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Articles

Transcriptomic analysis reveals genes involved in photoperiod-mediated carotenoid accumulation mechanisms in the fruit endocarp of ‘Xishuangbanna’ cucumber

Article number
1411_24
Pages
231 – 254
Language
English
Abstract
The accumulation of carotenoids is a key nutritional quality trait in many horticultural crops.
Although the structural genes that encode the biosynthetic enzymes are well characterized, little is known regarding photoperiod-mediated carotenoid accumulation in the fruit of some horticultural crops.
An orange-fleshed ‘Xishuangbanna’ (XIS) is a photoperiod-sensitive cucumber and accumulates abundant beta-carotene at the mature fruit stage.
However, the underlying molecular regulatory mechanism of the photoperiodic effect on carotenoid accumulation in the endocarp of XIS cucumber fruit remains unexplored.
We performed physiological and RNA-seq analysis using two cucumber genotypes SWCC8 (orange-fleshed) and CC3 (white-fleshed), established under two photoperiod conditions (8L/16D vs. 12L/12D) at four fruit developmental stages.
Results show that day-neutral treatments significantly increased fruit beta-carotene content by 42.1% compared to SD in XIS at 40 DAP with no significant changes in CC3. Sugar levels increased under day-neutral and decreased in short day durations.
GO and KEGG analysis revealed that the predominantly expressed genes were mainly associated with carbohydrates, circadian rhythm, carotenoid biosynthesis, plant hormone signaling, and photosynthesis.
Day-neutral condition elevated expression of key carotenoid biosynthesis genes PSY1, PDS, ZDS1, LYCb, and CHY1 during later stages between 30 to 40 days of fruit development, which was consistent with beta-carotene accumulation in XIS. Compared to XIS, CC3 showed expression of DEGs related to carotenoid cleavage and oxidative stresses.
This could explain reduced beta-carotene in CC3 and genotypic responses to photoperiod.
Further analysis of WGCNA revealed that carbohydrate-related genes (pentose-phosphatase synthase, beta-glucosidase, and trehalose-6-phosphatase) and photoperiod signaling genes (LHY, APRR7/5, FKF1, PIF3, COP1, GIGANTEA, and CK2) co-express with the carotenoid biosynthetic genes, thus suggesting a cross-talk between carbohydrates and light related genes to induce beta-carotene accumulation.
Therefore, a mechanism of photoperiod-mediated carotenoid accumulation is envisaged involving synergistic interaction between light and carbohydrate-related genes.
The results highlighted herein provide a framework for future gene functional analysis and molecular breeding of carotenoid accumulation in plants.

Publication
Authors
H.O. Obel, Chunyan Cheng, Zhen Tian, Ji Li, Yuhui Wang, Qunfeng Lou, Xiaqing Yu, J. Otieno Ogweno, Jinfeng Chen
Keywords
photoperiod, β-carotene, ‘Xishuangbanna’ cucumber, transcriptomics, WGCNA, light signaling, carbohydrate metabolism
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