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      Multiple levels of crosstalk in hormone networks regulating plant defense

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          Summary

          Plant hormones are essential for regulating the interactions between plants and their complex biotic and abiotic environments. Each hormone initiates a specific molecular pathway and these different hormone pathways are integrated in a complex network of synergistic, antagonistic and additive interactions. This inter‐pathway communication is called hormone crosstalk. By influencing the immune network topology, hormone crosstalk is essential for tailoring plant responses to diverse microbes and insects in diverse environmental and internal contexts. Crosstalk provides robustness to the immune system but also drives specificity of induced defense responses against the plethora of biotic interactors. Recent advances in dry‐lab and wet‐lab techniques have greatly enhanced our understanding of the broad‐scale effects of hormone crosstalk on immune network functioning and have revealed underlying principles of crosstalk mechanisms. Molecular studies have demonstrated that hormone crosstalk is modulated at multiple levels of regulation, such as by affecting protein stability, gene transcription and hormone homeostasis. These new insights into hormone crosstalk regulation of plant defense are reviewed here, with a focus on crosstalk acting on the jasmonic acid pathway in Arabidopsis thaliana, highlighting the transcription factors MYC2 and ORA59 as major targets for modulation by other hormones.

          Significance Statement

          Plant hormone pathways interact with each other in a complex network, which manages synergistic, antagonistic and additive effects between different sectors of the network, thereby providing robustness and specificity to the immune system. Here we review hormone crosstalk regulation at the network, protein, gene expression and hormone homeostasis levels.

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          Most cited references131

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          JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.

          Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCF(COI1) ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl-isoleucine (JA-Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCF(COI1) ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCF(COI1)-JAZ1 protein complex as a site of perception of the plant hormone JA-Ile.
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            Structure and function of the feed-forward loop network motif.

            Engineered systems are often built of recurring circuit modules that carry out key functions. Transcription networks that regulate the responses of living cells were recently found to obey similar principles: they contain several biochemical wiring patterns, termed network motifs, which recur throughout the network. One of these motifs is the feed-forward loop (FFL). The FFL, a three-gene pattern, is composed of two input transcription factors, one of which regulates the other, both jointly regulating a target gene. The FFL has eight possible structural types, because each of the three interactions in the FFL can be activating or repressing. Here, we theoretically analyze the functions of these eight structural types. We find that four of the FFL types, termed incoherent FFLs, act as sign-sensitive accelerators: they speed up the response time of the target gene expression following stimulus steps in one direction (e.g., off to on) but not in the other direction (on to off). The other four types, coherent FFLs, act as sign-sensitive delays. We find that some FFL types appear in transcription network databases much more frequently than others. In some cases, the rare FFL types have reduced functionality (responding to only one of their two input stimuli), which may partially explain why they are selected against. Additional features, such as pulse generation and cooperativity, are discussed. This study defines the function of one of the most significant recurring circuit elements in transcription networks.
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              Determination and inference of eukaryotic transcription factor sequence specificity.

              Transcription factor (TF) DNA sequence preferences direct their regulatory activity, but are currently known for only ∼1% of eukaryotic TFs. Broadly sampling DNA-binding domain (DBD) types from multiple eukaryotic clades, we determined DNA sequence preferences for >1,000 TFs encompassing 54 different DBD classes from 131 diverse eukaryotes. We find that closely related DBDs almost always have very similar DNA sequence preferences, enabling inference of motifs for ∼34% of the ∼170,000 known or predicted eukaryotic TFs. Sequences matching both measured and inferred motifs are enriched in chromatin immunoprecipitation sequencing (ChIP-seq) peaks and upstream of transcription start sites in diverse eukaryotic lineages. SNPs defining expression quantitative trait loci in Arabidopsis promoters are also enriched for predicted TF binding sites. Importantly, our motif "library" can be used to identify specific TFs whose binding may be altered by human disease risk alleles. These data present a powerful resource for mapping transcriptional networks across eukaryotes. Copyright © 2014 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                s.vanwees@uu.nl
                Journal
                Plant J
                Plant J
                10.1111/(ISSN)1365-313X
                TPJ
                The Plant Journal
                John Wiley and Sons Inc. (Hoboken )
                0960-7412
                1365-313X
                19 December 2020
                January 2021
                : 105
                : 2 ( doiID: 10.1111/tpj.v105.2 )
                : 489-504
                Affiliations
                [ 1 ] Plant‐Microbe Interactions Department of Biology Science4Life Utrecht University P.O. Box 800.56 Utrecht 3408 TB The Netherlands
                Author notes
                [*] [* ] For correspondence (e‐mail s.vanwees@ 123456uu.nl ).

                Author information
                https://orcid.org/0000-0001-7301-9202
                https://orcid.org/0000-0002-2295-7271
                Article
                TPJ15124
                10.1111/tpj.15124
                7898868
                33617121
                7143da4a-a4ff-4a67-b2cf-ab65e97e1f19
                © 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 26 August 2020
                : 21 November 2020
                : 30 November 2020
                Page count
                Figures: 3, Tables: 0, Pages: 16, Words: 38964
                Funding
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek , open-funder-registry 10.13039/501100003246;
                Award ID: ALWGS.2016.005
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior , open-funder-registry 10.13039/501100002322;
                Award ID: DF 70040‐020
                Funded by: Ministry of Education , open-funder-registry 10.13039/100009950;
                Categories
                Si Phytohormones 2021
                Plant Hormone Functions and Interactions in Biological Systems
                Custom metadata
                2.0
                January 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.7 mode:remove_FC converted:22.02.2021

                Plant science & Botany
                hormone crosstalk,defense,network,jasmonic acid,salicylic acid,abscisic acid,ethylene,myc2,ora59

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