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Histone demethylase SlJMJ6 promotes fruit ripening by removing H3K27 methylation of ripening-related genes in tomato [RNA-Seq]

ABSTRACT: Here, we found that the tomato jmjC domain-containing gene SlJMJ6 encodes a histone lysine demethylase that specifically demethylates H3K27 methylation. Overexpression of SlJMJ6 accelerated fruit ripening in tomato, which is associated with the up-regulated expression of a large number of ripening-related genes. Integrated analysis of RNA-seq and ChIP-seq data identified 55 genes that are targeted directly by SlJMJ6 and transcriptionally up-regulated with decreased H3K27m3 in SlJMJ6 overexpressing (SlJMJ6-OE) fruits. A large number of the SlJMJ6-regulated genes are involved in transcription regulation, ethylene biosynthesis, cell wall degradation, pigment biosynthesis, and hormone signaling. Fourteen ripening-related genes including RIN, ACS4, ACO1, PL, TBG4 were confirmed to be directly regulated by SlJMJ6 through removing H3K27me3. Taken together, these results indicated that SlJMJ6 is a ripening prompting H3K27me3 demethylase that activates the expression of the ripening-related genes by modulating H3K27me3, thereby facilitating fruit ripening in tomato. To our knowledge, this is the first report of the involvement of a histone lysine demethylase in the regulation of fruit ripening.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE142713 | GEO | 2020/04/13

REPOSITORIES: GEO

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Histone demethylase SlJMJ6 promotes fruit ripening by removing H3K27 methylation of ripening-related genes in tomato [ChIP-Seq]

Project description:Here, we found that the tomato jmjC domain-containing gene SlJMJ6 encodes a histone lysine demethylase that specifically demethylates H3K27 methylation. Overexpression of SlJMJ6 accelerated fruit ripening in tomato, which is associated with the up-regulated expression of a large number of ripening-related genes. Integrated analysis of RNA-seq and ChIP-seq data identified 55 genes that are targeted directly by SlJMJ6 and transcriptionally up-regulated with decreased H3K27m3 in SlJMJ6 overexpressing (SlJMJ6-OE) fruits. A large number of the SlJMJ6-regulated genes are involved in transcription regulation, ethylene biosynthesis, cell wall degradation, pigment biosynthesis, and hormone signaling. Fourteen ripening-related genes including RIN, ACS4, ACO1, PL, TBG4 were confirmed to be directly regulated by SlJMJ6 through removing H3K27me3. Taken together, these results indicated that SlJMJ6 is a ripening prompting H3K27me3 demethylase that activates the expression of the ripening-related genes by modulating H3K27me3, thereby facilitating fruit ripening in tomato. To our knowledge, this is the first report of the involvement of a histone lysine demethylase in the regulation of fruit ripening.

2020-04-13 | GSE142712 | GEO

RdDM is involved in epigenetic regulation of strawberry fruit ripening

Project description:DNA methylation is a conserved epigenetic mark that influences diverse biological processes in many eukaryotes. Recently, DNA methylation was proposed to regulate fleshy fruit ripening. Fleshy fruits can be distinguished by their ripening process as climacteric fruits, such as tomatoes, or non-climacteric fruits, such as strawberries. Tomatoes undergo a global decrease in DNA methylation during ripening, due to increased expression of a DNA demethylase gene. The dynamics and biological relevance of DNA methylation during ripening of non-climacteric fruits, or other climacteric fruits, are unknown. Here, we generated and characterized single-base resolution maps of the DNA methylome in strawberry fruit, from immature to ripe stages. We observed an overall loss of DNA methylation during strawberry fruit ripening. Thus, ripening-induced DNA hypomethylation occurs not only in climacteric fruit, but also in non-climacteric fruit. However, we discovered that the mechanisms underlying DNA hypomethylation during ripening of tomato and strawberry are distinct. Unlike in tomatoes, DNA demethylase genes were not up-regulated during ripening of strawberries. Instead, genes involved in RNA-directed DNA methylation were down-regulated during strawberry ripening. Further, ripening-induced DNA hypomethylation was associated with decreased siRNA levels, consistent with reduced RdDM activity. Therefore, we propose that DNA hypomethylation during strawberry ripening is caused by diminished RdDM activity. Finally, hundreds of ripening-related genes displayed altered expression that was associated with, and thus potentially regulated by, DNA hypomethylation during ripening. Our findings provide new insight into the DNA methylation dynamics during the ripening of non-climateric fruit and reveal a novel function of RdDM in regulating an important process in plant development.

