Light Regulation of Carotenoid Biosynthesis in the Peel of Mandarin and Sweet Orange Fruits.

Joanna Lado,María J Rodrigo,Paul J.R Cronje,Lorenzo Zacarías,Enriqueta Alós,Matías Manzi,Aurelio Gómez-Cadenas

doi:10.3389/fpls.2019.01288

Abstract

Carotenoids are the pigments responsible for the coloration of the peel and pulp of Citrus fruits. Light is one of the major environmental factors influencing coloration and carotenoid content and composition of fleshy fruits and therefore their commercial and nutritional quality. Agronomical observations indicate that citrus fruits exposed to sunlight develop a brighter peel coloration than shaded fruit inside the tree canopy. In the present study, the effect of light deprivation on carotenoid profile, and in the expression of genes of carotenoid metabolism and their precursors have been analyzed in fruits of Clemenules mandarin (Citrus clementine) and Navelina orange (Citrus sinensis). Fruit shading accelerated peel degreening, chlorophyll degradation, and reduced chloroplastic-type carotenoids. Time-course shading experiments revealed that the stage of fruit ripening appears to be determinant for the effect of darkness in carotenoid biosynthesis. Fruit shading produced a down-regulation of the expression of key carotenoids biosynthetic genes (PSY, PDS, ZDS1, LCY2a, LCY2b, and CHX). However, expression of MEP pathway genes (DXS, HDR1, and GGPPS1) and the carotenoid cleavage dioxygenase, CCD4b1, responsible of the formation of the apocarotenoid β-citraurin, were not substantially affected by dark-grown conditions. The content of abscisic acid (ABA), an end product of the carotenoid pathway, was not affected by the light regime, suggesting that effect of shading on the precursor’s pool is not sufficient to impair ABA synthesis. A moderate increase in total carotenoid and in the expression of biosynthetic genes was observed in mature dark-grown mandarin and orange fruits. Collectively, results suggest that light stimulates carotenoid biosynthesis in the peel of citrus fruits but a light-independent regulation may also operate.

Highlights

Fruit color is a crucial parameter for quality standards, marketability, and consumer acceptance, and of particular relevance for fruit destined to fresh consumption (Lado et al, 2018)
Effect of Light on Citrus Fruit Carotenogenesis pigments accumulated in the peel and pulp of citrus fruit and beside providing coloration they exert different functions related to energy capture and dissipation during photosynthesis, are precursors of the plant hormones abscisic acid (ABA) and strigolactones, among others, and render nutritional and health-related properties by their antioxidant and pro-vitamin A capacity (Rodríguez-Concepción et al, 2018)
All these changes in carotenoids composition occur alongside the induction of the expression of carotenoid biosynthetic genes: first there is an increase in the transcript levels of phytoene synthase (PSY), the first rate limiting and committed step of carotenoid biosynthesis, followed by the stimulation of phytoene desaturase (PDS), ζ-carotene desaturase (ZDS), β-carotene hydroxylase (β-CHX) and the chromoplastspecific lycopene cyclase 2 (Rodrigo et al, 2013a; Ikoma et al, 2016; Wei et al, 2017)

Summary

Introduction

Fruit color is a crucial parameter for quality standards, marketability, and consumer acceptance, and of particular relevance for fruit destined to fresh consumption (Lado et al, 2018). The peel of sweet oranges and mandarins accumulates during ripening citrus-specific C30 apocarotenoids, mainly β-citraurin, derived from the enzymatic cleavage of zeaxanthin and β-cryptoxanthin, and their contents are highly correlated with the orangereddish pigmentation of the peel (Ma et al, 2013; Rodrigo et al, 2013b) All these changes in carotenoids composition occur alongside the induction of the expression of carotenoid biosynthetic genes: first there is an increase in the transcript levels of phytoene synthase (PSY), the first rate limiting and committed step of carotenoid biosynthesis, followed by the stimulation of phytoene desaturase (PDS), ζ-carotene desaturase (ZDS), β-carotene hydroxylase (β-CHX) and the chromoplastspecific lycopene cyclase 2 (βLCY2) (Rodrigo et al, 2013a; Ikoma et al, 2016; Wei et al, 2017). At the end of the MEP pathway, the formation of the key precursor geranyl geranyl pyrophosphate (GGPP), which constitutes a key branching point in the biosynthesis of isoprenoids in plants, is catalyzed by GGPP synthases (GGPPs), a complex family of different isoforms that vary in expression, localization and activity (Beck et al, 2013; Ruiz-Sola et al, 2016)

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