Decoding altitude-activated regulatory mechanisms occurring during apple peel ripening

Evangelos Karagiannis,Eirini Sarrou,Michail Michailidis,Alisdair R. Fernie,Martina Samiotaki,Stefan Martens,Georgia Tanou,George Stamatakis,Athanassios Molassiotis,Federico Scossa

doi:10.1038/s41438-020-00340-x

Abstract

Apple (Malus domestica Borkh) is an important fruit crop cultivated in a broad range of environmental conditions. Apple fruit ripening is a physiological process, whose molecular regulatory network response to different environments is still not sufficiently investigated and this is particularly true of the peel tissue. In this study, the influence of environmental conditions associated with low (20 m) and high (750 m) altitude on peel tissue ripening was assessed by physiological measurements combined with metabolomic and proteomic analyses during apple fruit development and ripening. Although apple fruit ripening was itself not affected by the different environmental conditions, several key color parameters, such as redness and color index, were notably induced by high altitude. Consistent with this observation, increased levels of anthocyanin and other phenolic compounds, including cyanidin-3-O-galactoside, quercetin-3-O-rhamnoside, quercetin-3-O-rutinoside, and chlorogenic acid were identified in the peel of apple grown at high altitude. Moreover, the high-altitude environment was characterized by elevated abundance of various carbohydrates (e.g., arabinose, xylose, and sucrose) but decreased levels of glutamic acid and several related proteins, such as glycine hydroxymethyltransferase and glutamate–glyoxylate aminotransferase. Other processes affected by high altitude were the TCA cycle, the synthesis of oxidative/defense enzymes, and the accumulation of photosynthetic proteins. From the obtained data we were able to construct a metabolite-protein network depicting the impact of altitude on peel ripening. The combined analyses presented here provide new insights into physiological processes linking apple peel ripening with the prevailing environmental conditions.

Highlights

Apple (Malus x domestica Borkh), with its wide diversity of climatic adaptation, has become the most widely planted tree fruit of the temperate zone and one of the most widely cultivated in the world[1]
The phenotype of apple fruit across development (Fig. 1a; the same fruits were photographed across seven different timepoints throughout development), and especially during the commercial harvest stage (Fig. 2) indicates that altitude and its associated climatic factors have a strong impact on apple peel color
Data showed that apple fruits sampled at various developmental stages from the two environmental conditions displayed a similar pattern of growth and ripening (Fig. 1b)—with these data suggesting, that the ripening status of the fruits was unaffected by altitude

Summary

Introduction

Apple (Malus x domestica Borkh), with its wide diversity of climatic adaptation, has become the most widely planted tree fruit of the temperate zone and one of the most widely cultivated in the world[1]. The ability of apple genotypes to produce different phenotypes as a function of environmental cues (so-called phenotypic plasticity) is considered one of the main processes by which this fruit species can face and adapt to the spatio-temporal variation of environmental factors[1]. Three distinct parts can be distinguished in apple fruit: the outer pericarp (peel), the mesocarp (flesh), and the core. Many apple fruit quality characteristics appear to be related to only one of the two pericarp tissues. Tasterelated traits such as the sugar and acid content mostly depend on the flesh[5], while the apple peel is the main site in the synthesis of many compounds of interest

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Conclusion