2018-11-13 | GSE113084 | GEO

Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Project description:DNA methylation is a conserved epigenetic mark important for genome integrity, development and environmental responses in plants and mammals. Active DNA demethylation in plants is initiated by a family of 5mC DNA glycosylases/lyases (i.e. DNA demethylases). The role of DNA demethylases in transposon regulation, pathogen responses, and gene imprinting and other developmental processes have been studied extensively in the model plant Arabidopsis thaliana. Recent studies suggested a role of active DNA demethylation in fruit ripening in tomato. In this study, we generated loss-of-function mutant alleles of a tomato gene, SlROS1/SlDML1/2, which is a close homolog of the Arabidopsis DNA demethylase gene ROS1. In the fruits of the tomato mutants, increased DNA methylation was found in thousands of genes. These genes include not only hundreds of ripening induced genes but also many ripening repressed genes. Our results show that SlROS1 is critical for tomato fruit ripening, and suggest that active DNA demethylation is required for both the activation of ripening induced genes and inhibition of ripening repressed genes.

2017-05-02 | GSE94903 | GEO

Global gene expression analysis of normal and ripening inhibitor (rin) mutant tomatoes during ripening

Project description:Ripening is an important stage of fruit development to determine its quality as a diet. A tomato (Solanum lycopersicum) MADS-box transcription factor, RIPENING INHIBITOR (RIN), has been believed to serve as a regulator of ripening lying upstream of ethylene-dependent and ethylene-independent pathways. Here, we have conducted global gene expression analysis to comprehensively identify tomato genes whose expressions are affected by the rin mutation using microarray with RNA samples from the normal and rin mutant tomato fruits at the pre-ripening (mature green) and ripening (pink coloring) stages. By analysing this microarray data, we identified 342 of positively regulated and 473 negatively regulated genes by RIN, which showed >5 and <0.2 of the fold change ratio (FC) of normal fruits at the ripening stage relative to those at the pre-ripening stage, respectively, in a RIN-dependent manner. A chromatin immunoprecipitation (ChIP) analysis of the normal ripening tomatoes with the anti-RIN antibody revealed that the positively regulated gene set contained at least 13 direct RIN targets.

2012-04-02 | GSE28564 | GEO

Global gene expression analysis of normal and ripening inhibitor (rin) mutant tomatoes during ripening

2012-04-01 | E-GEOD-28564 | biostudies-arrayexpress

Global increase in DNA Methylation during ripening of sweet orange [ncRNA-seq]

Project description:Using sRNA-Seq to provide small RNA status in fruit ripening stages in sweet orange DNA methylation is an important epigenetic mark involved in many biological processes. The genome of the climacteric tomato fruit undergoes a global loss of DNA methylation due to active DNA demethylation during the ripening process. It is unclear whether the ripening of other fruits is also associated with global DNA demethylation. We characterized the single-base resolution DNA methylomes of sweet orange fruits. Compared to immature orange fruits, ripe orange fruits gained DNA methylation at over 30,000 genomic regions and lost DNA methylation at about 1,000 genomic regions, suggesting a global increase in DNA methylation during orange fruit ripening. This increase in DNA methylation was correlated with decreased expression of DNA demethylase genes. The application of a DNA methylation inhibitor interfered with ripening, indicating that the DNA hypermethylation is critical for the proper ripening of orange fruits. We found that ripening-associated DNA hypermethylation was associated with the repression of several hundred genes, such as photosynthesis genes, and with the activation of hundreds of genes including genes involved in ABA responses. Our results suggest important roles of DNA methylation in orange fruit ripening.

2018-12-28 | GSE120025 | GEO

Understanding the complexity of fruit ripening by transcriptome analysis of rin mutant fruit

Project description:[original title] Understanding the complexity of fruit ripening by transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes A tomato MADS-box transcription factor, LeMADS-RIN, controls fruit ripening and mutation in this gene results in non-ripening phenotype of fruit. This mutation down-regulates certain ripening related ethylene responses, however, other ethylene responses are normal. A complete understanding of this mutation and its effect on fruit transcriptome during ripening is not clear. In this study, microarray analysis has been used to investigate the influence of rin mutation on fruit transcriptome at different stages of ripening. A total of 2,398 genes were found to be differentially expressed in wild type fruit pericarp, which on cluster analysis indicated a major shift in their expression profiles in rin mutant fruit. A total of 1,802 genes were found to be differentially expressed between wild type and rin mutant fruits and 17% of these genes encoded regulatory elements, suggesting that mutation in LeMADS-RIN results in disturbance in the regulatory transcriptional networks during ripening. Since LeMADS-RIN has been reported to bind to the CArG box of LeACS2 promoter, in-silico analysis of 51 putative promoter sequences of the genes, that showed ripening associated up-regulation in wild type but showed impairment in up-regulation in rin mutant fruit during ripening, were searched for presence of CArG box along with ethylene and auxin responsive elements. The study revealed that only 24 putative promoter sequences harbor LeMADS-RIN specific CArG box suggesting an alternative mode of regulation by LeMADS-RIN for CArG box deficient genes. Three chronological stages of tomato (Solanum lycopersicon) fruit ripening were compared between wild type and rin mutant

