The cucumber (Cucumis sativus) fruit is covered with bloom trichomes and warts (composed of spines and tubercules), which have an important impact on the commercial value of the crop. However, little is known about the regulatory mechanism underlying their formation. Here, we reported that the cucumber WD-repeat homolog CsTTG1, which is localized in the nucleus and cytomembrane, plays an important role in the formation of cucumber fruit bloom trichomes and warts. Functional characterization of CsTTG1 revealed that it is mainly expressed in the epidermis of cucumber ovary and that its overexpression in cucumber alters the density of fruit bloom trichomes and spines, thereby promoting the warty fruit trait. Conversely, silencing CsTTG1 expression inhibits the initiation of fruit spines. Molecular and genetic analyses showed that CsTTG1 acts in parallel to Mict/CsGL1, a key trichome formation factor, to regulate the initiation of fruit trichomes, including fruit bloom trichomes and spines, and that the further differentiation of fruit spines and formation of tubercules regulated by CsTTG1 is dependent on Mict. Using yeast two-hybrid assay and bimolecular fluorescence complementation assay, we determined that CsTTG1 directly interacts with Mict. Collectively, our results indicate that CsTTG1 is an important component of the molecular network that regulates fruit bloom trichome and wart formation in cucumber.
Cucumber fruit trichomes could be classified into eight types; all of them are multicellular with complex and different developmental processes as compared with unicellular trichomes in other plants. The fruit trichomes or fruit spines of cucumber, Cucumis sativus L., are highly specialized structures originating from epidermal cells with diverse morphology, which grow perpendicular to the fruit surface. To understand the underlying molecular mechanisms of fruit trichome development, in this study, we conducted morphological characterization and classification of cucumber fruit trichomes and their developmental processes. We examined the fruit trichomes among 200 cucumber varieties, which could be classified into eight morphologically distinct types (I-VIII). Investigation of the organogenesis of the eight types of trichomes revealed two main developmental patterns. The development of glandular trichomes had multiple stages including initiation and expansion of the trichome precursor cell protuberating out of the epidermal surface, followed by periclinal bipartition to two cells (top and bottom) which later formed the head region and the stalk, respectively, through subsequent cell divisions. The non-glandular trichome development started with the expansion of the precursor cell perpendicularly to the epidermal plane followed by cell periclinal division to form a stalk comprising of some rectangle cells and a pointed apex cell. The base cell then started anticlinal bipartition to two cells, which then underwent many cell divisions to form a multicellular spherical structure. In addition, phytohormones as environmental cues were closely related to trichome development. We found that GA and BAP were capable of increasing trichome number per fruit with distinct effects under different concentrations.
The cucumber (Cucumis sativus L.) is an important vegetable crop worldwide, and fruit trichomes or spines are an important trait for external fruit quality. The mechanisms underlying spine formation are not well understood, but the plant-specific NAC family of transcription factors may play important roles in fruit spine initiation and development. In this study, we conducted a genome-wide survey and identified 91 NAC gene homologs in the cucumber genome. Clustering analysis classified these genes into six subfamilies; each contained a varying number of NAC family members with a similar intron–exon structure and conserved motifs. Quantitative real-time PCR analysis revealed tissue-specific expression patterns of these genes, including 10 and 12 that exhibited preferential expression in the stem and fruit, respectively. Thirteen of the 91 NAC genes showed higher expression in the wild-type plant than in its near-isogenic trichome mutant, suggesting their important roles in fruit spine development. Exogenous application of four plant hormones promoted spine formation and increased spine density on the cucumber fruits; several NAC genes showed differential expression over time in response to phytohormone treatments on cucumber fruit, implying their essential roles in fruit-trichome development. Among the NAC genes identified, 12 were found to be targets of 13 known cucumber micro-RNAs. Collectively, these findings provide a useful resource for further analysis of the interactions between NAC genes and genes underlying trichome organogenesis and development during fruit spine development in cucumber.
The fruit epidermal features such as the size of tubercules are important fruit quality traits for cucumber production. But the mechanisms underlying tubercule formation remain elusive. Here, tubercule size locus CsTS1 was identified by map-based cloning and was found to encode an oleosin protein. Allelic variation was identified in the promoter region of CsTS1, resulting in low expression of CsTS1 in all 22 different small-warty or nonwarty cucumber lines. High CsTS1 expression levels were closely correlated with increased fruit tubercule size among 44 different cucumber lines. Transgenic complementation and RNAi-mediated gene silencing of CsTS1 in transgenic cucumber plants demonstrated that CsTS1 positively regulates the development of tubercules. CsTS1 is highly expressed in the peel at fruit tubercule forming and enlargement stage. Auxin content and expression of three auxin signalling pathway genes were altered in the 35S:CsTS1 and CsTS1-RNAi fruit tubercules, a result that was supported by comparing the cell size of the control and transgenic fruit tubercules. CsTu, a C H zinc finger domain transcription factor that regulates tubercule initiation, binds directly to the CsTS1 promoter and promotes its expression. Taken together, our results reveal a novel mechanism in which the CsTu-TS1 complex promotes fruit tubercule formation in cucumber.
SummaryGibberellins are phytohormones with many roles, including the regulation of fruit development. However, little is known about the relationship between GA perception and fleshy fruit ontogeny, and particularly locule formation.We characterized the expression of cucumber (Cucumis sativus) GA receptor gene (CsGID1a) using quantitative real-time PCR, in situ hybridization and a promoter::bglucuronidase (GUS) assay. CsGID1a-RNAi cucumber fruits were observed by dissecting microscope, scanning electron microscopy and transmission electron microscopy. Finally, genome-wide gene expression in young fruits from a control and the RNAi line was compared using a digital gene expression (DGE) analysis approach.The expression pattern of CsGID1a was found to be closely correlated with fruit locule formation, and silencing CsGID1a in cucumber resulted in fruits with abnormal carpels and locules. Overexpression of CsGID1a in the Arabidopsis thaliana double mutant (gid1a gid1c) resulted in 'cucumber locule-like' fruits. The DGE analysis suggested that expression of genes related to auxin synthesis and transport, as well as the cell cycle, was altered in CsGID1a-RNAi fruits, a result that was supported by comparing the auxin content and cellular structures of the control and transgenic fruits.This study demonstrates a previously uncharacterized GA signaling pathway that is essential for cucumber fruit locule formation.
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