A histone modication-based synthetic circuit to engineer temporal gene expression in Arabidopsis floral meristems

• Project/Area Number: 18H02465
• Research Category: Grant-in-Aid for Scientific Research (B)
• Allocation Type: Single-year Grants
• Section: 一般
• Review Section: Basic Section 44030:Plant molecular biology and physiology-related
• Research Institution: Nara Institute of Science and Technology
• Principal Investigator: Nobutoshi Yamaguchi 奈良先端科学技術大学院大学, 先端科学技術研究科, 准教授 (90767899)
• Project Period (FY): 2018-04-01 – 2023-03-31
• Project Status: Completed (Fiscal Year 2022)
• Budget Amount: ¥17,030,000 (Direct Cost: ¥13,100,000、Indirect Cost: ¥3,930,000); Fiscal Year 2022: ¥2,860,000 (Direct Cost: ¥2,200,000、Indirect Cost: ¥660,000); Fiscal Year 2021: ¥3,250,000 (Direct Cost: ¥2,500,000、Indirect Cost: ¥750,000); Fiscal Year 2020: ¥2,990,000 (Direct Cost: ¥2,300,000、Indirect Cost: ¥690,000); Fiscal Year 2019: ¥3,640,000 (Direct Cost: ¥2,800,000、Indirect Cost: ¥840,000); Fiscal Year 2018: ¥4,290,000 (Direct Cost: ¥3,300,000、Indirect Cost: ¥990,000)
• Keywords: シロイヌナズナ / 花発生 / エピゲノム / 遺伝子発現 / 転写因子 / 植物分子遺伝学 / エピジェネティクス / 花の形態形成

Outline of Final Research Achievements

The AG regulates floral meristem termination by preventing maintenance of the histone modification H3K27me3 along the KNU coding sequence. At two days after AG binding, cell division has diluted the repressive mark H3K27me3, allowing activation of KNU transcription prior to floral meristem termination. However, how many other downstream genes are temporally regulated by this intrinsic epigenetic timer is remain unknown.

Here, we identify direct AG targets regulated through cell cycle-coupled H3K27me3 dilution in Arabidopsis thaliana. Expression of the targets occurred later in plants with longer H3K27me3-marked regions. We established a mathematical model to predict gene expression and manipulated temporal gene expression using the H3K27me3-marked del region from the KNU coding sequence. Our results suggest that AG controls the timing of expression of various target genes via cell cycle-coupled dilution of H3K27me3 for proper floral meristem termination and stamen development.

Academic Significance and Societal Importance of the Research Achievements

本研究により、メチル基をもつヒストンの数と分化遺伝子の誘導時期を方程式にして、花の幹細胞の自己複製と分化のバランスを決める際に起こる仕組みを数学的に明らかにし、一般的な法則を見出しました。この法則に従って、メチル基をもつヒストンの数を人為的に増やすと、方程式で計算される時期に分化遺伝子が誘導される実証実験にも成功しました。植物の幹細胞の自己複製と分化の普遍的な仕組みを知るだけでなく、その仕組みを有効に使って農業や園芸の分野で利用していくうえでも大きく貢献すると期待されます。

