The Role of Carotenogenic Metabolic Flux in Carotenoid Accumulation and Chromoplast Differentiation: Lessons From the Melon Fruit.

Ari Feder,Galil Tzuri,Zohar Freiman,Ari Schaffer,Ayala Meir,Noam Chayut,Yaakov Tadmor,Yula Shnaider,Amit Gur,Uzi Saar,Amit Gal-On,Joseph Burger,Shachar Ohali,Nurit Katzir,Fabian Baumkoler,Dalia Wolf,Li Li

doi:10.3389/fpls.2019.01250

Abstract

Carotenoids have various roles in plant physiology. Plant carotenoids are synthesized in plastids and are highly abundant in the chromoplasts of ripening fleshy fruits. Considerable research efforts have been devoted to elucidating mechanisms that regulate carotenoid biosynthesis, yet, little is known about the mechanism that triggers storage capacity, mainly through chromoplast differentiation. The Orange gene (OR) product stabilizes phytoene synthase protein (PSY) and triggers chromoplast differentiation. OR underlies carotenoid accumulation in orange cauliflower and melon. The OR’s ‘golden SNP’, found in melon, alters the highly evolutionary conserved Arginine108 to Histidine and controls β-carotene accumulation in melon fruit, in a mechanism yet to be elucidated. We have recently shown that similar carotenogenic metabolic flux is active in non-orange and orange melon fruit. This flux probably leads to carotenoid turnover but known carotenoid turnover products are not detected in non-orange fruit. Arrest of this metabolic flux, using chemical inhibitors or mutations, induces carotenoid accumulation and biogenesis of chromoplasts, regardless of the allelic state of OR. We suggest that the ‘golden SNP’ induces β-carotene accumulation probably by negatively affecting the capacity to synthesize downstream compounds. The accumulation of carotenoids induces chromoplast biogenesis through a metabolite-induced mechanism. Carotenogenic turnover flux can occur in non-photosynthetic tissues, which do not accumulate carotenoids. Arrest of this flux by the ‘golden SNP’ or other flux-arrest mutations is a potential tool for the biofortification of agricultural products with carotenoids.

Highlights

Carotenoids exhibit diverse roles during the plant life cycle, are essential components of the photosynthetic apparatus, color agents, and precursors of hormones and aroma compounds, and are signaling molecules involved in various developmental and environmental signaling pathways (Nisar et al, 2015; Rodriguez-Concepcion et al, 2018a)
The melon’s ORANGE gene (CmOR) resides at the gf locus and its ‘golden’ SNP, replacing the evolutionary conserved Arginine108 (Arg108) with Histidine (His), controls chromoplast differentiation and carotenoid accumulation during melon fruit development (Tzuri et al, 2015). Except for this single aminoacid substitution, not much is known about the initial molecular signaling pathway triggering chromoplast differentiation. In this mini-review, we emphasize the role of the carotenogenic metabolic flux, its association with the ‘golden SNP’ and its arrest during the process of fruit ripening, which we suggest initiates chromoplast differentiation and carotenoid accumulation
This mini-review summarizes studies that indicate the role of the Orange gene (OR) gene in stabilizing the carotenogenic metabolic flux for chromoplast differentiation and carotenoid accumulation

Summary

INTRODUCTION

Carotenoids exhibit diverse roles during the plant life cycle, are essential components of the photosynthetic apparatus, color agents, and precursors of hormones and aroma compounds, and are signaling molecules involved in various developmental and environmental signaling pathways (Nisar et al, 2015; Rodriguez-Concepcion et al, 2018a). The melon’s ORANGE gene (CmOR) resides at the gf locus and its ‘golden’ SNP (single nucleotide polymorphism), replacing the evolutionary conserved Arginine108 (Arg108) with Histidine (His), controls chromoplast differentiation and carotenoid accumulation during melon fruit development (Tzuri et al, 2015). Except for this single aminoacid substitution, not much is known about the initial molecular signaling pathway triggering chromoplast differentiation. In this mini-review, we emphasize the role of the carotenogenic metabolic flux, its association with the ‘golden SNP’ and its arrest during the process of fruit ripening, which we suggest initiates chromoplast differentiation and carotenoid accumulation

REGULATION OF CAROTENOID BIOSYNTHESIS

CONTROLLING THE CAROTENOID METABOLIC FLUX AND ACCUMULATION

Findings

CONCLUSIONS AND FUTURE PERSPECTIVES