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      First RNA-seq approach to study fruit set and parthenocarpy in zucchini ( Cucurbita pepo L.)

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          Abstract

          Background

          Zucchini fruit set can be limited due to unfavourable environmental conditions in off-seasons crops that caused ineffective pollination/fertilization. Parthenocarpy, the natural or artificial fruit development without fertilization, has been recognized as an important trait to avoid this problem, and is related to auxin signalling. Nevertheless, differences found in transcriptome analysis during early fruit development of zucchini suggest that other complementary pathways could regulate fruit formation in parthenocarpic cultivars of this species. The development of next-generation sequencing technologies (NGS) as RNA-sequencing (RNA-seq) opens a new horizon for mapping and quantifying transcriptome to understand the molecular basis of pathways that could regulate parthenocarpy in this species. The aim of the current study was to analyze fruit transcriptome of two cultivars of zucchini, a non-parthenocarpic cultivar and a parthenocarpic cultivar, in an attempt to identify key genes involved in parthenocarpy.

          Results

          RNA-seq analysis of six libraries (unpollinated, pollinated and auxin treated fruit in a non-parthenocarpic and parthenocarpic cultivar) was performed mapping to a new version of C. pepo transcriptome, with a mean of 92% success rate of mapping. In the non-parthenocarpic cultivar, 6479 and 2186 genes were differentially expressed (DEGs) in pollinated fruit and auxin treated fruit, respectively. In the parthenocarpic cultivar, 10,497 in pollinated fruit and 5718 in auxin treated fruit. A comparison between transcriptome of the unpollinated fruit for each cultivar has been performed determining that 6120 genes were differentially expressed. Annotation analysis of these DEGs revealed that cell cycle, regulation of transcription, carbohydrate metabolism and coordination between auxin, ethylene and gibberellin were enriched biological processes during pollinated and parthenocarpic fruit set.

          Conclusion

          This analysis revealed the important role of hormones during fruit set, establishing the activating role of auxins and gibberellins against the inhibitory role of ethylene and different candidate genes that could be useful as markers for parthenocarpic selection in the current breeding programs of zucchini.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1632-2) contains supplementary material, which is available to authorized users.

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          Most cited references42

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          Gene Ontology: tool for the unification of biology

          Genomic sequencing has made it clear that a large fraction of the genes specifying the core biological functions are shared by all eukaryotes. Knowledge of the biological role of such shared proteins in one organism can often be transferred to other organisms. The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing. To this end, three independent ontologies accessible on the World-Wide Web (http://www.geneontology.org) are being constructed: biological process, molecular function and cellular component.
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            Cellular responses to auxin: division versus expansion.

            The phytohormone auxin is a major regulator of plant growth and development. Many aspects of these processes depend on the multiple controls exerted by auxin on cell division and cell expansion. The detailed mechanisms by which auxin controls these essential cellular responses are still poorly understood, despite recent progress in the identification of auxin receptors and components of auxin signaling pathways. The purpose of this review is to provide an overview of the present knowledge of the molecular mechanisms involved in the auxin control of cell division and cell expansion. In both cases, the involvement of at least two signaling pathways and of multiple targets of auxin action reflects the complexity of the subtle regulation of auxin-mediated cellular responses. In addition, it offers the necessary flexibility for generating differential responses within a given cell depending on its developmental context.
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              The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis.

              Auxin/indole-3-acetic acid (Aux/IAA) proteins are transcriptional regulators that mediate many aspects of plant responses to auxin. While functions of most Aux/IAAs have been defined mainly by gain-of-function mutant alleles in Arabidopsis thaliana, phenotypes associated with loss-of-function mutations have been scarce and subtle. We report here that the downregulation of IAA9, a tomato (Solanum lycopersicum) gene from a distinct subfamily of Aux/IAA genes, results in a pleiotropic phenotype, consistent with its ubiquitous expression pattern. IAA9-inhibited lines have simple leaves instead of wild-type compound leaves, and fruit development is triggered before fertilization, giving rise to parthenocarpy. This indicates that IAA9 is a key mediator of leaf morphogenesis and fruit set. In addition, antisense plants displayed auxin-related growth alterations, including enhanced hypocotyl/stem elongation, increased leaf vascularization, and reduced apical dominance. Auxin dose-response assays revealed that IAA9 downregulated lines were hypersensitive to auxin, although the only early auxin-responsive gene that was found to be upregulated in the antisense lines was IAA3. The activity of the IAA3 promoter was stimulated in the IAA9 antisense genetic background, indicating that IAA9 acts in planta as a transcriptional repressor of auxin signaling. While no mutation in any member of subfamily IV has been reported to date, the phenotypes associated with the downregulation of IAA9 reveal distinct and novel roles for members of the Aux/IAA gene family.
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                Author and article information

                Contributors
                teresa.pomares@juntadeandalucia.es
                mercedes.rio.celestino@juntadeandalucia.es
                mariab.roman@juntadeandalucia.es
                z42diraj@uco.es
                mpicosi@btc.upv.es
                pedro.gomez.j@juntadeandalucia.es
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                6 February 2019
                6 February 2019
                2019
                : 19
                : 61
                Affiliations
                [1 ]Genomics and Biotechnology Department, IFAPA Research Centre La Mojonera, Camino de San Nicolás, 1, 04745 La Mojonera, Almería, Spain
                [2 ]ISNI 0000 0001 2195 4653, GRID grid.425162.6, Genomics and Biotechnology Department, , IFAPA Research Centre Alameda del Obispo, ; Avd. Menéndez Pidal s/n, 14004 Córdoba, Spain
                [3 ]ISNI 0000 0001 2183 9102, GRID grid.411901.c, Genetics Department, , University of Cordoba, ; Av. de Medina Azahara, 5, 14071 Córdoba, Spain
                [4 ]ISNI 0000 0004 1770 5832, GRID grid.157927.f, Institute for the Conservation and Breeding of Agricultural Biodiversity (COMAV-UPV), , Universitat Politècnica de València, ; Camino de Vera s/n, 46022 Valencia, Spain
                Article
                1632
                10.1186/s12870-019-1632-2
                6366093
                30727959
                74cf30b4-473d-452c-93f9-9b4c7b9c32ee
                © The Author(s). 2019

                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
                : 10 May 2018
                : 4 January 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100007652, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria;
                Award ID: RTA2014-00078
                Award ID: RTA2011-00044-C02-01/02
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003359, Generalitat Valenciana;
                Award ID: PROMETEO/2017/078
                Funded by: IFAPA
                Award ID: PP.AVA.AVA201601.7
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                cucurbita pepo,zucchini,parthenocarpy,fruit set,differential gene expression,rna-seq

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