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VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development
VviAGL11, the Arabidopsis SEEDSTICK homolog, has been proposed to have a causative role in grapevine stenospermocarpy. An association between a mutation in the coding sequence (CDS) and the seedless phenotype was reported, however, no working mechanisms have been demonstrated yet. We performed a dee...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9433981/ https://www.ncbi.nlm.nih.gov/pubmed/36061618 http://dx.doi.org/10.1093/hr/uhac133 |
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author | Amato, Alessandra Cardone, Maria Francesca Ocarez, Nallatt Alagna, Fiammetta Ruperti, Benedetto Fattorini, Chiara Velasco, Riccardo Mejía, Nilo Zenoni, Sara Bergamini, Carlo |
author_facet | Amato, Alessandra Cardone, Maria Francesca Ocarez, Nallatt Alagna, Fiammetta Ruperti, Benedetto Fattorini, Chiara Velasco, Riccardo Mejía, Nilo Zenoni, Sara Bergamini, Carlo |
author_sort | Amato, Alessandra |
collection | PubMed |
description | VviAGL11, the Arabidopsis SEEDSTICK homolog, has been proposed to have a causative role in grapevine stenospermocarpy. An association between a mutation in the coding sequence (CDS) and the seedless phenotype was reported, however, no working mechanisms have been demonstrated yet. We performed a deep investigation of the full VviAGL11 gene sequence in a collection of grapevine varieties belonging to several seedlessness classes that revealed three different promoter-CDS combinations. By investigating the expression of the three VviAGL11 alleles, and by evaluating their ability to activate the promoter region, we observed that VviAGL11 self-activates in a specific promoter-CDS combination manner. Furthermore, by transcriptomic analyses on ovule and developing seeds in seeded and seedless varieties and co-expression approaches, candidate VviAGL11 targets were identified and further validated through luciferase assay and in situ hybridization. We demonstrated that VviAGL11 Wild Type CDS activates Methyl jasmonate esterase and Indole-3-acetate beta-glucosyltransferase, both involved in hormone signaling and Isoflavone reductase, involved in secondary metabolism. The dominant-negative effect of the mutated CDS was also functionally ectopically validated in target induction. VviAGL11 was shown to co-localize with its targets in the outer seed coat integument, supporting its direct involvement in seed development, possibly by orchestrating the crosstalk among MeJA, auxin, and isoflavonoids synthesis. In conclusion, the VviAGL11 expression level depends on the promoter-CDS allelic combination, and this will likely affect its ability to activate important triggers of the seed coat development. The dominant-negative effect of the mutated VviAGL11 CDS on the target genes activation was molecularly validated. A new regulatory mechanism correlating VviAGL11 haplotype assortment and seedlessness class in grapevine is proposed. |
format | Online Article Text |
id | pubmed-9433981 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-94339812022-09-01 VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development Amato, Alessandra Cardone, Maria Francesca Ocarez, Nallatt Alagna, Fiammetta Ruperti, Benedetto Fattorini, Chiara Velasco, Riccardo Mejía, Nilo Zenoni, Sara Bergamini, Carlo Hortic Res Article VviAGL11, the Arabidopsis SEEDSTICK homolog, has been proposed to have a causative role in grapevine stenospermocarpy. An association between a mutation in the coding sequence (CDS) and the seedless phenotype was reported, however, no working mechanisms have been demonstrated yet. We performed a deep investigation of the full VviAGL11 gene sequence in a collection of grapevine varieties belonging to several seedlessness classes that revealed three different promoter-CDS combinations. By investigating the expression of the three VviAGL11 alleles, and by evaluating their ability to activate the promoter region, we observed that VviAGL11 self-activates in a specific promoter-CDS combination manner. Furthermore, by transcriptomic analyses on ovule and developing seeds in seeded and seedless varieties and co-expression approaches, candidate VviAGL11 targets were identified and further validated through luciferase assay and in situ hybridization. We demonstrated that VviAGL11 Wild Type CDS activates Methyl jasmonate esterase and Indole-3-acetate beta-glucosyltransferase, both involved in hormone signaling and Isoflavone reductase, involved in secondary metabolism. The dominant-negative effect of the mutated CDS was also functionally ectopically validated in target induction. VviAGL11 was shown to co-localize with its targets in the outer seed coat integument, supporting its direct involvement in seed development, possibly by orchestrating the crosstalk among MeJA, auxin, and isoflavonoids synthesis. In conclusion, the VviAGL11 expression level depends on the promoter-CDS allelic combination, and this will likely affect its ability to activate important triggers of the seed coat development. The dominant-negative effect of the mutated VviAGL11 CDS on the target genes activation was molecularly validated. A new regulatory mechanism correlating VviAGL11 haplotype assortment and seedlessness class in grapevine is proposed. Oxford University Press 2022-06-10 /pmc/articles/PMC9433981/ /pubmed/36061618 http://dx.doi.org/10.1093/hr/uhac133 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Nanjing Agricultural University https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Article Amato, Alessandra Cardone, Maria Francesca Ocarez, Nallatt Alagna, Fiammetta Ruperti, Benedetto Fattorini, Chiara Velasco, Riccardo Mejía, Nilo Zenoni, Sara Bergamini, Carlo VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title | VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title_full | VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title_fullStr | VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title_full_unstemmed | VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title_short | VviAGL11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
title_sort | vviagl11 self-regulates and targets hormone- and secondary metabolism-related genes during seed development |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9433981/ https://www.ncbi.nlm.nih.gov/pubmed/36061618 http://dx.doi.org/10.1093/hr/uhac133 |
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