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  • 1. Giacomello, Stefania
    et al.
    Salmen, Fredrik
    Terebieniec, Barbara K.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Vickovic, Sanja
    Navarro, José Fernandez
    Alexeyenko, Andrey
    Reimegard, Johan
    McKee, Lauren S.
    Mannapperuma, Chanaka
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Bulone, Vincent
    Ståhl, Patrik L.
    Sundström, Jens F.
    Street, Nathaniel
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Lundeberg, Joakim
    Spatially resolved transcriptome profiling in model plant species2017Ingår i: Nature Plants, ISSN 2055-026X, Vol. 3, nr 6, artikel-id 17061Artikel i tidskrift (Refereegranskat)
    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 universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Schiffthaler, Bastian
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Robinson, Kathryn M.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Terebieniec, Barbara K.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Vucak, Matej
    Mannapperuma, Chanaka
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Bailey, Mark
    Jansson, Stefan
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Hvidsten, Torgeir
    Street, Nathaniel R.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Leaf shape in Populus tremula is a complex, omnigenic trait2020Ingår i: Ecology and Evolution, E-ISSN 2045-7758, Vol. 10, nr 21, s. 11922-11940Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Leaf shape is a defining feature of how we recognize and classify plant species. Although there is extensive variation in leaf shape within many species, few studies have disentangled the underlying genetic architecture. We characterized the genetic architecture of leaf shape variation in Eurasian aspen (Populus tremula L.) by performing genome‐wide association study (GWAS) for physiognomy traits. To ascertain the roles of identified GWAS candidate genes within the leaf development transcriptional program, we generated RNA‐Seq data that we used to perform gene co‐expression network analyses from a developmental series, which is publicly available within the PlantGenIE resource. We additionally used existing gene expression measurements across the population to analyze GWAS candidate genes in the context of a population‐wide co‐expression network and to identify genes that were differentially expressed between groups of individuals with contrasting leaf shapes. These data were integrated with expression GWAS (eQTL) results to define a set of candidate genes associated with leaf shape variation. Our results identified no clear adaptive link to leaf shape variation and indicate that leaf shape traits are genetically complex, likely determined by numerous small‐effect variations in gene expression. Genes associated with shape variation were peripheral within the population‐wide co‐expression network, were not highly connected within the leaf development co‐expression network, and exhibited signatures of relaxed selection. As such, our results are consistent with the omnigenic model.

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  • 3.
    Mähler, Niklas
    et al.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Norwegian Univ Life Sci, Dept Chem Biotechnol & Food Sci, Norway.
    Wang, Jing
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och geovetenskap. Centre for Integrative Genetics, Faculty of Biosciences, Norwegian University of Life Sciences, Norway.
    Terebieniec, Barbara K.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Ingvarsson, Pär K.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för ekologi, miljö och geovetenskap. Swedish Univ Agr Sci, Dept Plant Biol, Uppsala, Sweden.
    Street, Nathaniel R.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Hvidsten, Torgeir R.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Norwegian Univ Life Sci, Dept Chem Biotechnol & Food Sci, As, Norway.
    Gene co-expression network connectivity is an important determinant of selective constraint2017Ingår i: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 13, nr 4, artikel-id e1006402Artikel i tidskrift (Refereegranskat)
    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.

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  • 4. 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 universitet, Teknisk-naturvetenskapliga fakulteten, Kemiska institutionen.
    Derba-Maceluch, Marta
    Department of Forest Genetics and Plant Physiology, SLU, Umeå Plant Science Centre (UPSC), Umeå, Sweden.
    Grahn, Thomas
    Schiffthaler, Bastian
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Ulvcrona, Thomas
    Ozparpucu, Merve
    Rüggeberg, Markus
    Lundqvist, Sven-Olof
    Street, Nathaniel
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Jönsson, Leif J.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Kemiska institutionen.
    Mellerowicz, Ewa J.
    Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome2018Ingår i: New Phytologist, ISSN 0028-646X, Vol. 219, nr 1, s. 230-245Artikel i tidskrift (Refereegranskat)
    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.

  • 5.
    Schiffthaler, Bastian
    et al.
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Terebieniec, Barbara K
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Mähler, Niklas
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Robinson, Kathryn M
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Mannapperuma, Chanaka
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Jansson, Stefan
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Street, Nathaniel R
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    An integrated functional genomics and systems genetics analysis of leaf shape in Populus tremula Manuskript (preprint) (Övrigt vetenskapligt)
    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.

  • 6.
    Terebieniec, Barbara
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik. Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC).
    Gene Expression and Growth Analyses in Populus RNAi lines Targeting Xylan Biosynthetic Gene Family GT 432012Självständigt arbete på avancerad nivå (masterexamen), 20 poäng / 30 hpStudentuppsats (Examensarbete)
    Abstract [en]

    Wood biomass is coming into focus as a good alternative renewable energy feedstock. Fast-growing woody plants, such as Populus species, offer potential as a bioenergy crop mediated by their abundance of energy containing cell wall polysaccharides.

    Furthermore, the first tree genome sequencing of Populus trichocarpa (poplar) offers an opportunity for genetic manipulation of woody cell components in order to optimize it for instance as an energy crop. Plant cell walls are very complex structures consisting of biopolymers, which form a network in the secondary wall. Cellulose, for instance, is organized as microfibrils consisting of β‐1,4‐glucan chains, whereas the hemicelluloses present heterogeneous polysaccharide groups. Within the hemicelluloses, xylans are the most abundant. The biosynthesis of hemicelluloses is still poorly understood.

    In order to investigate the biological role of GT43 genes during wood formation, transgenic hybrid aspen RNAi lines targeting GT43 have been created (Ratke et al., unpublished). Three GT43 genes (GT43B, GT43C and GT43F), and their double (GT43BC, GT43BF, GT43CF) and triple (GT43BCF) combinations, were selected to be targeted by RNAi. All the constructs were fused to the constitutive cauliflower 35 (CaM35S) and a wood-specific (WP) promoter and transformed into hybrid aspen (Populus tremula x tremuloides).

    The first part of the study focuses on selecting the most down‐regulated GT43 RNAi lines by using real‐time quantitative PCR analysis. We used a stepwise screening strategy starting from 20 individual in vitro transformant lines per construct. During the two in vitro screening steps we used in vitro grown stem tissue as an RNA source. The first in vitro screening narrowed down the number of lines to eight per each construct. After second in vitro screening, four most down regulated lines per construct were selected in order to grow them in greenhouse conditions and obtain woody tissue for further analyses. Third screening was applied when the GT43 RNAi plants were growing under greenhouse conditions and it used petioles as an RNA source. After the third screening, three best lines were selected per construct based on RNA analysis and additional chemical analyses not presented here. For the final gene expression analysis of selected three best lines per construct, we used freeze-dried wood or bark powder as an RNA source. The GT43 gene expression analysis base on quantitative real‐time PCR.

    These results are promising for developing Populus into a bioenergy crop. The use of molecular tools such a quantitative real-time PCR in stepwise screenings in order to select most down‐regulated lines of hybrid aspen resulted in selection of significantly altered lines as compared to the wild type. The future development of this technology should possibly use a higher number of transgenic lines as a starting point for selection.

  • 7.
    Terebieniec, Barbara
    Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Umeå Plant Science Centre (UPSC). Umeå universitet, Teknisk-naturvetenskapliga fakulteten, Institutionen för fysiologisk botanik.
    Using systems genetics to explore the complexity of leaf shape variation in Populus tremula2019Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
    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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