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  • 1. Giacomello, Stefania
    et al.
    Salmen, Fredrik
    Terebieniec, Barbara K.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Vickovic, Sanja
    Navarro, José Fernandez
    Alexeyenko, Andrey
    Reimegard, Johan
    McKee, Lauren S.
    Mannapperuma, Chanaka
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Bulone, Vincent
    Ståhl, Patrik L.
    Sundström, Jens F.
    Street, Nathaniel
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Lundeberg, Joakim
    Spatially resolved transcriptome profiling in model plant species2017In: Nature Plants, ISSN 2055-026X, Vol. 3, no 6, article id 17061Article in journal (Refereed)
    Abstract [en]

    Understanding complex biological systems requires functional characterization of specialized tissue domains. However, existing strategies for generating and analysing high-throughput spatial expression profiles were developed for a limited range of organisms, primarily mammals. Here we present the first available approach to generate and study highresolution, spatially resolved functional profiles in a broad range of model plant systems. Our process includes highthroughput spatial transcriptome profiling followed by spatial gene and pathway analyses. We first demonstrate the feasibility of the technique by generating spatial transcriptome profiles from model angiosperms and gymnosperms microsections. In Arabidopsis thaliana we use the spatial data to identify differences in expression levels of 141 genes and 189 pathways in eight inflorescence tissue domains. Our combined approach of spatial transcriptomics and functional profiling offers a powerful new strategy that can be applied to a broad range of plant species, and is an approach that will be pivotal to answering fundamental questions in developmental and evolutionary biology.

  • 2.
    Mähler, Niklas
    et al.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Norwegian Univ Life Sci, Dept Chem Biotechnol & Food Sci, Norway.
    Wang, Jing
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Centre for Integrative Genetics, Faculty of Biosciences, Norwegian University of Life Sciences, Norway.
    Terebieniec, Barbara K.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Ingvarsson, Pär K.
    Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Swedish Univ Agr Sci, Dept Plant Biol, Uppsala, Sweden.
    Street, Nathaniel R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Hvidsten, Torgeir R.
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Norwegian Univ Life Sci, Dept Chem Biotechnol & Food Sci, As, Norway.
    Gene co-expression network connectivity is an important determinant of selective constraint2017In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 13, no 4, article id e1006402Article in journal (Refereed)
    Abstract [en]

    While several studies have investigated general properties of the genetic architecture of natural variation in gene expression, few of these have considered natural, outbreeding populations. In parallel, systems biology has established that a general feature of biological networks is that they are scale-free, rendering them buffered against random mutations. To date, few studies have attempted to examine the relationship between the selective processes acting to maintain natural variation of gene expression and the associated co-expression network structure. Here we utilised RNA-Sequencing to assay gene expression in winter buds undergoing bud flush in a natural population of Populus tremula, an outbreeding forest tree species. We performed expression Quantitative Trait Locus (eQTL) mapping and identified 164,290 significant eQTLs associating 6,241 unique genes (eGenes) with 147,419 unique SNPs (eSNPs). We found approximately four times as many local as distant eQTLs, with local eQTLs having significantly higher effect sizes. eQTLs were primarily located in regulatory regions of genes (UTRs or flanking regions), regardless of whether they were local or distant. We used the gene expression data to infer a co-expression network and investigated the relationship between network topology, the genetic architecture of gene expression and signatures of selection. Within the co-expression network, eGenes were underrepresented in network module cores (hubs) and overrepresented in the periphery of the network, with a negative correlation between eQTL effect size and network connectivity. We additionally found that module core genes have experienced stronger selective constraint on coding and non-coding sequence, with connectivity associated with signatures of selection. Our integrated genetics and genomics results suggest that purifying selection is the primary mechanism underlying the genetic architecture of natural variation in gene expression assayed in flushing leaf buds of P. tremula and that connectivity within the co-expression network is linked to the strength of purifying selection.

  • 3. Ratke, Christine
    et al.
    Terebieniec, Barbara K.
    Department of Forest Genetics and Plant Physiology, SLU, Umeå Plant Science Centre (UPSC), Umeå, Sweden.
    Winestrand, Sandra
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Derba-Maceluch, Marta
    Department of Forest Genetics and Plant Physiology, SLU, Umeå Plant Science Centre (UPSC), Umeå, Sweden.
    Grahn, Thomas
    Schiffthaler, Bastian
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Ulvcrona, Thomas
    Ozparpucu, Merve
    Rüggeberg, Markus
    Lundqvist, Sven-Olof
    Street, Nathaniel
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Jönsson, Leif J.
    Umeå University, Faculty of Science and Technology, Department of Chemistry.
    Mellerowicz, Ewa J.
    Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome2018In: New Phytologist, ISSN 0028-646X, Vol. 219, no 1, p. 230-245Article in journal (Refereed)
    Abstract [en]

    Xylan is one of the main compounds determining wood properties in hardwood species. The xylan backbone is thought to be synthesized by a synthase complex comprising two members of the GT43 family. We downregulated all GT43 genes in hybrid aspen (Populus tremulaxtremuloides) to understand their involvement in xylan biosynthesis.

