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  • 1.
    de La Torre, Amanda R.
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Plant Sciences, University of California–Davis, Davis, CA.
    Li, Zhen
    Van de Peer, Yves
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Plant Biology, Uppsala Biocenter, Swedish University of Agr icultural Sciences, Uppsala, Sweden.
    Contrasting Rates of Molecular Evolution and Patterns of Selection among Gymnosperms and Flowering Plants2017In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 34, no 6, p. 1363-1377Article in journal (Refereed)
    Abstract [en]

    The majority of variation in rates of molecular evolution among seed plants remains both unexplored and unexplained. Although some attention has been given to flowering plants, reports of molecular evolutionary rates for their sister plant clade (gymnosperms) are scarce, and to our knowledge differences in molecular evolution among seed plant clades have never been tested in a phylogenetic framework. Angiosperms and gymnosperms differ in a number of features, of which contrasting reproductive biology, life spans, and population sizes are the most prominent. The highly conserved morphology of gymnosperms evidenced by similarity of extant species to fossil records and the high levels of macrosynteny at the genomic level have led scientists to believe that gymnosperms are slow-evolving plants, although some studies have offered contradictory results. Here, we used 31,968 nucleotide sites obtained from orthologous genes across a wide taxonomic sampling that includes representatives of most conifers, cycads, ginkgo, and many angiosperms with a sequenced genome. Our results suggest that angiosperms and gymnosperms differ considerably in their rates of molecular evolution per unit time, with gymnosperm rates being, on average, seven times lower than angiosperm species. Longer generation times and larger genome sizes are some of the factors explaining the slow rates of molecular evolution found in gymnosperms. In contrast to their slow rates of molecular evolution, gymnosperms possess higher substitution rate ratios than angiosperm taxa. Finally, our study suggests stronger and more efficient purifying and diversifying selection in gymnosperm than in angiosperm species, probably in relation to larger effective population sizes.

  • 2. Griffin, Robert M.
    et al.
    Dean, Rebecca
    Grace, Jaime L.
    Ryden, Patrik
    Umeå University, Faculty of Medicine, Department of Clinical Microbiology.
    Friberg, Urban
    The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression2013In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 30, no 9, p. 2168-2176Article in journal (Refereed)
    Abstract [en]

    Males and females share most of their genomes, and differences between the sexes can therefore not evolve through sequence divergence in protein coding genes. Sexual dimorphism is instead restricted to occur through sex-specific expression and splicing of gene products. Evolution of sexual dimorphism through these mechanisms should, however, also be constrained when the sexes share the genetic architecture for regulation of gene expression. Despite these obstacles, sexual dimorphism is prevalent in the animal kingdom and commonly evolves rapidly. Here, we ask whether the genetic architecture of gene expression is plastic and easily molded by sex-specific selection, or if sexual dimorphism evolves rapidly despite pervasive genetic constraint. To address this question, we explore the relationship between the intersexual genetic correlation for gene expression (r(MF)), which captures how independently genes are regulated in the sexes, and the evolution of sex-biased gene expression. Using transcriptome data from Drosophila melanogaster, we find that most genes have a high r(MF) and that genes currently exposed to sexually antagonistic selection have a higher average r(MF) than other genes. We further show that genes with a high r(MF) have less pronounced sex-biased gene expression than genes with a low r(MF) within D. melanogaster and that the strength of the r(MF) in D. melanogaster predicts the degree to which the sex bias of a gene's expression has changed between D. melanogaster and six other species in the Drosophila genus. In sum, our results show that a shared genome constrains both short- and long-term evolution of sexual dimorphism.

  • 3.
    Ingvarsson, Pär K
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Molecular population genetics of herbivore-induced protease inhibitor genes in European aspen (Populus tremula, L., Salicaceae)2005In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 22, no 9, p. 1802-1812Article in journal (Refereed)
    Abstract [en]

    Plants defend themselves against the attack of natural enemies by using an array of both constitutively expressed and induced defenses. Long-lived woody perennials are overrepresented among plant species that show strong induced defense responses, whereas annual plants and crop species are underrepresented. However, most studies of plant defense genes have been performed on annual or short-lived perennial weeds or crop species. Here I use molecular population genetic methods to survey six wound-inducible protease inhibitors (PIs) in a long-lived woody, perennial plant species, the European aspen (Populus tremula), to evaluate the likelihood of either recurrent selective sweeps or balancing selection maintaining amino acid polymorphisms in these genes. The results show that none of the six PI genes have reduced diversities at synonymous sites, as would be expected in the presence of recurrent selective sweeps. However, several genes show some evidence of nonneutral evolution such as enhanced linkage disequilibrium and a large number of high-frequency-derived mutations. A group of at least four Kunitz trypsin inhibitor genes appear to have experienced elevated levels of nonsynonymous substitutions, indicating allelic turnover on an evolutionary timescale. One gene, T11, has enhanced levels of intraspecific polymorphism at nonsynonymous sites and also has an unusual haplotype structure characterized by two divergent haplotypes occurring at roughly equal frequencies in the sample. One haplotype has very low levels of intraallelic nucleotide diversity, whereas the other haplotype has levels of diversity comparable to other genes in P. tremula. Patterns of sequence diversity at T11 do not fit a simple model of either balancing selection or recurrent selective sweeps. This suggests that selection at T11 is more complex, possibly involving allelic cycling.

