Dataset Information

Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis.

ABSTRACT: Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure-function relationships of the plant cell wall, it is imperative to trace the origin of its different components. The present study is focused on plant 1,4-β-xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and algae. It substantiates the findings by heterologous expression and biochemical characterization of a charophyte alga xylan synthase. Of the 12 known gene classes involved in 1,4-β-xylan formation, XYS1/IRX10 in plants, IRX7, IRX8, IRX9, IRX14 and GUX occurred for the first time in charophyte algae. An XYS1/IRX10 ortholog from Klebsormidium flaccidum, designated K. flaccidumXYLAN SYNTHASE-1 (KfXYS1), possesses 1,4-β-xylan synthase activity, and 1,4-β-xylan occurs in the K. flaccidum cell wall. These data suggest that plant 1,4-β-xylan originated in charophytes and shed light on the origin of one of the key cell wall innovations to occur in charophyte algae, facilitating terrestrialization and emergence of polysaccharide-based plant cell walls.

SUBMITTER: Jensen JK

PROVIDER: S-EPMC5902652 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis.

Jensen Jacob Krüger JK Busse-Wicher Marta M Poulsen Christian Peter CP Fangel Jonatan Ulrik JU Smith Peter James PJ Yang Jeong-Yeh JY Peña Maria-Jesus MJ Dinesen Malene Hessellund MH Martens Helle Juel HJ Melkonian Michael M Wong Gane Ka-Shu GK Moremen Kelley W KW Wilkerson Curtis Gene CG Scheller Henrik Vibe HV Dupree Paul P Ulvskov Peter P Urbanowicz Breeanna Rae BR Harholt Jesper J

The New phytologist 20180220 3

Insights into the evolution of plant cell walls have important implications for comprehending these diverse and abundant biological structures. In order to understand the evolving structure-function relationships of the plant cell wall, it is imperative to trace the origin of its different components. The present study is focused on plant 1,4-β-xylan, tracing its evolutionary origin by genome and transcriptome mining followed by phylogenetic analysis, utilizing a large selection of plants and al ...[more]

PMID: 29460505

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Project description:BackgroundXylan is a major hemicellulosic component in the cell walls of higher plants especially in the secondary walls of vascular cells which are playing important roles in physiological processes and overall mechanical strength. Being the second most abundant cell wall polymer after cellulose, xylan is an abundant non-cellulosic carbohydrate constituent of plant biomass. Xylan structures have been demonstrated to contribute to plant biomass recalcitrance during bioenergy applications. A critical understanding of xylan composition, structure, and biosynthesis in developing plant stems will allow an increased understanding of how cell walls are put together in this organ in a basic research, and, in applied research, will improve strategies in xylan engineering to reduce biomass recalcitrance for economically feasible biofuel production.MethodsWe describe an approach to enable the monitoring of xylan epitope structures in cell walls during the stem maturation process in Arabidopsis. The technique integrates glycome profiling, an in vitro immunoanalytical platform, and in situ immunolocalisation to provide comprehensive details on the presence, relative abundances, and dynamics with which diverse xylan epitope structures are integrated to the cell walls throughout the stem maturation process.ResultsOur experimental results and the supporting in silico analysis demonstrated that xylan deposition in stems occurs early on in stem development; however, xylan epitope types (representing substituted and unsubstituted regions on xylan backbone made of β-(1,4)-linked xylose residues) and the strength of their integration into the final wall structure vary during stem maturation.ConclusionsOur novel approach thus provides a method to comprehensively survey the differences in xylan epitope patterning and deposition occurring in stem development and thereby providing a robust tool for characterising altered xylan integration patterns in cell walls during the stem maturation process in diverse plant cell wall biosynthetic mutants. Our findings also suggest that this approach could rapidly and reliably delineate xylan deposition patterns in the cell walls of plants belonging to diverse phylogenetic classes providing novel insights into the functional roles of xylans in overall growth and development.