    All three clades of the GT43 family were targeted for downregulation using RNA interference individually or in different combinations, either constitutively or specifically in developing wood.

    Simultaneous downregulation in developing wood of the B (IRX9) and C (IRX14) clades resulted in reduced xylan Xyl content relative to reducing end sequence, supporting their role in xylan backbone biosynthesis. This was accompanied by a higher lignocellulose saccharification efficiency. Unexpectedly, GT43 suppression in developing wood led to an overall growth stimulation, xylem cell wall thinning and a shift in cellulose orientation. Transcriptome profiling of these transgenic lines indicated that cell cycling was stimulated and secondary wall biosynthesis was repressed. We suggest that the reduced xylan elongation is sensed by the cell wall integrity surveying mechanism in developing wood.

    Our results show that wood-specific suppression of xylan-biosynthetic GT43 genes activates signaling responses, leading to increased growth and improved lignocellulose saccharification.

  • 4.
    Schiffthaler, Bastian
    et al.
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Terebieniec, Barbara K
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Mähler, Niklas
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Robinson, Kathryn M
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Mannapperuma, Chanaka
    Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
    Jansson, Stefan
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    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).
    An integrated functional genomics and systems genetics analysis of leaf shape in Populus tremula Manuscript (preprint) (Other academic)
    Abstract [en]

    Leaf shape is an important component of our relationship with the living world, representing a defining feature of how we recognise and classify plant species. There is extensive variation in the form and function of leaves within and between species. In the current study we utilised variation in leaf shape represented among individuals of a collection of Eurasian aspen (Populus tremula L.) sampled across Sweden and the remarkable extent of heterophylly present to establish morphological, cellular and transcriptional developmental time lines. We performed gene expression network and phenotypical regression analyses to identify genes of central importance or that were highly predictive of shape and size phenotypes during leaf development using a systems biology approach. We complemented this developmental study with a genome wide association study of leaf shape variation to identify single nucleotide polymorphisms associated with leaf shape and size, their genomic context and the biological role of associated genes. We then compared these association candidate genes to differentially expressed genes between groups of genotypes with highly contrasting leaf shapes, also considering whether there were expression quantitative trait loci associated with the genes. We demonstrate that our developmental gene expression series captured known biology for homologs of functionally characterised Arabidopsis thaliana genes and biological processes of importance during leaf development. We identified genes of high importance from the developmental series and natural variation analyses. These included genes with characterised functions in leaf development in addition to many novel candidates. Our systems genetics approach identified numerous genes supported by the developmental time series, phenotypic and expression association mapping and differential expression between phenotypic extremes. As such, we describe a rich resource for directing future functional characterisation studies and a comprehensive data resource characterising the role of gene expression during leaf development in aspen.

  • 5.
    Terebieniec, Barbara
    Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
    Using systems genetics to explore the complexity of leaf shape variation in Populus tremula2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Leaves are essential for sustaining humanity as they function as the energy and oxygen-producing organ of plants. Intensive research on physiological processes has contributed immensely to our understanding of the function of leaves. However, comparatively little is known about how leaf size and shape is determined. The aim of my PhD was to assay leaf shape variation among individuals of Populus tremula (European aspen) sampled across the distribution range of Sweden to characterize the genetic architecture underlying variation, including elucidating contributing molecular mechanisms.

    In this PhD I employed an integrated systems genetics and systems biology approach to identify genetic components of variation and to assign biological function to these. We integrated population-wide data on leaf shape, gene expression and genome variation from a collection of P. tremula genotypes and used this to perform genome-wide association studies. We then integrated these results with a systems biology transcriptomics study of leaf development to provide developmental and biological context. We demonstrate that our developmental gene expression series captured known homologs of functionally characterized Arabidopsis thaliana genes and biological processes of importance during leaf development. In addition to these known genes of high importance, we also identified many novel candidate genes. Our systems genetics approach identified numerous genes with a potential role in leaf development that was supported by the developmental time series. From our association studies and population analyses we have shown that there are no large-effect loci contributing to variation in leaf shape and that highly ranked loci associated with leaf shape are primarily located in the regulatory regions of genes. Furthermore, we identified loci controlling variation in gene expression and sets of genes with significant differential expression between groups of genotypes with highly contrasting leaf shapes. We show that genes with significant associations influencing expression among genotypes are enriched in the periphery of the corresponding gene co-expression network and that they experience relaxed selective constraint. Taken together, these results suggest that leaf shape is a highly complex trait controlled by a large number of loci, each contributing only a small effect, that those loci likely act via modulation of gene expression and that they do not show signals of adaptive selection. In addition, we adapted and optimized the method of spatial transcriptomics for use in plant species. This method provides a transcriptome-wide in situ, spatially-resolved assay of transcript expression at high spatial resolution.

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