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      Overexpression of plum auxin receptor PslTIR1 in tomato alters plant growth, fruit development and fruit shelf-life characteristics

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          Abstract

          Background

          TIR1-like proteins are F-box auxin receptors. Auxin binding to the F-box receptor proteins promotes the formation of SCF TIR1 ubiquitin ligase complex that targets the auxin repressors, Aux/IAAs, for degradation via the ubiquitin/26S proteasome pathway. The release of auxin response factors (ARFs) from their Aux/IAA partners allows ARFs to mediate auxin-responsive changes in downstream gene transcription. In an attempt to understand the potential role of auxin during fruit development, a plum auxin receptor, PslTIR1, has previously been characterized at the cellular, biochemical and molecular levels, but the biological significance of this protein is still lacking. In the present study, tomato ( Solanum lycopersicum) was used as a model to investigate the phenotypic and molecular changes associated with the overexpression of PslTIR1.

          Results

          The findings of the present study highlighted the critical role of PslTIR1 as positive regulator of auxin-signalling in coordinating the development of leaves and fruits. This was manifested by the entire leaf morphology of transgenic tomato plants compared to the wild-type compound leaf patterning. Moreover, transgenic plants produced parthenocarpic fruits, a characteristic property of auxin hypersensitivity. The autocatalytic ethylene production associated with the ripening of climacteric fruits was not significantly altered in transgenic tomato fruits. Nevertheless, the fruit shelf-life characteristics were affected by transgene presence, mainly through enhancing fruit softening rate. The short shelf-life of transgenic tomatoes was associated with dramatic upregulation of several genes encoding proteins involved in cell-wall degradation, which determine fruit softening and subsequent fruit shelf-life.

          Conclusions

          The present study sheds light into the involvement of PslTIR1 in regulating leaf morphology, fruit development and fruit softening-associated ripening, but not autocatalytic ethylene production. The results demonstrate that auxin accelerates fruit softening independently of ethylene action and this is probably mediated through the upregulation of many cell-wall metabolism genes.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-016-0746-z) contains supplementary material, which is available to authorized users.

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          Most cited references47

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          Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana.

          One of the most striking examples of plant developmental plasticity to changing environmental conditions is the modulation of root system architecture (RSA) in response to nitrate supply. Despite the fundamental and applied significance of understanding this process, the molecular mechanisms behind nitrate-regulated changes in developmental programs are still largely unknown. Small RNAs (sRNAs) have emerged as master regulators of gene expression in plants and other organisms. To evaluate the role of sRNAs in the nitrate response, we sequenced sRNAs from control and nitrate-treated Arabidopsis seedlings using the 454 sequencing technology. miR393 was induced by nitrate in these experiments. miR393 targets transcripts that code for a basic helix-loop-helix (bHLH) transcription factor and for the auxin receptors TIR1, AFB1, AFB2, and AFB3. However, only AFB3 was regulated by nitrate in roots under our experimental conditions. Analysis of the expression of this miR393/AFB3 module, revealed an incoherent feed-forward mechanism that is induced by nitrate and repressed by N metabolites generated by nitrate reduction and assimilation. To understand the functional role of this N-regulatory module for plant development, we analyzed the RSA response to nitrate in AFB3 insertional mutant plants and in miR393 overexpressors. RSA analysis in these plants revealed that both primary and lateral root growth responses to nitrate were altered. Interestingly, regulation of RSA by nitrate was specifically mediated by AFB3, indicating that miR393/AFB3 is a unique N-responsive module that controls root system architecture in response to external and internal N availability in Arabidopsis.
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            Recent advances in ethylene research.

            Ethylene regulates many aspects of the plant life cycle, including seed germination, root initiation, flower development, fruit ripening, senescence, and responses to biotic and abiotic stresses. It thus plays a key role in responses to the environment that have a direct bearing on a plant's fitness for adaptation and reproduction. In recent years, there have been major advances in our understanding of the molecular mechanisms regulating ethylene synthesis and action. Screening for mutants of the triple response phenotype of etiolated Arabidopsis seedlings, together with map-based cloning and candidate gene characterization of natural mutants from other plant species, has led to the identification of many new genes for ethylene biosynthesis, signal transduction, and response pathways. The simple chemical nature of ethylene contrasts with its regulatory complexity. This is illustrated by the multiplicity of genes encoding the key ethylene biosynthesis enzymes 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase, multiple ethylene receptors and signal transduction components, and the complexity of regulatory steps involving signalling relays and control of mRNA and protein synthesis and turnover. In addition, there are extensive interactions with other hormones. This review integrates knowledge from the model plant Arabidopsis and other plant species and focuses on key aspects of recent research on regulatory networks controlling ethylene synthesis and its role in flower development and fruit ripening.
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              Fruits: A Developmental Perspective.

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                Author and article information

                Contributors
                ielshark@uoguelph.ca
                ssherif@uoguelph.ca
                welkayal@uoguelph.ca
                brian.jones@sydney.edu.au
                zhengguoli@cqu.edu.cn
                asulliva@uoguelph.ca
                +1 (905) 562-4141 , jsubrama@uoguelph.ca
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                29 February 2016
                29 February 2016
                2016
                : 16
                : 56
                Affiliations
                [ ]Department of Plant Agriculture, University of Guelph, Vineland Station, ON Canada
                [ ]Damanhour University, Faculty of Agriculture, Damanhour, Egypt
                [ ]The University of Sydney, Faculty of Agriculture, Sydney, Australia
                [ ]Chongqing University, Genetic Engineering Research Center, Bioengineering College, Chongqing, China
                [ ]Department of Plant Agriculture, University of Guelph, Guelph, ON Canada
                Article
                746
                10.1186/s12870-016-0746-z
                4772300
                26927309
                378385b1-d088-44a8-8ae8-58420f19503c
                © El-Sharkawy et al. 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 7 September 2015
                : 26 February 2016
                Funding
                Funded by: Ontario Tender Fruit Producers Marketing Board
                Funded by: Early Researcher Award
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100000094, Ontario Ministry of Agriculture, Food and Rural Affairs (CA);
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Plant science & Botany
                auxin receptors,auxin/ethylene cross-talk,cell-wall metabolism,fruit-set,fruit firmness,plant development,reproductive growth,shelf-life

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