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      Intergenerational environmental effects: functional signals in offspring transcriptomes and metabolomes after parental jasmonic acid treatment in apomictic dandelion

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          Summary

          • Parental environments can influence offspring traits. However, the magnitude of the impact of parental environments on offspring molecular phenotypes is poorly understood. Here, we test the direct effects and intergenerational effects of jasmonic acid ( JA) treatment, which is involved in herbivory‐induced defense signaling, on transcriptomes and metabolomes in apomictic common dandelion ( Taraxacum officinale).

          • In a full factorial crossed design with parental and offspring JA and control treatments, we performed leaf RNA‐seq gene expression analysis, LCMS metabolomics and total phenolics assays in offspring plants.

          • Expression analysis, leveraged by a de novo assembled transcriptome, revealed an induced response to JA exposure that is consistent with known JA effects. The intergenerational effect of treatment was considerable: 307 of 858 detected JA‐responsive transcripts were affected by parental JA treatment. In terms of the numbers of metabolites affected, the magnitude of the chemical response to parental JA exposure was c. 10% of the direct JA treatment response. Transcriptome and metabolome analyses both identified the phosphatidylinositol signaling pathway as a target of intergenerational JA effects.

          • Our results highlight that parental environments can have substantial effects in offspring generations. Transcriptome and metabolome assays provide a basis for zooming in on the potential mechanisms of inherited JA effects.

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          Most cited references40

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          Statistical methods for assessing agreement between two methods of clinical measurement.

          In clinical measurement comparison of a new measurement technique with an established one is often needed to see whether they agree sufficiently for the new to replace the old. Such investigations are often analysed inappropriately, notably by using correlation coefficients. The use of correlation is misleading. An alternative approach, based on graphical techniques and simple calculations, is described, together with the relation between this analysis and the assessment of repeatability.
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            Induced systemic resistance by beneficial microbes.

            Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
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              Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor

              Jasmonates (JAs) are a family of plant hormones that regulate plant growth, development, and responses to stress. The F-box protein CORONATINE-INSENSITIVE 1 (COI1) mediates JA signaling by promoting hormone-dependent ubiquitination and degradation of transcriptional repressor JAZ proteins. Despite its importance, the mechanism of JA perception remains unclear. Here we present structural and pharmacological data to show that the true JA receptor is a complex of both COI1 and JAZ. COI1 contains an open pocket that recognizes the bioactive hormone, (3R,7S)-jasmonoyl-L-isoleucine (JA-Ile), with high specificity. High-affinity hormone binding requires a bipartite JAZ degron sequence consisting of a conserved α-helix for COI1 docking and a loop region to trap the hormone in its binding pocket. In addition, we identify a third critical component of the JA co-receptor complex, inositol pentakisphosphate, which interacts with both COI1 and JAZ adjacent to the ligand. Our results unravel the mechanism of JA perception and highlight the ability of F-box proteins to evolve as multi-component signaling hubs.
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                Author and article information

                Contributors
                k.verhoeven@nioo.knaw.nl
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                16 October 2017
                January 2018
                : 217
                : 2 ( doiID: 10.1111/nph.2018.217.issue-2 )
                : 871-882
                Affiliations
                [ 1 ] Terrestrial Ecology Netherlands Institute of Ecology (NIOO‐KNAW) Droevendaalsesteeg 10 Wageningen the Netherlands
                [ 2 ] Plant–Microbe Interactions Utrecht University Padualaan 6 Utrecht the Netherlands
                [ 3 ] Molecular Genetics and Microbiology, and the Genetics Institute University of Florida 2033 Mowry Road Gainesville FL 32610 USA
                [ 4 ] Center for Plant Molecular Biology Tübingen University Auf der Morgenstelle 32 Tübingen D‐72076 Germany
                [ 5 ] Molecular Interaction Ecology Department of Plant Science Radboud University Nijmegen PO Box 9010 Nijmegen 6500 NL the Netherlands
                Author notes
                [*] [* ] Author for correspondence:

                Koen J. F. Verhoeven

                Tel: +31 (0)317 473624

                Email: k.verhoeven@ 123456nioo.knaw.nl

                Article
                NPH14835 2017-24190
                10.1111/nph.14835
                5741498
                29034954
                dc4da418-ff7b-493a-9e62-9b0ecb287d43
                © 2017 The Authors. New Phytologist © 2017 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 April 2017
                : 31 August 2017
                Page count
                Figures: 6, Tables: 2, Pages: 12, Words: 9987
                Funding
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek
                Award ID: VIDI 864.10.008
                Award ID: Visiting Scholar Grant 040.11.358
                Funded by: KNAW
                Funded by: National Institutes of Health (NIH)
                Award ID: U24 DK097209
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph14835
                January 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.2.8 mode:remove_FC converted:12.01.2018

                Plant science & Botany
                induced defenses,jasmonic acid (ja),lc‐ms,metabolomics,rna‐seq,taraxacum officinale (common dandelion),transcriptomics,transgenerational effects

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