Comparative transcriptome analyses shed light on carotenoid production and plastid development in melon fruit

Noam Chayut,Adi Faigenboim,Xuesong Zhou,Li Li,Hui Yuan,Tianhu Sun,Zhangjun Fei,Yi Zheng,Yaakov Tadmor,Yuval Saar,Michael Mazourek,Joseph Burger,Anna Hermanns,Maixia Hui,Elad Oren

doi:10.1038/s41438-021-00547-6

Abstract

Carotenoids, such as β-carotene, accumulate in chromoplasts of various fleshy fruits, awarding them with colors, aromas, and nutrients. The Orange (CmOr) gene controls β-carotene accumulation in melon fruit by posttranslationally enhancing carotenogenesis and repressing β-carotene turnover in chromoplasts. Carotenoid isomerase (CRTISO) isomerizes yellow prolycopene into red lycopene, a prerequisite for further metabolism into β-carotene. We comparatively analyzed the developing fruit transcriptomes of orange-colored melon and its two isogenic EMS-induced mutants, low-β (Cmor) and yofi (Cmcrtiso). The Cmor mutation in low-β caused a major transcriptomic change in the mature fruit. In contrast, the Cmcrtiso mutation in yofi significantly changed the transcriptome only in early fruit developmental stages. These findings indicate that melon fruit transcriptome is primarily altered by changes in carotenoid metabolic flux and plastid conversion, but minimally by carotenoid composition in the ripe fruit. Clustering of the differentially expressed genes into functional groups revealed an association between fruit carotenoid metabolic flux with the maintenance of the photosynthetic apparatus in fruit chloroplasts. Moreover, large numbers of thylakoid localized photosynthetic genes were differentially expressed in low-β. CmOR family proteins were found to physically interact with light-harvesting chlorophyll a–b binding proteins, suggesting a new role of CmOR for chloroplast maintenance in melon fruit. This study brings more insights into the cellular and metabolic processes associated with fruit carotenoid accumulation in melon fruit and reveals a new maintenance mechanism of the photosynthetic apparatus for plastid development.

Highlights

Carotenoids fulfill diverse biological functions in plants[1,2,3]
Based on transcriptome analysis, we discovered a new role of CmOR in regulating light-harvesting chlorophyll a–b binding (LHCB) proteins to maintain photosynthetic apparatus and plastid development
The color was notably different at 30 days after anthesis (DAA) with the low-β flesh remaining green and the wild type (WT) fruit turning orange (Fig. 1b)

Summary

Introduction

Carotenoids fulfill diverse biological functions in plants[1,2,3]. They are essential for plants due to their roles in photosynthesis and photoprotection. Carotenoid isomerase (CRTISO) converts the yellow colored prolycopene into the red colored all-trans lycopene[13,14] (Fig. 1a). All-trans lycopene is the substrate for lycopene β- and ε-ring cyclases to yield β-carotene and αcarotene in the subsequent two branches of the metabolic pathway. Alpha-carotene is converted into lutein, the most abundant photosynthetic carotenoid, while β-carotene is hydroxylated to form various other xanthophylls[15]. Carotenes and xanthophylls can be further cleaved by carotenoid cleavage dioxygenase enzymes to produce various apocarotenoids including volatiles and scent molecules or phytohormones ABA and strigolactones[15]

Methods

Results

Conclusion