Abstract

Carotenoids have essential roles in light-harvesting processes and protecting the photosynthetic machinery from photo-oxidative damage. Phytoene synthase (PSY) and Orange (Or) are key plant proteins for carotenoid biosynthesis and accumulation. We previously isolated the sweetpotato (Ipomoea batatas) Or gene (IbOr), which is involved in carotenoid accumulation and salt stress tolerance. The molecular mechanism underlying IbOr regulation of carotenoid accumulation was unknown. Here, we show that IbOr has an essential role in regulating IbPSY stability via its holdase chaperone activity both in vitro and in vivo. This protection results in carotenoid accumulation and abiotic stress tolerance. IbOr transcript levels increase in sweetpotato stem, root, and calli after exposure to heat stress. IbOr is localized in the nucleus and chloroplasts, but interacts with IbPSY only in chloroplasts. After exposure to heat stress, IbOr predominantly localizes in chloroplasts. IbOr overexpression in transgenic sweetpotato and Arabidopsis conferred enhanced tolerance to heat and oxidative stress. These results indicate that IbOr holdase chaperone activity protects IbPSY stability, which leads to carotenoid accumulation, and confers enhanced heat and oxidative stress tolerance in plants. This study provides evidence that IbOr functions as a molecular chaperone, and suggests a novel mechanism regulating carotenoid accumulation and stress tolerance in plants.

Highlights

  • Carotenoids are essential in plants for light harvesting, photoprotection, and abscisic acid (ABA) biosynthesis[1]

  • To identify a possible functional role for IbOr under heat stress conditions, IbOr expression was analyzed by quantitative RT-PCR in heat-treated sweetpotato tissues (Supplementary Fig. S1)

  • IbOr is a key protein involved in carotenoid accumulation and environmental stress tolerance in sweetpotato[7,33], but the molecular mechanism of IbOr function was previously unknown

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Summary

Introduction

Carotenoids are essential in plants for light harvesting, photoprotection, and abscisic acid (ABA) biosynthesis[1]. Due to the nutritional importance of carotenoids, metabolic engineering of carotenoid biosynthesis has been performed to enhance carotenoid contents in staple crops[1] We observed that transgenic sweetpotato calli overexpressing IbOr had higher carotenoid levels, increased antioxidant activity, and enhanced salt stress tolerance[7]. It was unclear how IbOr regulated carotenoid accumulation, plant DnaJ proteins are reported as heat-shock proteins involved in abiotic stress tolerance and holdase chaperone function[30]. We report the holdase chaperone function of IbOr, which regulates IbPSY stability, enhances carotenoid accumulation, and confers heat stress tolerance in sweetpotato

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