  • 4.
    Ingvarsson, Pär K
    Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
    Natural selection on synonymous and non-synonymous mutations shape patterns of polymorphism in Populus tremula2010In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 27, no 3, p. 650-660Article in journal (Refereed)
    Abstract [en]

    One important goal of population genetics is to understand the relative importance of different evolutionary processes for shaping variation in natural populations. Here, I use multilocus data to show that natural selection on both synonymous and nonsynonymous mutations plays an important role in shaping levels of synonymous polymorphism in European aspen (Populus tremula). Previous studies have documented a preferential fixation of synonymous mutations encoding preferred codons in P. tremula. The results presented here show that this has resulted in an increase in codon bias in P. tremula, consistent with stronger selection acting on synonymous codon usage. In addition, positive selection on nonsynonymous mutations appears to be common in P. tremula, with approximately 30% of all mutations having been fixed by positive selection. In addition, the recurrent fixation of beneficial mutations also reduces standing levels of polymorphism as evidenced by a significantly negative relationship between the rate of protein evolution synonymous site diversity and silent site diversity. Finally, I use approximate Bayesian methods to estimate the strength of selection acting on beneficial substitutions. These calculations show that recurrent hitchhiking reduces polymorphism by, on average, 30%. The product of strength of selection acting on beneficial mutations and the rate by which these occur across the genome (2Nes) equals 1.54x10 – 7, which is in line with estimates from Drosophila where recurrent hitchhiking has also been shown to have significant effects on standing levels of polymorphism.

  • 5. Karakostis, Konstantinos
    et al.
    Ponnuswamy, Anand
    Fusee, Leila T. S.
    Bailly, Xavier
    Laguerre, Laurent
    Worall, Erin
    Vojtesek, Borek
    Nylander, Karin
    Umeå University, Faculty of Medicine, Department of Medical Biosciences.
    Fåhraeus, Robin
    Umeå University, Faculty of Medicine, Department of Medical Biosciences. E´quipe Labellise´e Ligue Contre le Cancer, Universite´ Paris 7, INSERM UMR 1162, Paris, France; Regional Centre for Applied Molecular Oncology, RECAMO and Masaryk Memorial Cancer Institute, Brno, Czech Republic.
    p53 mRNA and p53 Protein Structures Have Evolved Independently to Interact with MDM22016In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 5, p. 1280-1292Article in journal (Refereed)
    Abstract [en]

    The p53 tumor suppressor and its key regulator MDM2 play essential roles in development, ageing, cancer, and cellular stress responses in mammals. Following DNA damage, MDM2 interacts with p53 mRNA in an ATM kinase-dependent fashion and stimulates p53 synthesis, whereas under normal conditions, MDM2 targets the p53 protein for degradation. The peptide-and RNA motifs that interact with MDM2 are encoded by the same conserved BOX-I sequence, but how these interactions have evolved is unknown. Here, we show that a temperature-sensitive structure in the invertebrate Ciona intestinalis (Ci) p53 mRNA controls its interaction with MDM2. We also show that a nonconserved flanking region of Ci-BOX-I domain prevents the p53-MDM2 protein-protein interaction. These results indicate that the temperature-regulated p53 mRNA-MDM2 interaction evolved to become kinase regulated in the mammalian DNA damage response. The data also suggest that the negative regulation of p53 by MDM2 via protein-protein interaction evolved in vertebrates following changes in the BOX-I flanking sequence.

