SEPALLATA1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes

Robert J Schaffer,Hilary S Ireland,John J Ross,Toby J Ling,Karine M David

doi:10.1093/aobpla/pls047

Robert J Schaffer, Hilary S Ireland + Show 3 more

Open Access

https://doi.org/10.1093/aobpla/pls047

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Abstract

Fruit ripening is an important developmental trait in fleshy fruits, making the fruit palatable for seed dispersers. In some fruit species, there is a strong association between auxin concentrations and fruit ripening. We investigated the relationship between auxin concentrations and the onset of ethylene-related ripening in Malus × domestica (apples) at both the hormone and transcriptome levels. Transgenic apples suppressed for the SEPALLATA1/2 (SEP1/2) class of gene (MADS8/9) that showed severely reduced ripening were compared with untransformed control apples. In each apple type, free indole-3-acetic acid (IAA) concentrations were measured during early ripening. The changes observed in auxin were assessed in light of global changes in gene expression. It was found that mature MADS8/9-suppressed apples had a higher concentration of free IAA. This was associated with increased expression of the auxin biosynthetic genes in the indole-3-acetamide pathway. Additionally, in the MADS8/9-suppressed apples, there was less expression of the GH3 auxin-conjugating enzymes. A number of genes involved in the auxin-regulated transcription (AUX/IAA and ARF classes of genes) were also observed to change in expression, suggesting a mechanism for signal transduction at the start of ripening. The delay in ripening observed in MADS8/9-suppressed apples may be partly due to high auxin concentrations. We propose that, to achieve low auxin associated with fruit maturation, the auxin homeostasis is controlled in a two-pronged manner: (i) by the reduction in biosynthesis and (ii) by an increase in auxin conjugation. This is associated with the change in expression of auxin-signalling genes and the up-regulation of ripening-related genes.

Highlights

Fruit ripening is associated with dramatic changes in fruit physiology
Transgenic apples suppressed for the SEPALLATA1/2 (SEP1/2) class of gene (MADS8/9) that showed severely reduced ripening were compared with untransformed control apples
To achieve low auxin associated with fruit maturation, the auxin homeostasis is controlled in a two-pronged manner: (i) by the reduction in biosynthesis and (ii) by an increase in auxin conjugation

Summary

Introduction

In Malus × domestica (apple), ripening is associated with a respiratory climacteric and an increase in ethylene. This coincides with a conversion of starches to sugars, a reduction in fruit acids, a change in background skin colour from green to yellow, a softening of the flesh and an increase in flavour and aroma volatiles. Using transgenic apple lines suppressed for a gene involved in ethylene biosynthesis, ACC OXIDASE 1 (ACO1), a model was proposed whereby increasing the concentrations of ripening-associated ethylene (type II) controls a sequential progression of events starting with starch/acid changes, followed by skin colour changes and culminating in flesh softening and aroma volatile production (Johnston et al 2009) (Fig. 1).

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