2012-02-29 | E-GEOD-20720 | biostudies-arrayexpress

RNA methylomes reveal the m6A-mediated regulation of DNA demethylase gene SlDML2 that is required for tomato fruit ripening

Project description:For exploring whether mRNA m6A modification participates in the regulation of tomato fruit ripening, we performed m6A-seq in three tomato fruit samples, including wild-type (WT) at 39 days post-anthesis (DPA) and 42 DPA, and Cnr mutant at 42 DPA, with three biological replicates. mRNA methylome analysis reveals that m6A methylation is a prevalent modification in mRNA of tomato fruit and the m6A sites are predominantly enriched in the stop codon and 3’ untranslated region, where m6A deposition has been proved to negatively correlate with gene expression. Hundreds of ripening-induced and ripening-repressed genes, including the SlDML2, were found to harbour changed m6A levels during fruit ripening or in the Cnr mutant, implicating the involvement of m6A modification in the regulation of fruit ripening.

2019-07-19 | GSE125306 | GEO

fruitENCODE: An encyclopedia of DNA elements for fruit ripening

Project description:Fleshy fruits evolved independently multiple times during angiosperm history, including the use of ethylene for the initiation and maintenance of ripening. ENCODE data of 355 transcriptome, 66 accessible chromatin, 160 histone and 45 DNA methylation profiles from eleven fleshy fruit species revealed three types of transcriptional feedback loops controlling ripening. Eudicots peach, papaya and melon evolved their circuits using carpel senescence NAC genes, whereas tomato, apple and pear utilized floral identity MADS genes derived from recent whole-genome-duplications. The monocot banana used both, forming a unique dual-loop circuit. Genes in these circuits and their tissue-specific H3K27me3 mark could be traced back to both dry fruits and ethylene-independent fleshy fruits, suggesting that the ethylene-dependent ripening mechanisms evolved from pre-existing genetic and epigenetic pathways in the ancestral angiosperms. FruitENCODE provides a comprehensive annotation of functional elements for fleshy fruit crops and new insight into the origins of climacteric fruit ripening.

2018-07-04 | GSE116581 | GEO

Sulfoxidation modification of NON-RIPENING (NOR) transcription factor is involved in the regulation of fruit ripening in tomato

Project description:Transcription factors (TFs) are important regulators of plant growth and development and responses to stresses. TFs themselves are also susceptible to multiple post-translational modifications (PTMs). Relatively, redox-mediated PTM of TFs in plants is not well elucidated. Here, we found that NON-RIPENING (NOR), a master TF regulating tomato fruit ripening, is a target of SlMsrE4 or SlMsrB2, the methionine sulfoxide reductase A and B in tomato, respectively. Methionine oxidation in NOR, i.e. sulfoxidation, or mimicking sulfoxidation by mutating Met138 to glutamine, leads to the decreased DNA-binding capacity and transcriptional regulatory activity in vitro. On the other hand, SlMsrE4 and SlMsrB2 can partially repair oxidized-NOR and restore its DNA-binding capacity. Genetic transformation of the nor mutant with NOR genomic DNA almost completely rescues the ripening phenotype. However, transformation of nor with NOR-M138Q, the mimicked methionine sulfoxidation, inhibits the restore of fruit ripening phenotype, and this is associated with the decreased DNA-binding and transcriptional activation of numerous ripening-related genes. Taken together, these findings uncover a novel mechanism by which Msr-mediated redox modification of NOR regulates the expression of ripening-related genes, thereby influencing tomato fruit ripening. To our knowledge, this is the first report that redox modification of TF regulates fruit ripening. nor is a NOR mutant, the phenotype is obstructed by maturity; NOR-12 is a rotational NOR in NOR mutant, the phenotype is a mature inhibition phenotype that basically restores nor mutant; Nor-18 is a rotation of NOR-M138Q in nor mutant, phenotype with the effect of restoring maturity, but the recovery efficiency is lower than the swing NOR.

2020-05-22 | GSE140853 | GEO

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