Abstract

BackgroundMany fruits, including watermelon, are proficient in carotenoid accumulation during ripening. While most genes encoding steps in the carotenoid biosynthetic pathway have been cloned, few transcriptional regulators of these genes have been defined to date. Here we describe the identification of a set of putative carotenoid-related transcription factors resulting from fresh watermelon carotenoid and transcriptome analysis during fruit development and ripening. Our goal is to both clarify the expression profiles of carotenoid pathway genes and to identify candidate regulators and molecular targets for crop improvement.ResultsTotal carotenoids progressively increased during fruit ripening up to ~55 μg g-1 fw in red-ripe fruits. Trans-lycopene was the carotenoid that contributed most to this increase. Many of the genes related to carotenoid metabolism displayed changing expression levels during fruit ripening generating a metabolic flux toward carotenoid synthesis. Constitutive low expression of lycopene cyclase genes resulted in lycopene accumulation. RNA-seq expression profiling of watermelon fruit development yielded a set of transcription factors whose expression was correlated with ripening and carotenoid accumulation. Nineteen putative transcription factor genes from watermelon and homologous to tomato carotenoid-associated genes were identified. Among these, six were differentially expressed in the flesh of both species during fruit development and ripening.ConclusionsTaken together the data suggest that, while the regulation of a common set of metabolic genes likely influences carotenoid synthesis and accumulation in watermelon and tomato fruits during development and ripening, specific and limiting regulators may differ between climacteric and non-climacteric fruits, possibly related to their differential susceptibility to and use of ethylene during ripening.

Highlights

  • Many fruits, including watermelon, are proficient in carotenoid accumulation during ripening

  • Chromoplast synthesized carotenoids accumulate during fruit ripening resulting in dramatic changes in tissue pigmentation

  • The amount of each identified carotenoid varied significantly during fruit ripening (p < 0.001), with the exception of phytofluene 2 and lutein that remained low in all ripening stages

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Summary

Introduction

Many fruits, including watermelon, are proficient in carotenoid accumulation during ripening. We describe the identification of a set of putative carotenoid-related transcription factors resulting from fresh watermelon carotenoid and transcriptome analysis during fruit development and ripening. Many of the genes related to carotenoid metabolism displayed changing expression levels during fruit ripening generating a metabolic flux toward carotenoid synthesis. RNA-seq expression profiling of watermelon fruit development yielded a set of transcription factors whose expression was correlated with ripening and carotenoid accumulation. Chromoplast synthesized carotenoids accumulate during fruit ripening resulting in dramatic changes in tissue pigmentation. Carotenoids play an essential role in attracting insects and herbivores that act as floral pollinators and seed dispersion vehicles, including the consumption of plant organs such as ripe fruits as food by humans. Carotenoids can undergo multiple structural modifications, namely, cyclization, hydroxylation, and epoxidation, yielding the great variety of carotenoids found in nature comprising more than 600 compounds [10]

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