A DEMETER-like DNA demethylase governs tomato fruit ripening

Liu, Ruie; How‐Kit, Alexandre; Stammitti, Linda; Teyssier, Emeline; Rolin, Dominique; Mortain‐Bertrand, Anne; Halle, Stefanie; Ming-chun, Liu; Kong, Jie; Wu, Chaoqun; Degraeve-Guibault, Charlotte; Chapman, Natalie H.; Maucourt, Mickaël; Hodgman, Charlie; Tost, Jörg; Bouzayen, Mondher; Hong, Yiguo; Seymour, Graham B.; Giovannoni, James J.; Gallusci, Philippe

doi:10.1073/pnas.1503362112

Cited by 272 publications

(309 citation statements)

References 34 publications

(41 reference statements)

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“…Several of these were found to be orthologous to genes that are known to be important regulators of flower and fruit development in other species. This suggests that apple fruit development is regulated by epigenetic processes, which is consistent with data obtained in tomato, demonstrating that DNA methylation is important for fruit ripening [56][57][58] .…”

Section: Discussionsupporting

confidence: 89%

High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development

et al. 2017

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Using the latest sequencing and optical mapping technologies, we have produced a high-quality de novo assembly of the apple (Malus domestica Borkh.) genome. Repeat sequences, which represented over half of the assembly, provided an unprecedented opportunity to investigate the uncharacterized regions of a tree genome; we identified a new hyper-repetitive retrotransposon sequence that was over-represented in heterochromatic regions and estimated that a major burst of different transposable elements (TEs) occurred 21 million years ago. Notably, the timing of this TE burst coincided with the uplift of the Tian Shan mountains, which is thought to be the center of the location where the apple originated, suggesting that TEs and associated processes may have contributed to the diversification of the apple ancestor and possibly to its divergence from pear. Finally, genome-wide DNA methylation data suggest that epigenetic marks may contribute to agronomically relevant aspects, such as apple fruit development.

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Section: Discussionsupporting

confidence: 89%

High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development

et al. 2017

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“…Tomato fruits undergo a dramatic loss in DNA methylation during ripening (27). The application of a DNA methylation inhibitor facilitated ripening, and RNAi-mediated down-regulation of putative DNA demethylases inhibited fruit ripening in tomato, suggesting that active DNA demethylation plays an important role in regulating fruit ripening (27,29). It remains unclear, however, how active DNA demethylation contributes to ripening and ripening-associated changes in DNA methylation patterns.…”

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confidence: 99%

“…Tomato contains four putative DNA demethylases (SlDML1 to -4) according to sequence homology with the Arabidopsis DNA demethylases, and two of them, SlDML1 and SlDML2, are most closely related to the Arabidopsis ROS1 (AtROS1) (29,30). A previous study used RNAi against the conserved HhH-GPD domain to investigate the function of SlDMLs in tomato (29).…”

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confidence: 99%

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

Lang

YiHai

Tang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

378

409

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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 5-mC DNA glycosylases/lyases (i.e., DNA demethylases). Recent reports 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, SlDML2, 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 included not only hundreds of ripening-induced genes but also many ripening-repressed genes. Our results show that SlDML2 is critical for tomato fruit ripening and suggest that active DNA demethylation is required for both the activation of ripeninginduced genes and the inhibition of ripening-repressed genes.DNA demethylase | 5-mC DNA glycosylase | DNA methylation | epigenetic regulation | gene silencing D NA methylation is a conserved epigenetic modification that is generally associated with inactive transcription in plants and mammals. As such, DNA methylation plays important roles in many biological processes, such as genome stability, gene imprinting, development, and response to the environment (1-3). In contrast to mammals, in which DNA methylation predominantly occurs at cytosines in the symmetric CG sequence context, plants commonly have methylation in the asymmetrical CHH sequence context (H = A, C, or T), as well as in the symmetrical CG and CHG contexts (1, 2). In plants, cytosines in all sequence contexts can be de novo methylated through the well-known RNA-directed DNA methylation pathway (RdDM), in which 24-nt siRNAs guide the DNA methyltransferase domains rearranged methyltransferase 2 (DRM2) to methylate target loci (4). DNA methylation can be maintained during replication; mCG and mCHG are maintained by the DNA methyltransferases DNA methyltransferase 1 (MET1) and chromomethylase 3 (CMT3), respectively, whereas mCHH is maintained by CMT2 and RdDM (4, 5).Cytosine methylation levels are dynamically regulated by DNA methylation and demethylation reactions (3, 6). DNA methylation can be lost either because of failure in maintaining methylation after replication (i.e., passive DNA demethylation) or because of active removal by enzymes (i.e., active DNA demethylation). Previous studies have identified and characterized several enzymes important for active DNA demethylation in Arabidopsis (7-11). The ROS1 family of bifunctional 5-methylcytosine DNA glycosylases/lyases, often referred to as DNA demethylases, initiate active DNA demethylation by removing the methylcytosine base from the DNA backbone, resulting in a single nucleotide gap that can be filled with an unmethylated cytosine through a base excision repair pathway (7,8,12,13). Several enzymes acting downstream of ROS1, such as the 3′ DNA phosphatase ZDP, AP endonuclease-like protein APE1L, and DNA ligase I (AtLIG1), have also been identified ...

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“…18 Indeed, they later on identified the molecular mechanism of this active DNA demethylation as being mainly mediated by the tomato DEME-TER-like DNA demethylase SlDML2. 19 This finding is especially interesting when considering the timing and extent of DNA demethylation as a probable source of variation in the diversity of kinetics and intensity of ripening among tomato varieties. Moreover, because changes in DNA methylation were also reported during pear and apple ripening, 20,21 one can ask whether such mechanism is conserved in all fleshy fruit species.…”

Section: Microscopy Molecules and Modeling: Elucidating Nuclear Orgmentioning

confidence: 98%

Chromatin and epigenetics in all their states: Meeting report of the first conference on Epigenetic and Chromatin Regulation of Plant Traits - January 14 – 15, 2016 - Strasbourg, France

Bey

Jamge²,

Klemme

et al. 2016

Epigenetics

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In January 2016, the first Epigenetic and Chromatin Regulation of Plant Traits conference was held in Strasbourg, France. An all-star lineup of speakers, a packed audience of 130 participants from over 20 countries, and a friendly scientific atmosphere contributed to make this conference a meeting to remember. In this article we summarize some of the new insights into chromatin, epigenetics, and epigenomics research and highlight nascent ideas and emerging concepts in this exciting area of research.

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A DEMETER-like DNA demethylase governs tomato fruit ripening

Cited by 272 publications

References 34 publications

High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development

High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development

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

Chromatin and epigenetics in all their states: Meeting report of the first conference on Epigenetic and Chromatin Regulation of Plant Traits - January 14 – 15, 2016 - Strasbourg, France

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