions after parasitoid infection and supports the role of signaling and hematopoiesis genes as key players in host immunity in Galerucella against parasitoid wasps.

  • 38.
    Yang, Xuyue
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Dainat, Jacques
    Hambäck, Peter A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Genome assemblies of three closely related leaf beetle species (Galerucella spp.)2021In: G3: Genes, Genomes, Genetics, E-ISSN 2160-1836, Vol. 11, no 8, article id jkab214Article in journal (Refereed)
    Abstract [en]

    Galerucella (Coleoptera: Chrysomelidae) is a leaf beetle genus that has been extensively used for ecological and evolutionary studies. It has also been used as biological control agent against invading purple loosestrife in North America, with large effects on biodiversity. Here, we report genome assembly and annotation of three closely related Galerucella species: G. calmariensis, G. pusilla, and G. tenella. The three assemblies have a genome size ranging from 460 to 588 Mbp, with N50 from 31,588 to 79,674 kbp, containing 29,202 to 40,929 scaffolds. Using an ab initio evidence-driven approach, 30,302 to 33,794 protein-coding genes were identified and functionally annotated. These draft genomes will contribute to the understanding of host-parasitoid interactions, evolutionary comparisons of leaf beetle species and future population genomics studies. 

  • 39.
    Yang, Xuyue
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology, Systematic Zoology.
    Hambäck, Peter A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    The genomic basis of adaptation to different host environments in a parasitoid wasp2021Manuscript (preprint) (Other academic)
    Abstract [en]

    Many insect species are infected by parasitic wasps in a constantly evolving network of interactions. Understanding the genetics of population differentiation in parasitic wasps is therefore important in the study of species diversity. Asecodes parviclava is a koinobiont endoparasitic wasp that exhibits large population variation in virulence when attacking host beetle species across Sweden. In this study, we sequenced, de novo assembled and annotated the entire genome of A. parviclava. Final assembly had a size = 384 Mbp, contained 11,196 scaffolds with a N50 = 302.549 kbp. Using an ab initio evidence-driven approach, 22,290 protein-coding genes were identified and functionally annotated. Using this genome we then performed a population genomic scan for selective patterns by generating whole genome re-sequencing data from individual wasps from 11 populations and using FST-based approaches. Finally, we searched specifically across sets of candidate venom and chemosensory genes, which may be the key traits leading to population differentiation. With 1% of SNPs as FST outliers, several regions of the genome appeared to be under strong selection. Specifically, candidate regions responsible for virulence variations included genes involved in the inhibition of host immune systems and odorant/gustatory receptors. Our study identified important regions and genes underlying mechanisms of host adaptations in parasitic wasps.

  • 40.
    Yang, Xuyue
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Wheat, Christopher W.
    Stockholm University, Faculty of Science, Department of Zoology.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Hambäck, Peter
    Lineage-specific targets of positive selection in three leaf beetles with different defence capacity against a parasitic waspManuscript (preprint) (Other academic)
    Abstract [en]

    Parasitoid wasps are the major causes of mortality of many target host species therefore traits related to host immune defence are usually favored by natural selection. One powerful approach to detect functionally important genes under natural selection is through the analysis of directional selection acting upon protein-coding gene sequences across different species. Here, we investigated patterns of positive selection across three close related leaf beetle species with different immune defence capacity against a parasitoid wasp using a Bayesian approach for the McDonald–Kreitman test. Focus upon single-copy orthologs for Coleoptera, as well as candidate immune related genes, we detected positive selection on coding regions in each of the species specific linesages of three species closely related species of Galerucella beetles. Among these, more immune genes were under positive selection in the species with the greatest immunocompetence (G. pusilla) against parasitoid wasps, while almost no immune genes were under positive selection in the species with the least immunocompetence (G. calmariensis). 

     

     

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