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The peach HECATE3-like gene FLESHY plays a double role during fruit development

Plant Molecular Biology volume 91, pages 97–114 (2016)Cite this article

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Abstract

Tight control of cell/tissue identity is essential for a correct and functional organ patterning, an important component of overall fruit development and eventual maturation and ripening. Despite many investigations regarding the molecular determinants of cell identity in fruits of different species, a useful model able to depict the regulatory networks governing this relevant part of fruit development is still missing. Here we described the peach fruit as a system to link the phenotype of a slow ripening (SR) selection to an altered transcriptional regulation of genes involved in determination of mesocarp cell identity providing insight toward molecular regulation of fruit tissue formation. Morpho-anatomical observations and metabolomics analyses performed during fruit development on the reference cultivar Fantasia, compared to SR, revealed that the mesocarp of SR maintained typical immaturity traits (e.g. small cell size, high amino acid contents and reduced sucrose) throughout development, along with a strong alteration of phenylpropanoid contents, resulting in accumulation of phenylalanine and lignin. These findings suggest that the SR mesocarp is phenotypically similar to a lignifying endocarp. To test this hypothesis, the expression of genes putatively involved in determination of drupe tissues identity was assessed. Among these, the peach HEC3-like gene FLESHY showed a strongly altered expression profile consistent with pit hardening and fruit ripening, generated at a post-transcriptional level. A double function for FLESHY in channelling the phenylpropanoid pathway to either lignin or flavour/aroma is suggested, along with its possible role in triggering auxin-ethylene cross talk at the start of ripening.

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Acknowledgments

This article is dedicated to the memory of our friend and colleague Angelo Ramina. We thank Daniel Jacob for developing and maintaining MeRy-B knowledge base and database. This research was financially supported by Project ex60 % (2013 and 2014) funded by the University of Padova.

Authors’ contributions

Claudio Bonghi conceived the study. Angela Rasori and Fiorenza Ziliotto made the molecular analyses, while Anna Petterle performed the histochemical assessments and microscopic analyses. Annick Moing, Stéphane Bernillon, Catherine Deborde and Mickaël Maucourt supervised and carried out the metabolomic analyses together with Angela Rasori and performed the related data mining. Alessandro Botton carried out the bioinformatic and statistical analyses and prepared the graphics. Serena Varotto gave useful advices and contributed to experiments. Claudio Bonghi and Alessandro Botton interpreted the results and wrote the paper.

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Authors and Affiliations

  1. Department of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padova, viale dell’Università, 16, Agripolis, 35020, Legnaro, Italy

    Alessandro Botton, Angela Rasori, Fiorenza Ziliotto, Anna Petterle, Serena Varotto & Claudio Bonghi

  2. UMR1332 Biologie du Fruit et Pathologie, INRA, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Annick Moing, Stéphane Bernillon & Catherine Deborde

  3. Plateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, MetaboHUB, IBVM, Centre INRA Bordeaux, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Annick Moing, Mickaël Maucourt, Stéphane Bernillon & Catherine Deborde

  4. UMR1332 Biologie du Fruit et Pathologie, University of Bordeaux, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Mickaël Maucourt

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  1. Alessandro Botton
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  2. Angela Rasori
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  3. Fiorenza Ziliotto
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  8. Anna Petterle
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  10. Claudio Bonghi
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Correspondence to Claudio Bonghi.

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Botton, A., Rasori, A., Ziliotto, F. et al. The peach HECATE3-like gene FLESHY plays a double role during fruit development. Plant Mol Biol 91, 97–114 (2016). https://doi.org/10.1007/s11103-016-0445-z

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  • DOI: https://doi.org/10.1007/s11103-016-0445-z

Keywords

  • Fruit patterning
  • Mesocarp identity
  • Metabolomics
  • MicroRNA
  • Phenylpropanoid pathway
  • Post-transcriptional regulation