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      Fungal endophyte infection of ryegrass reprograms host metabolism and alters development

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          Summary

          • Beneficial associations between plants and microbes play an important role in both natural and agricultural ecosystems. For example, associations between fungi of the genus Epichloë, and cool‐season grasses are known for their ability to increase resistance to insect pests, fungal pathogens and drought. However, little is known about the molecular changes induced by endophyte infection.

          • To study the impact of endophyte infection, we compared the expression profiles, based on RNA sequencing, of perennial ryegrass infected with Epichloë festucae with noninfected plants.

          • We show that infection causes dramatic changes in the expression of over one third of host genes. This is in stark contrast to mycorrhizal associations, where substantially fewer changes in host gene expression are observed, and is more similar to pathogenic interactions. We reveal that endophyte infection triggers reprogramming of host metabolism, favouring secondary metabolism at a cost to primary metabolism. Infection also induces changes in host development, particularly trichome formation and cell wall biogenesis.

          • Importantly, this work sheds light on the mechanisms underlying enhanced resistance to drought and super‐infection by fungal pathogens provided by fungal endophyte infection. Finally, our study reveals that not all beneficial plant–microbe associations behave the same in terms of their effects on the host.

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          Most cited references35

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          NIH Image to ImageJ: 25 years of image analysis.

          For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the analysis of scientific images. We discuss the origins, challenges and solutions of these two programs, and how their history can serve to advise and inform other software projects.
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            Metabolic priming by a secreted fungal effector.

            Maize smut caused by the fungus Ustilago maydis is a widespread disease characterized by the development of large plant tumours. U. maydis is a biotrophic pathogen that requires living plant tissue for its development and establishes an intimate interaction zone between fungal hyphae and the plant plasma membrane. U. maydis actively suppresses plant defence responses by secreted protein effectors. Its effector repertoire comprises at least 386 genes mostly encoding proteins of unknown function and expressed exclusively during the biotrophic stage. The U. maydis secretome also contains about 150 proteins with probable roles in fungal nutrition, fungal cell wall modification and host penetration as well as proteins unlikely to act in the fungal-host interface like a chorismate mutase. Chorismate mutases are key enzymes of the shikimate pathway and catalyse the conversion of chorismate to prephenate, the precursor for tyrosine and phenylalanine synthesis. Root-knot nematodes inject a secreted chorismate mutase into plant cells likely to affect development. Here we show that the chorismate mutase Cmu1 secreted by U. maydis is a virulence factor. The enzyme is taken up by plant cells, can spread to neighbouring cells and changes the metabolic status of these cells through metabolic priming. Secreted chorismate mutases are found in many plant-associated microbes and might serve as general tools for host manipulation.
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              New insights into pectin methylesterase structure and function.

              In bacteria, fungi and plants, pectin methylesterases are ubiquitous enzymes that modify the degree of methylesterification of pectins, which are major components of plant cell walls. Such changes in pectin structure are associated with changes in cellular adhesion, plasticity, pH and ionic contents of the cell wall and influence plant development and stress responses. In plants, pectin methylesterases belong to large multigene families, are regulated in a highly specific manner, and are involved in vegetative and reproductive processes, including wood and pollen formation, in addition to plant-pathogen interactions. Although, overall, protein structures are highly conserved between isoforms, recent data indicate that structural variations might be associated with the targeting and functions of specific pectin methylesterases.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                December 2015
                25 August 2015
                : 208
                : 4 ( doiID: 10.1111/nph.2015.208.issue-4 )
                : 1227-1240
                Affiliations
                [ 1 ] Institute of Fundamental SciencesMassey University Palmerston North 4442New Zealand
                [ 2 ] The Bio‐Protection Research CentreMassey University Palmerston North 4442New Zealand
                [ 3 ] Institute of Agriculture and EnvironmentMassey University Palmerston North 4442New Zealand
                [ 4 ] Research School of BiologyCollege of Medicine, Biology and Environment Australian National University Canberra ACT 0200Australia
                [ 5 ] School of Medical SciencesUniversity of Otago Dunedin 9054New Zealand
                Author notes
                [*] [* ] Author for correspondence:

                Murray P. Cox

                Tel: +64 6 356 9099 ext 84747

                Email: m.p.cox@ 123456massey.ac.nz

                [†]

                These authors contributed equally to this work.

                Article
                NPH13614 2015-19871
                10.1111/nph.13614
                5049663
                26305687
                85ba2054-2429-4901-a563-068f8723efb7
                © 2015 The Authors. New Phytologist © 2015 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 03 June 2015
                : 18 July 2015
                Page count
                Pages: 14
                Funding
                Funded by: Bio‐Protection Research Centre
                Funded by: Massey University Research Fund
                Funded by: Royal Society of New Zealand Rutherford Fellowship
                Award ID: RDF‐10‐MAU‐001
                Funded by: Royal Society of New Zealand Marsden Fund
                Award ID: MAU‐14‐03
                Award ID: MAU‐13‐02
                Funded by: Australian Research Council Future Fellowship
                Award ID: FT110100698
                Funded by: AgResearch
                Funded by: Massey University
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph13614
                December 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:04.10.2016

                Plant science & Botany
                endophyte,metabolism,mutualism,rnaseq,ryegrass,symbiosis
                Plant science & Botany
                endophyte, metabolism, mutualism, rnaseq, ryegrass, symbiosis

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