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 journalArticlepeer-review

14 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

Bibliographical note

Funding Information:
1This work was supported by the Rural Development Administration (RDA) Woo Jang-Choon Project (grant no. PJ009106 to J.H.H.) and the National Agricultural Genome Program (grant no. PJ013440 to J.H.H.). 2These authors contributed equally to the article. 3Current address: Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, Tsukuba, Ibaraki 305-0074, Japan. 4Author for contact: huhjh@snu.ac.kr. 5Senior author. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jin Hoe Huh (huhjh@snu.ac.kr). J.-S.K. and J.H.H. conceived the research plans; J.-S.K. and J.Y.L. performed most of the experiments; J.-S.K., J.Y.L., B.-G.K., S.-D.Y., W.T.K., and J.H.H. analyzed the data; H.S. analyzed RNA-seq and DNA methylome data; J.-S.K., J.Y.L., and J.H.H. wrote the article with contributions from all the authors; J.H.H. agrees to serve as the author responsible for contact and ensures communication. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.18.01471

Publisher Copyright:
© 2019 American Society of Plant Biologists. All rights reserved.

All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

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