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      The Arabidopsis Elongator Subunit ELP3 and ELP4 Confer Resistance to Bacterial Speck in Tomato

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          Abstract

          Although production of tomato ( Solanum lycopersicum) is threatened by a number of major diseases worldwide, it has been difficult to identify effective and durable management measures against these diseases. In this study, we attempted to improve tomato disease resistance by transgenic overexpression of genes encoding the Arabidopsis thaliana Elongator (AtELP) complex subunits AtELP3 and AtELP4. We show that overexpression of AtELP3 and AtELP4 significantly enhanced resistance to tomato bacterial speck caused by the Pseudomonas syringae pv. tomato strain J4 ( Pst J4) without clear detrimental effects on plant growth and development. Interestingly, the transgenic plants exhibited resistance to Pst J4 only when inoculated through foliar sprays but not through infiltration into the leaf apoplast. Although this result suggested possible involvement of stomatal immunity, we found that Pst J4 inoculation did not induce stomatal closure and there were no differences in stomatal apertures and conductance between the transgenic and control plants. Further RNA sequencing and real-time quantitative PCR analyses revealed a group of defense-related genes to be induced to higher levels after infection in the AtELP4 transgenic tomato plants than in the control, suggesting that the enhanced disease resistance of the transgenic plants may be attributed to elevated induction of defense responses. Additionally, we show that the tomato genome contains single-copy genes encoding all six Elongator subunits (SlELPs), which share high identities with the AtELP proteins, and that SlELP3 and SlELP4 complemented the Arabidopsis Atelp3 and Atelp4 mutants, respectively, indicating that the function of tomato Elongator is probably conserved. Taken together, our results not only shed new light on the tomato Elongator complex, but also revealed potential candidate genes for engineering disease resistance in tomato.

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          Most cited references54

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          An early step in wobble uridine tRNA modification requires the Elongator complex.

          Elongator has been reported to be a histone acetyltransferase complex involved in elongation of RNA polymerase II transcription. In Saccharomyces cerevisiae, mutations in any of the six Elongator protein subunit (ELP1-ELP6) genes or the three killer toxin insensitivity (KTI11-KTI13) genes cause similar pleiotropic phenotypes. By analyzing modified nucleosides in individual tRNA species, we show that the ELP1-ELP6 and KTI11-KTI13 genes are all required for an early step in synthesis of 5-methoxycarbonylmethyl (mcm5) and 5-carbamoylmethyl (ncm5) groups present on uridines at the wobble position in tRNA. Transfer RNA immunoprecipitation experiments showed that the Elp1 and Elp3 proteins specifically coprecipitate a tRNA susceptible to formation of an mcm5 side chain, indicating a direct role of Elongator in tRNA modification. The presence of mcm5U, ncm5U, or derivatives thereof at the wobble position is required for accurate and efficient translation, suggesting that the phenotypes of elp1-elp6 and kti11-kti13 mutants could be caused by a translational defect. Accordingly, a deletion of any ELP1-ELP6 or KTI11-KTI13 gene prevents an ochre suppressor tRNA that normally contains mcm5U from reading ochre stop codons.
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            Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance.

            Plant diseases cause massive losses in agriculture. Increasing the natural defenses of plants may reduce the impact of phytopathogens on agricultural productivity. Pattern-recognition receptors (PRRs) detect microbes by recognizing conserved pathogen-associated molecular patterns (PAMPs). Although the overall importance of PAMP-triggered immunity for plant defense is established, it has not been used to confer disease resistance in crops. We report that activity of a PRR is retained after its transfer between two plant families. Expression of EFR (ref. 4), a PRR from the cruciferous plant Arabidopsis thaliana, confers responsiveness to bacterial elongation factor Tu in the solanaceous plants Nicotiana benthamiana and tomato (Solanum lycopersicum), making them more resistant to a range of phytopathogenic bacteria from different genera. Our results in controlled laboratory conditions suggest that heterologous expression of PAMP recognition systems could be used to engineer broad-spectrum disease resistance to important bacterial pathogens, potentially enabling more durable and sustainable resistance in the field.
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              Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin.

              The generation of cortical projection neurons relies on the coordination of radial migration with branching. Here, we report that the multisubunit histone acetyltransferase Elongator complex, which contributes to transcript elongation, also regulates the maturation of projection neurons. Indeed, silencing of its scaffold (Elp1) or catalytic subunit (Elp3) cell-autonomously delays the migration and impairs the branching of projection neurons. Strikingly, neurons defective in Elongator show reduced levels of acetylated alpha-tubulin. Reduction of alpha-tubulin acetylation via expression of a nonacetylatable alpha-tubulin mutant leads to comparable defects in cortical neurons and suggests that alpha-tubulin is a target of Elp3. This is further supported by the demonstration that Elp3 promotes acetylation and counteracts HDAC6-mediated deacetylation of this substrate in vitro. Our results uncover alpha-tubulin as a target of the Elongator complex and suggest that a tight regulation of its acetylation underlies the maturation of cortical projection neurons.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                24 July 2018
                2018
                : 9
                : 1066
                Affiliations
                [1] 1Department of Plant Pathology, University of Florida , Gainesville, FL, United States
                [2] 2Interdisciplinary Center for Biotechnology Research, University of Florida , Gainesville, FL, United States
                [3] 3Department of Microbiology and Cell Science, University of Florida , Gainesville, FL, United States
                Author notes

                Edited by: Zhengqing Fu, University of South Carolina, United States

                Reviewed by: Yuxin Hu, Institute of Botany (CAS), China; Wen-Ming Wang, Sichuan Agricultural University, China

                *Correspondence: Jeffrey B. Jones, jbjones@ 123456ufl.edu Zhonglin Mou, zhlmou@ 123456ufl.edu

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.01066
                6066517
                1456fbd1-8661-4e93-852d-f211e3a8f704
                Copyright © 2018 Pereira, Yu, Zhang, Jones and Mou.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 09 May 2018
                : 29 June 2018
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 59, Pages: 14, Words: 0
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                tomato,the elongator complex,atelp4,transgenic overexpression,disease resistance,pseudomonas syringae

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