Manipulation of β-carotene levels in tomato fruits results in increased ABA content and extended shelf life

Gianfranco Diretto, Sarah Frusciante, Claudia Fabbri, Nicolas Schauer, Lucas Busta, Zhonghua Wang, Antonio J. Matas, Alessia Fiore, Jocelyn K.C. Rose, Alisdair R. Fernie, Reinhard Jetter, Benedetta Mattei, Jim Giovannoni, Giovanni Giuliano

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

Abstract

Tomato fruit ripening is controlled by the hormone ethylene and by a group of transcription factors, acting upstream of ethylene. During ripening, the linear carotene lycopene accumulates at the expense of cyclic carotenoids. Fruit-specific overexpression of LYCOPENE β-CYCLASE (LCYb) resulted in increased β-carotene (provitamin A) content. Unexpectedly, LCYb-overexpressing fruits also exhibited a diverse array of ripening phenotypes, including delayed softening and extended shelf life. These phenotypes were accompanied, at the biochemical level, by an increase in abscisic acid (ABA) content, decreased ethylene production, increased density of cell wall material containing linear pectins with a low degree of methylation, and a thicker cuticle with a higher content of cutin monomers and triterpenoids. The levels of several primary metabolites and phenylpropanoid compounds were also altered in the transgenic fruits, which could be attributed to delayed fruit ripening and/or to ABA. Network correlation analysis and pharmacological experiments with the ABA biosynthesis inhibitor, abamine, indicated that altered ABA levels were a direct effect of the increased β-carotene content and were in turn responsible for the extended shelf life phenotype. Thus, manipulation of β-carotene levels results in an improvement not only of the nutritional value of tomato fruits, but also of their shelf life.

Original languageEnglish (US)
Pages (from-to)1185-1199
Number of pages15
JournalPlant Biotechnology Journal
Volume18
Issue number5
DOIs
StatePublished - May 1 2020
Externally publishedYes

Bibliographical note

Funding Information:
The work was supported by the European Commission (Projects DISCO, grant agreement: 613513; and Traditom, grant agreement: 634561) to GG, a Special Research Opportunity Grant from the Natural Sciences and Engineering Research Council of Canada, the Canada Chairs Program and the Canada Foundation for Innovation to RJ and the United States Department of Agriculture?Agricultural Research Service and the US National Science Foundation (grant IOS-1539831) to JG, and benefited from the networking activities within the European Cooperation in Science and Technology Action FA1106 (Qualityfruit) and CA15136 (EUROCAROTEN). We thank Florian Wurst and Peter Beyer, Freiburg University (Germany), for help in ABA measurements; Asaph Aharoni and Yoseph Hirschberg for providing annotated tomato cuticle and ABA-relative gene lists, respectively; and Christian Chervin, Julien Pirrello and Mondher Boutzayen for help in fruit abamine treatments. The authors declare to have no conflict of interest.

Funding Information:
The work was supported by the European Commission (Projects DISCO, grant agreement: 613513; and Traditom, grant agreement: 634561) to GG, a Special Research Opportunity Grant from the Natural Sciences and Engineering Research Council of Canada, the Canada Chairs Program and the Canada Foundation for Innovation to RJ and the United States Department of Agriculture—Agricultural Research Service and the US National Science Foundation (grant IOS‐1539831) to JG, and benefited from the networking activities within the European Cooperation in Science and Technology Action FA1106 (Qualityfruit) and CA15136 (EUROCAROTEN). We thank Florian Wurst and Peter Beyer, Freiburg University (Germany), for help in ABA measurements; Asaph Aharoni and Yoseph Hirschberg for providing annotated tomato cuticle and ABA‐relative gene lists, respectively; and Christian Chervin, Julien Pirrello and Mondher Boutzayen for help in fruit abamine treatments. The authors declare to have no conflict of interest.

Publisher Copyright:
© 2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.

Keywords

  • ABA
  • ripening
  • tomato
  • β-carotene

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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