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Integrative Analysis of Transcriptomic and Methylomic Data in Photoperiod-Dependent Regulation of Cucumber Sex Expression.

ABSTRACT: The cucumber (Cucumis sativus) is characterized by its diversity and seasonal plasticity in sexual type. A long day length condition significantly decreased the cucumber female flower ratio by 17.7-52.9%, and the effect of photoperiod treatment is more significant under low temperature than under high temperature. Transcriptome analysis indicates that the photoperiod treatment preferentially significantly influenced flower development processes, particularly MADS-box genes in shoot apices. The long-day treatment resulted in predominantly transposable element (TE)- and gene-associated CHH-types of DNA methylation changes. Nevertheless, there was significant enrichment of CG- and CHG-types of DNA methylation changes nearing transcription start sites (TSSs)/transcription end sites (TESs) and gene bodies, respectively. Predominantly negative association between differentially methylated regions (DMRs) and differentially expressed genes (DEGs) were observed which implied epiregulation of DEGs. Two MADS-box genes that were significantly downregulated by long photoperiod showed significant hypermethylation in promoter regions that is essentially TE-rich. This study indicates MADS-box genes which are partially regulated by promoter methylation state may mediate photoperiod-dependent regulation of cucumber sex expression.

SUBMITTER: Lai YS

PROVIDER: S-EPMC6288824 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Integrative Analysis of Transcriptomic and Methylomic Data in Photoperiod-Dependent Regulation of Cucumber Sex Expression.

Lai Yun-Song YS Zhang Wei W Zhang Xiaohui X Shen Di D Wang Haiping H Qiu Yang Y Song Jiangping J Li Xixiang X

G3 (Bethesda, Md.) 20181210 12

The cucumber (<i>Cucumis sativus</i>) is characterized by its diversity and seasonal plasticity in sexual type. A long day length condition significantly decreased the cucumber female flower ratio by 17.7-52.9%, and the effect of photoperiod treatment is more significant under low temperature than under high temperature. Transcriptome analysis indicates that the photoperiod treatment preferentially significantly influenced flower development processes, particularly MADS-box genes in shoot apices ...[more]

PMID: 30377155

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Project description:BACKGROUND:Cucumbers (Cucumis sativus) are known for their plasticity in sex expression. DNA methylation status determines gene activity but is susceptible to environmental condition changes. Thus, DNA methylation-based epigenetic regulation may at least partially account for the instability of cucumber sex expression. Do temperature and photoperiod that are the two most important environmental factors have equal effect on cucumber sex expression by similar epigenetic regulation mechanism? To answer this question, we did a two-factor experiment of temperature and photoperiod and generated methylome and transcriptome data from cucumber shoot apices. RESULTS:The seasonal change in the femaleness of a cucumber core germplasm collection was investigated over five consecutive years. As a result, 71.3% of the 359 cucumber accessions significantly decreased their femaleness in early autumn when compared with spring. High temperature and long-day photoperiod treatments, which mimic early autumn conditions, are both unfavorable for female flower formation, and temperature is the predominant factor. High temperatures and long-day treatments both predominantly resulted in hypermethylation compared to demethylation, and temperature effect was decisive. The targeted cytosines shared in high-temperature and long-day photoperiod treatment showed the same change in DNA methylation level. Moreover, differentially expressed TEs (DETs) and the predicted epiregulation sites were clustered across chromosomes, and importantly, these sites were reproducible among different treatments. Essentially, the photoperiod treatment preferentially and significantly influenced flower development processes, while temperature treatment produced stronger responses from phytohormone-pathway-related genes. Cucumber AGAMOUS was likely epicontrolled exclusively by photoperiod while CAULIFLOWER A and CsACO3 were likely epicontrolled by both photoperiod and temperature. CONCLUSIONS:Seasonal change of sex expression is a germplasm-wide phenomenon in cucumbers. High temperature and long-day photoperiod might have the same effect on the methylome via the same mechanism of gene-TE interaction but resulted in different epicontrol sites that account for different mechanisms between temperature- and photoperiod-dependent sex expression changes.

Project description:BackgroundNumerous studies have established a link between maternal diet and the physiological and metabolic phenotypes of their offspring. In previous studies in sheep, we demonstrated that different maternal diets altered the transcriptome of fetal tissues. However, the mechanisms underlying transcriptomic changes are poorly understood. DNA methylation is an epigenetic mark regulating transcription and is largely influenced by dietary components of the one-carbon cycle that generate the methyl group donor, SAM. Therefore, in the present study, we tested whether different maternal diets during pregnancy would alter the DNA methylation and gene expression patterns in fetal tissues.ResultsPregnant ewes were randomly divided into two groups which received either hay or corn diet from mid-gestation (day 67 ± 5) until day 131 ± 1 when fetuses were collected by necropsy. A total of 1516 fetal longissimus dorsi (LD) tissues were used for DNA methylation analysis and gene expression profiling. Whole genome DNA methylation using methyl-binding domain enrichment analysis revealed 60 differentially methylated regions (DMRs) between hay and corn fetuses with 39 DMRs more highly methylated in the hay fetuses vs. 21 DMRs more highly methylated in the corn fetuses. Three DMRs (LPAR3, PLIN5-PLIN4, and the differential methylation of a novel lincRNA) were validated using bisulfite sequencing. These DMRs were associated with differential gene expression. Additionally, significant DNA methylation differences were found at the single CpG level. Integrative methylome and transcriptome analysis revealed an association between gene expression and inter-/intragenic methylated regions. Furthermore, intragenic DMRs were found to be associated with expression of neighboring genes.ConclusionsThe findings of this study imply that maternal diet from mid- to late-gestation can shape the epigenome and the transcriptome of fetal tissues, and putatively affect phenotypes of the lambs.

Dataset Information

Integrative Analysis of Transcriptomic and Methylomic Data in Photoperiod-Dependent Regulation of Cucumber Sex Expression.

Publications

Integrative Analysis of Transcriptomic and Methylomic Data in Photoperiod-Dependent Regulation of Cucumber Sex Expression.

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