ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression

June Sik Kim, Joo Young Lim, Hosub Shin, Beom Gi Kim, Sang Dong Yoo, Woo Taek Kim, Jin Hoe Huh

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

DNA methylation plays an important role in diverse developmental processes in many eukaryotes, including the response to environmental stress. Abscisic acid (ABA) is a plant hormone that is up-regulated under stress. The involvement of DNA methylation in the ABA response has been reported but is poorly understood. DNA demethylation is a reverse process of DNA methylation and often induces structural changes of chromatin leading to transcriptional activation. In Arabidopsis (Arabidopsis thaliana), active DNA demethylation depends on the activity of REPRESSOR OF SILENCING 1 (ROS1), which directly excises 5-methylcytosine from DNA. Here we showed that ros1 mutants were hypersensitive to ABA during early seedling development and root elongation. Expression levels of some ABA-inducible genes were decreased in ros1 mutants, and more than 60% of their proximal regions became hypermethylated, indicating that a subset of ABA-inducible genes are under the regulation of ROS1-dependent DNA demethylation. Notable among them is NICOTINAMIDASE 3 (NIC3) that encodes an enzyme that converts nicotinamide to nicotinic acid in the NAD+ salvage pathway. Many enzymes in this pathway are known to be involved in stress responses. The nic3 mutants display hypersensitivity to ABA, whereas overexpression of NIC3 restores normal ABA responses. Our data suggest that NIC3 is responsive to ABA but requires ROS1-mediated DNA demethylation at the promoter as a prerequisite to transcriptional activation. These findings suggest that ROS1-induced active DNA demethylation maintains the active state of NIC3 transcription in response to ABA.

Original languageEnglish
Pages (from-to)1810-1821
Number of pages12
JournalPlant physiology
Volume179
Issue number4
DOIs
Publication statusPublished - 2019 Apr

Fingerprint

Abscisic Acid
abscisic acid
DNA
DNA methylation
DNA Methylation
transcriptional activation
Arabidopsis
mutants
Transcriptional Activation
5-Methylcytosine
nicotinamide
Plant Growth Regulators
Niacinamide
Niacin
niacin
Enzymes
enzymes
Eukaryota
Seedlings
hypersensitivity

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Kim, J. S., Lim, J. Y., Shin, H., Kim, B. G., Yoo, S. D., Kim, W. T., & Huh, J. H. (2019). ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression. Plant physiology, 179(4), 1810-1821. https://doi.org/10.1104/pp.18.01471
Kim, June Sik ; Lim, Joo Young ; Shin, Hosub ; Kim, Beom Gi ; Yoo, Sang Dong ; Kim, Woo Taek ; Huh, Jin Hoe. / ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression. In: Plant physiology. 2019 ; Vol. 179, No. 4. pp. 1810-1821.
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abstract = "DNA methylation plays an important role in diverse developmental processes in many eukaryotes, including the response to environmental stress. Abscisic acid (ABA) is a plant hormone that is up-regulated under stress. The involvement of DNA methylation in the ABA response has been reported but is poorly understood. DNA demethylation is a reverse process of DNA methylation and often induces structural changes of chromatin leading to transcriptional activation. In Arabidopsis (Arabidopsis thaliana), active DNA demethylation depends on the activity of REPRESSOR OF SILENCING 1 (ROS1), which directly excises 5-methylcytosine from DNA. Here we showed that ros1 mutants were hypersensitive to ABA during early seedling development and root elongation. Expression levels of some ABA-inducible genes were decreased in ros1 mutants, and more than 60{\%} of their proximal regions became hypermethylated, indicating that a subset of ABA-inducible genes are under the regulation of ROS1-dependent DNA demethylation. Notable among them is NICOTINAMIDASE 3 (NIC3) that encodes an enzyme that converts nicotinamide to nicotinic acid in the NAD+ salvage pathway. Many enzymes in this pathway are known to be involved in stress responses. The nic3 mutants display hypersensitivity to ABA, whereas overexpression of NIC3 restores normal ABA responses. Our data suggest that NIC3 is responsive to ABA but requires ROS1-mediated DNA demethylation at the promoter as a prerequisite to transcriptional activation. These findings suggest that ROS1-induced active DNA demethylation maintains the active state of NIC3 transcription in response to ABA.",
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Kim, JS, Lim, JY, Shin, H, Kim, BG, Yoo, SD, Kim, WT & Huh, JH 2019, 'ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression', Plant physiology, vol. 179, no. 4, pp. 1810-1821. https://doi.org/10.1104/pp.18.01471

ROS1-dependent DNA demethylation is required for ABA-inducible NIC3 expression. / Kim, June Sik; Lim, Joo Young; Shin, Hosub; Kim, Beom Gi; Yoo, Sang Dong; Kim, Woo Taek; Huh, Jin Hoe.

In: Plant physiology, Vol. 179, No. 4, 04.2019, p. 1810-1821.

Research output: Contribution to journalArticle

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