  • 6. Knöppel, Anna
    et al.
    Lind, Peter A
    Lustig, Ulrika
    Näsvall, Joakim
    Andersson, Dan I
    Minor fitness costs in an experimental model of horizontal gene transfer in bacteria.2014In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 31, no 5Article in journal (Refereed)
    Abstract [en]

    Genes introduced by horizontal gene transfer (HGT) from other species constitute a significant portion of many bacterial genomes, and the evolutionary dynamics of HGTs are important for understanding the spread of antibiotic resistance and the emergence of new pathogenic strains of bacteria. The fitness effects of the transferred genes largely determine the fixation rates and the amount of neutral diversity of newly acquired genes in bacterial populations. Comparative analysis of bacterial genomes provides insight into what genes are commonly transferred, but direct experimental tests of the fitness constraints on HGT are scarce. Here, we address this paucity of experimental studies by introducing 98 random DNA fragments varying in size from 0.45 to 5 kb from Bacteroides, Proteus, and human intestinal phage into a defined position in the Salmonella chromosome and measuring the effects on fitness. Using highly sensitive competition assays, we found that eight inserts were deleterious with selection coefficients (s) ranging from ≈ -0.007 to -0.02 and 90 did not have significant fitness effects. When inducing transcription from a PBAD promoter located at one end of the insert, 16 transfers were deleterious and 82 were not significantly different from the control. In conclusion, a major fraction of the inserts had minor effects on fitness implying that extra DNA transferred by HGT, even though it does not confer an immediate selective advantage, could be maintained at selection-transfer balance and serve as raw material for the evolution of novel beneficial functions.

  • 7.
    Lind, Peter A.
    et al.
    Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology). Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden.
    Arvidsson, Lars
    Berg, Otto G
    Andersson, Dan I
    Variation in mutational robustness between different proteins and the predictability of fitness effects2017In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 34, no 2, p. 408-418Article in journal (Refereed)
    Abstract [en]

    Random mutations in genes from disparate protein classes may have different distributions of fitness effects (DFEs) depending on different structural, functional and evolutionary constraints. We measured the fitness effects of 156 single mutations in the genes encoding AraC (transcription factor), AraD (enzyme), and AraE (transporter) used for bacterial growth on L- arabinose. Despite their different molecular functions these genes all had bimodal DFEs with most mutations either being neutral or strongly deleterious, providing a general expectation for the DFE. This contrasts with the unimodal DFEs previously obtained for ribosomal protein genes where most mutations were slightly deleterious. Based on theoretical considerations, we suggest that the 33-fold higher average mutational robustness of ribosomal proteins is due to stronger selection for reduced costs of translational and transcriptional errors. While the large majority of synonymous mutations were deleterious for ribosomal proteins genes, no fitness effects could be detected for the AraCDE genes. Four mutations in AraC and AraE increased fitness, suggesting that slightly advantageous mutations make up a significant fraction of the DFE, but that they often escape detection due to the limited sensitivity of commonly used fitness assays. We show that the fitness effects of amino acid substitutions can be predicted based on evolutionary conservation, but that weakly deleterious mutations are less reliably detected. This suggests that large-effect mutations and the fraction of highly deleterious mutations can be computationally predicted, but that experiments are required to characterize the DFE close to neutrality, where many mutations ultimately fixed in a population will occur.

  • 8. Shpiz, Sergey
    et al.
    Kwon, Dmitry
    Uneva, Anastasiya
    Kim, Maria
    Klenov, Mikhail
    Rozovsky, Yakov
    Georgiev, Pavel
    Savitsky, Mikhail
    Kalmykova, Alla
    Characterization of Drosophila telomeric retroelement TAHRE: transcription, transpositions, and RNAi-based regulation of expression.2007In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 24, no 11Article in journal (Refereed)
    Abstract [en]

    Telomeres in Drosophila are maintained by transpositions of specialized telomeric retroelements HeT-A and TART rather than by the telomerase activity adding short DNA repeats to chromosome ends in other eukaryotes. A novel element TAHRE was previously found in the telomeric regions of the genome of Drosophila melanogaster stock sequenced by the Genome Project. Comparative genomic analysis confirmed by Southern analysis and in situ hybridization of polytene chromosomes reveals conserved TAHRE elements in the genomes of melanogaster subgroup species. Spontaneous attachment of TAHRE retroelement to the broken end of terminally deleted chromosome allows us to consider TAHRE as the third retrotransposon family involved in telomere maintenance in Drosophila. The abundance of TAHRE transcripts in ovaries is strongly upregulated owing to mutations in the RNA interference genes spn-E, aub, piwi, and vasa locus. spn-E mutations eliminate TAHRE-specific short RNAs in the ovaries. These data suggest that TAHRE is a conservative element involved along with HeT-A and TART in telomere maintenance and a target of the RNAi-based system in the Drosophila germ line. This study reveals similar distribution of TAHRE and HeT-A transcripts, which accumulate in the oocyte, whereas TART transcripts localize in nurse cells. Taking into account a common pattern of HeT-A and TAHRE expression, one may consider TAHRE as a source of reverse transcriptase enzymatic activity for HeT-A transpositions in ovaries.

