Ethylene is involved in strawberry fruit ripening in an organ-specific manner.

Catharina Merchante,María T Ariza,Irene Aragüez,Sonia Osorio,Marcos P Civello,Gustavo A Martínez,Alisdair R Fernie,Victoriano Valpuesta,Nieves Medina-Escobar,Natalia Villarreal,Miguel A Botella,José G Vallarino

doi:10.1093/jxb/ert257

Abstract

The fruit of the strawberry Fragaria×ananassa has traditionally been classified as non-climacteric because its ripening process is not governed by ethylene. However, previous studies have reported the timely endogenous production of minor amounts of ethylene by the fruit as well as the differential expression of genes of the ethylene synthesis, reception, and signalling pathways during fruit development. Mining of the Fragaria vesca genome allowed for the identification of the two main ethylene biosynthetic genes, 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase. Their expression pattern during fruit ripening was found to be stage and organ (achene or receptacle) specific. Strawberry plants with altered sensitivity to ethylene could be employed to unravel the role of ethylene in the ripening process of the strawberry fruit. To this end, independent lines of transgenic strawberry plants were generated that overexpress the Arabidopsis etr1-1 mutant ethylene receptor, which is a dominant negative allele, causing diminished sensitivity to ethylene. Genes involved in ethylene perception as well as in its related downstream processes, such as flavonoid biosynthesis, pectin metabolism, and volatile biosynthesis, were differently expressed in two transgenic tissues, the achene and the receptacle. The different transcriptional responsiveness of the achene and the receptacle to ethylene was also revealed by the metabolic profiling of the primary metabolites in these two organs. The free amino acid content was higher in the transgenic lines compared with the control in the mature achene, while glucose and fructose, and citric and malic acids were at lower levels. In the receptacle, the most conspicuous change in the transgenic lines was the depletion of the tricarboxylic acid cycle intermediates at the white stage of development, most probably as a consequence of diminished respiration. The results are discussed in the context of the importance of ethylene during strawberry fruit ripening.

Highlights

The strawberry (Fragaria×ananassa, Duch.) is an important diseases, obesity, cancer, and ageing are currently under invescrop worldwide, and the potential benefits of its consumption tigation (Seeram, 2008; Giampieri et al, 2012)
The strawberry fruit is composed of two organs that are very different in terms of origin, physiological role, and prevailing metabolic networks; these organs are the achenes, which are the true fruits, and the receptacles, which are derived from the flower receptacles (Fait et al, 2008; Csukasi et al, 2011)
A third consideration is the inherent difficulty in measuring the independent endogenous production of ethylene in the achenes and receptacle, which is exacerbated by the low level of internal production of this hormone by the strawberry fruit (Iannetta et al, 2006)

Summary

Introduction

The strawberry (Fragaria×ananassa, Duch.) is an important diseases, obesity, cancer, and ageing are currently under invescrop worldwide, and the potential benefits of its consumption tigation (Seeram, 2008; Giampieri et al, 2012). The main reason for this relatively poor understanding in comparison with other fruits is that what is commonly referred to as the strawberry fruit is a false fruit that is composed of achenes (true fruits that evolve from ovaries), and the engrossed flower receptacle (fleshy part), and both organs are connected through vascular bundles (Perkins-Veazie, 1995) These two organs, the achene and the receptacle, highly interconnected throughout their developmental programmes, at early developmental stages, are very different in terms of cell ontogeny and function, as has been revealed by both gene expression studies (Aharoni and O’Connell, 2002; Csukasi et al, 2012) and metabolic profiling (Fait et al, 2008). Studies on the whole fruit, without dissection into its two composite parts, mask tissue-specific differences, the knowledge of which is required to draw reliable conclusions

Methods

Results

Conclusion