Transcriptome regulation of carotenoids in five flesh-colored watermelons (Citrullus lanatus)

Abstract

Background Fruit flesh color in watermelon (Citrullus lanatus) is a great index for evaluating the appearance quality and a key contributor influencing consumers’ preferences. But the molecular mechanism of this intricate trait remains largely unknown. Here, the carotenoids and transcriptome dynamics during the fruit development of cultivated watermelon with five different flesh colors were analyzed. Results A total of 13 carotenoids and 16,781 differentially expressed genes (DEGs), including 1295 transcription factors (TFs), were detected in five watermelon genotypes during the fruit development. The comprehensive accumulation patterns of carotenoids were closely related to flesh color. A number of potential structural genes and transcription factors were found to be associated with the carotenoid biosynthesis pathway using comparative transcriptome analysis. The differentially expressed genes were divided into six subclusters and distributed in different GO terms and metabolic pathways. Furthermore, we performed weighted gene co-expression network analysis and predicted the hub genes in six main modules determining carotenoid contents. Cla018406 (a chaperone protein dnaJ-like protein) may be a candidate gene for β-carotene accumulation and highly expressed in orange flesh-colored fruit. Cla007686 (a zinc finger CCCH domain-containing protein) was highly expressed in the red flesh-colored watermelon, maybe a key regulator of lycopene accumulation. Cla003760 (membrane protein) and Cla021635 (photosystem I reaction center subunit II) were predicted to be the hub genes and may play an essential role in yellow flesh formation. Conclusions The composition and contents of carotenoids in five watermelon genotypes vary greatly. A series of candidate genes were revealed through combined analysis of metabolites and transcriptome. These results provide an important data resource for dissecting candidate genes and molecular basis governing flesh color formation in watermelon fruit.

Genetic mapping of a single nuclear locus determines the white flesh color in watermelon (Citrullus lanatus L.)

“…In this study, the flesh color inheritance analysis using the F 2 and F 3 segregation populations produced from the cross between the canary yellow (HSH-F) and white (Sanbai) flesh lines obtained a 3:1 segregation ratio of canary yellow/white flesh ( Table 1 ). Consistent with previous studies, the canary yellow flesh contained abundant xanthophyll, whereas white flesh watermelon accumulated trace carotenoids ( Figure 1B and Supplementary Table S2 ) ( Bang et al., 2010 ; Zhao et al., 2013 ; Lv et al., 2015 ; Diao et al., 2021 ; Yuan et al., 2021 ). To examine whether the white flesh in Sanbai resulted from the malfunction of the canary yellow flesh locus, we crossed an orange flesh line (CG149), which accumulated massive carotene but lacked xanthophyll ( Figure 1B and Supplementary Table S2 ), with the canary yellow (HSH-F) and white flesh (Sanbai) lines.…”

“…A high transcript abundance of LCYB / LCYE was associated with the high accumulation of carotene in fruits ( Lu et al., 2006 ; Ampomah-Dwamena et al., 2009 ; Liu et al., 2015 ). In watermelon, the production of violaxanthin and lutein in yellow flesh was positively correlated with the expression levels of CHYB and ZEP ( Lv et al., 2015 ; Yuan et al., 2021 ). In addition, the modulation of carotenogenic enzymes and the regulation of chromoplast biogenesis, development, and differentiation have been demonstrated to strongly affect carotenoid accumulation ( Yuan et al., 2015 ; Sun et al., 2018 ; Feder et al., 2019 ).…”

Integrated analysis of carotenoid metabolites and transcriptome identifies key genes controlling carotenoid compositions and content in sweetpotato tuberous roots (Ipomoea batatas L.)

“…KEGG enrichment analysis and NR annotation showed that, there are 27 structural genes participated in carotenoid metabolic pathway among the four combinations (LY vs. W, Y vs. W, O vs. W, OR vs. W), and the sweetpotato carotenoid metabolic pathway were mapped ( Figure 3 ). The pathway was constructed based on KEGG and references ( Suematsu et al., 2020 ; Xu et al., 2021 ; Yuan et al., 2021 ; KEGG, 2022 ). Of which 10 DEGs namely Or (1), CRTISO (1), CYP97B2 (1), CHYB (1), ZEP (2), NSY (1) and DWARF27 (3) were playing major role in carotenoid biosynthesis pathway and 17 DEGs namely CCD1 (8), CCD4 (1), CCD7 (1), NCED (4) and CYP707A (3) were related to carotenoid degradation pathway.…”

“…In recent years, several transcription factors that regulate and control the carotenoid metabolic pathway have been identified in several crop species ( Ampomah-Dwamena et al., 2019 ; Yuan et al., 2021 ). In present study, we performed WGCNA to identify transcription factors that coordinately regulate the biosynthesis and accumulation of carotenoids.…”

Genetic Analysis of Fruit Quality Traits in Sweet Watermelon (Citrullus lanatus var. lanatus): A Review

“…The genes designated as Cla018767 , Cla018768 , Cla018769, Cla018770, and Cla018771 were linked to controlling red-flesh color development in watermelon for being involved in lycopene biosynthesis ( Li et al, 2020 ). The genes Cla003760 and Cla021635 conferred yellow flesh color development ( Yuan et al, 2021 ). Carotenoid metabolic pathway genes namely: ClPSY1 ( Cla009122 ), ClZDS ( Cla003751 ), ClNCED-7 ( Cla005404 ), ClCRTISO ( Cla017593 ), ClCHYB ( Cla006149 ), ClLCYB ( Cla005011 ), ClPDS ( Cla010898 ), ClNCED-1 ( Cla009779 ), and ClCHXE ( Cla011420 ) are involved in the development of white and pale-yellow fruit flesh color of watermelon (Wang et al, 2021).…”