Project description:BackgroundXylan is the most abundant un-cellulosic polysaccharides of plant cell walls. Much progress in xylan biosynthesis has been gained in the model plant species Arabidopsis. Two homologous pairs Irregular Xylem 9 (IRX9)/9L and IRX14/14L from glycosyltransferase (GT) family 43 have been proved to play crucial roles in xylan backbone biosynthesis. However, xylan biosynthesis in grass such as Miscanthus remains poorly understood.ResultsWe characterized seven GT43 members in M. lutarioriparius, a promising bioenergy crop. Quantitative real-time RT-PCR (qRT-PCR) analysis revealed that the expression of MlGT43 genes was ubiquitously detected in the tissues examined. In-situ hybridization demonstrated that MlGT43A-B and MlGT43F-G were specifically expressed in sclerenchyma, while MlGT43C-E were expressed in both sclerenchyma and parenchyma. All seven MlGT43 proteins were localized to Golgi apparatus. Overexpression of MlGT43A-E but not MlGT43F and MlGT43G in Arabidopsis irx9 fully or partially rescued the mutant defects, including morphological changes, collapsed xylem and increased xylan contents, whereas overexpression of MlGT43F and MlGT43G but not MlGT43A-E complemented the defects of irx14, indicating that MlGT43A-E are functional orthologues of IRX9, while MlGT43F and MlGT43G are functional orthologues of IRX14. However, overexpression of all seven MlGT43 genes could not rescue the mucilage defects of irx14 seeds. Furthermore, transient transactivation analyses of MlGT43A-E reporters demonstrated that MlGT43A and MlGT43B but not MlGT43C-E were differentially activated by MlSND1, MlMYB46 or MlVND7.ConclusionThe results demonstrated that all seven MlGT43s are functionally conserved in xylan biosynthesis during secondary cell wall formation but diversify in seed coat mucilage xylan biosynthesis. The results obtained provide deeper insight into xylan biosynthesis in grass, which lay the foundation for genetic modification of grass cell wall components and structure to better suit for next-generation biofuel production.

Project description:BackgroundHorehound (Marrubium vulgare) is a medicinal plant whose signature bioactive compounds, marrubiin and related furanoid diterpenoid lactones, have potential applications for the treatment of cardiovascular diseases and type II diabetes. Lack of scalable plant cultivation and the complex metabolite profile of M. vulgare limit access to marrubiin via extraction from plant biomass. Knowledge of the marrubiin-biosynthetic enzymes can enable the development of metabolic engineering platforms for marrubiin production. We previously identified two diterpene synthases, MvCPS1 and MvELS, that act sequentially to form 9,13-epoxy-labd-14-ene. Conversion of 9,13-epoxy-labd-14-ene by cytochrome P450 monooxygenase (P450) enzymes can be hypothesized to facilitate key functional modification reactions in the formation of marrubiin and related compounds.ResultsMining a M. vulgare leaf transcriptome database identified 95 full-length P450 candidates. Cloning and functional analysis of select P450 candidates showing high transcript abundance revealed a member of the CYP71 family, CYP71AU87, that catalyzed the hydroxylation of 9,13-epoxy-labd-14-ene to yield two isomeric products, 9,13-epoxy labd-14-ene-18-ol and 9,13-epoxy labd-14-ene-19-ol, as verified by GC-MS and NMR analysis. Additional transient Nicotiana benthamiana co-expression assays of CYP71AU87 with different diterpene synthase pairs suggested that CYP71AU87 is specific to the sequential MvCPS1 and MvELS product 9,13-epoxy-labd-14-ene. Although the P450 products were not detectable in planta, high levels of CYP71AU87 gene expression in marrubiin-accumulating tissues supported a role in the formation of marrubiin and related diterpenoids in M. vulgare.ConclusionsIn a sequential reaction with the diterpene synthase pair MvCPS1 and MvELS, CYP71AU87 forms the isomeric products 9,13-epoxy labd-14-ene-18/19-ol as probable intermediates in marrubiin biosynthesis. Although its metabolic relevance in planta will necessitate further genetic studies, identification of the CYP71AU87 catalytic activity expands our knowledge of the functional landscape of plant P450 enzymes involved in specialized diterpenoid metabolism and can provide a resource for the formulation of marrubiin and related bioactive natural products.

Dataset Information

Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis.

Publications

Identification of an algal xylan synthase indicates that there is functional orthology between algal and plant cell wall biosynthesis.

Similar Datasets

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