  • 9.
    Sullivan, Alexis R.
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Schiffthaler, Bastian
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Thompson, Stacey Lee
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Biology, Dalhousie University, Halifax, NS, Canada.
    Street, Nathaniel R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Wang, Xiao-Ru
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Interspecific Plastome Recombination Reflects Ancient Reticulate Evolution in Picea (Pinaceae)2017In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 34, no 7, p. 1689-1701Article in journal (Refereed)
    Abstract [en]

    Plastid sequences are a cornerstone in plant systematic studies and key aspects of their evolution, such as uniparental inheritance and absent recombination, are often treated as axioms. While exceptions to these assumptions can profoundly influence evolutionary inference, detecting them can require extensive sampling, abundant sequence data, and detailed testing. Using advancements in high-throughput sequencing, we analyzed the whole plastomes of 65 accessions of Picea, a genus of similar to 35 coniferous forest tree species, to test for deviations from canonical plastome evolution. Using complementary hypothesis and data-driven tests, we found evidence for chimeric plastomes generated by interspecific hybridization and recombination in the clade comprising Norway spruce (P. abies) and 10 other species. Support for interspecific recombination remained after controlling for sequence saturation, positive selection, and potential alignment artifacts. These results reconcile previous conflicting plastid-based phylogenies and strengthen the mounting evidence of reticulate evolution in Picea. Given the relatively high frequency of hybridization and biparental plastid inheritance in plants, we suggest interspecific plastome recombination may be more widespread than currently appreciated and could underlie reported cases of discordant plastid phylogenies.

  • 10.
    Virel, Ana
    et al.
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Backman, Lars
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Molecular evolution and structure of α-actinin2004In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 21, no 6, p. 1024-1031Article in journal (Refereed)
    Abstract [en]

    The N-terminal actin-binding domain of -actinin is connected to the C-terminal EF-hands by a rod domain. Because of its ability to form dimers, -actinin can cross-link actin filaments in muscle cells as well as in nonmuscle cells. In the prototypic -actinins, the rod domain contains four triple helical bundles, or so-called spectrin repeats. We have found some atypical -actinins in early diverging organisms, such as protozoa and yeast, where the rod domain contains one and two spectrin repeats, respectively. This implies that the four repeats present in modern -actinins arose after two consecutive intragenic duplications from an -actinin with a single repeat. Further, the evolutionary gene tree of -actinins shows that the appearance of four distinct -actinin isoforms may have occurred after the vertebrate-invertebrate split. The topology of the tree lends support to the hypothesis that two rounds (2R) of genome duplication occurred early in the vertebrate radiation. The phylogeny also considers these atypical isoforms as the most basal to -actinins of vertebrates and other eukaryotes. The analysis also positioned -actinin of the fungi Encephalitozoo cuniculi close to the protozoa, supporting the suggestion that microsporidia are early eukaryotes. Because -actinin is considered the basal member of the spectrin family, our studies will improve the understanding of the origin and evolution of this superfamily.

  • 11.
    Wang, Jing
    et al.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Street, Nathaniel
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Scofield, Douglas
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Ecology and Genetics: Evolutionary Biology, Uppsala University, Uppsala, Sweden; Uppsala Multidisciplinary Center for Advanced Computational Science, Uppsala University, Uppsala, Sweden.
    Ingvarsson, Pär
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
    Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens2016In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 7, p. 1754-1767Article in journal (Refereed)
    Abstract [en]

    Despite the global economic and ecological importance of forest trees, the genomic basis of differential adaptation and speciation in tree species is still poorly understood. Populus tremula and P. tremuloides are two of the most widespread tree species in the Northern Hemisphere. Using whole-genome re-sequencing data of 24 P. tremula and 22 P. tremuloidesindividuals, we find that the two species diverged ~2.2-3.1 million years ago, coinciding with the severing of the Bering land bridge and the onset of dramatic climatic oscillations during the Pleistocene. Both species have experienced substantial population expansions following long-term declines after species divergence. We detect widespread and heterogeneous genomic differentiation between species, and in accordance with the expectation of allopatric speciation, coalescent simulations suggest that neutral evolutionary processes can account for most of the observed patterns of genetic differentiation. However, there is an excess of regions exhibiting extreme differentiation relative to those expected under demographic simulations, which is indicative of the action of natural selection. Overall genetic differentiation is negatively associated with recombination rate in both species, providing strong support for a role of linked selection in generating the heterogeneous genomic landscape of differentiation between species. Finally, we identify a number of candidate regions and genes that may have been subject to positive and/or balancing selection during the speciation process.

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