Research Products

• [Journal Article] AGAMOUS regulates various target genes via cell cycle?coupled H3K27me3 dilution in floral meristems and stamens (2023)
  • Author(s): Pelayo Margaret Anne、Morishita Fumi、Sawada Haruka、Matsushita Kasumi、Iimura Hideaki、He Zemiao、Looi Liang Sheng、Katagiri Naoya、Nagamori Asumi、Suzuki Takamasa、?irl Marek、Soukup Ale?、Satake Akiko、Ito Toshiro、Yamaguchi Nobutoshi
  • Journal Title: The Plant Cell Volume: - Issue: 8 Pages: 2821-2847
  • DOI: 10.1093/plcell/koad123
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Local and terminal cell differentiation mediated by the jasmonic acid-mediated autophagy evokes petal abscission in Arabidopsis thaliana. (2022)
  • Author(s): Yamamoto H, Furuta Y, Hirakawa T, Uemura A, Pelayo M, Iimura H, Katagiri N, Takeda-Kamiya N, Kumaishi K, Ishiguro S, Ichihashi Y, Suzuki T, Goh T, Toyooka K, Ito T, Yamaguchi N
  • Journal Title: Research Square Volume: -
• [Journal Article] A phase-separated transcription factor regulates an interspecific barrier. (2022)
  • Author(s): Fuji S, Yamamoto E, Tangpranomkom S, Kimura Y, Miura H, Yamaguchi N, Niidome M, Shimosato-Asano H, Kato Y, Wada Y, Ito T, Takayama S
  • Journal Title: Research Square Volume: -
• [Journal Article] Identification and characterization of drought-tolerant local pigmented rice from Indonesia (2022)
  • Author(s): Sebastian Alfino、Nugroho Ilham Cahyo、Putra Herdin Surya Dwi、Susanto Febri Adi、Wijayanti Putri、Yamaguchi Nobutoshi、Nuringtyas Tri Rini、Purwestri Yekti Asih
  • Journal Title: Physiology and Molecular Biology of Plants Volume: 28 Issue: 5 Pages: 1061-1075
  • DOI: 10.1007/s12298-022-01185-5
• [Journal Article] Seed Halopriming Improves Salinity Tolerance of Some Rice Cultivars During Seedling Stage (2022)
  • Author(s): Hidayah Anik、Nisak Rizka Rohmatin、Susanto Febri Adi、Nuringtyas Tri Rini、Yamaguchi Nobutoshi、Purwestri Yekti Asih
  • Journal Title: Botanical Studies Volume: 63 Issue: 1
  • DOI: 10.1186/s40529-022-00354-9
• [Journal Article] Editorial: Epigenetics in Plant Development (2022)
  • Author(s): Nobutoshi Yamaguchi
  • Journal Title: Frontiers in Plant Science Volume: -
  • DOI: 10.21203/rs.3.rs-1240596/v1
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Abscisic acid-dependent histone demethylation during postgermination growth arrest in Arabidopsis. (2019)
  • Author(s): Wu, J., Ichihashi, Y., Suzuki, T., Shibata, A., Shirasu, K., Yamaguchi, N. and Ito T.
  • Journal Title: Plant Cell and Environment Volume: 42 Pages: 2198-2214
  • Peer Reviewed
• [Journal Article] Histone demethylases control root elongation in response to stress-signaling hormone abscisic acid. (2019)
  • Author(s): Wu, J., Yamaguchi, N. and Ito T.
  • Journal Title: Plant Signaling and Behavior Volume: 14 Pages: 1604019-1604019
  • Peer Reviewed
• [Journal Article] When to stop: an update on molecular mechanisms of floral meristem termination. (2019)
  • Author(s): Xu Y., Yamaguchi, N. Gan, E-S., and Ito, T.
  • Journal Title: Journal of Experimental Botany Volume: 70 Pages: 1711-1718
  • Peer Reviewed
• [Journal Article] Integration of transcriptional repression and Polycomb-mediated silencing of WUSCHEL in floral meristems. (2019)
  • Author(s): Sun, B., Zhou, Y., Cai, J., Shang E., Yamaguchi, N., Xiao, J., Looi, L-S., Wee W-Y., Gao, X., Wagner, D., and Ito, T.
  • Journal Title: Plant Cell Volume: 31 Pages: 1488-1505
  • NAID: 120006726651
  • Peer Reviewed
• [Journal Article] The roles of plant hormones and their interactions with regulatory genes in determining meristem activity. (2019)
  • Author(s): Ze Hong, L., Hirakawa, T., Yamaguchi, N., Ito, T.
  • Journal Title: International Journals of Molecular Sciences Volume: 20 Pages: 4065-4065
  • Peer Reviewed
• [Journal Article] Lateral root initiation requires the sequential induction of transcription factors LBD16 and PUCHI in Arabidopsis thaliana. (2019)
  • Author(s): Goh, T., Toyokura, K., Yamaguchi, N., Okamoto, T., Uehara, T., Kaneko, S., Takebayashi, Y., Kasahara, H., Ikeyama, Y., Okushima, Y., Nakajima, K., Mimura, T., Tasaka, M., and Fukaki, H.
  • Journal Title: New Phytologist Volume: 222 Pages: 2-2
  • Peer Reviewed
• [Journal Article] CRABS CLAW and SUPERMAN coordinate hormone-, stress-, and metabolic-related gene expression during Arabidopsis stamen development. (2019)
  • Author(s): Ze Hong, L., Tatsumi, Y., Ichihashi, Y., Suzuki, T., Shibata, A., Shirasu, K., Yamaguchi, N. and Ito T.
  • Journal Title: Frontiers in Ecology and Evolution. Volume: 7 Pages: 437-437
  • Peer Reviewed
• [Journal Article] Abscisic acid‐dependent histone demethylation during postgermination growth arrest in Arabidopsis (2019)
  • Author(s): Wu Jinfeng、Ichihashi Yasunori、Suzuki Takamasa、Shibata Arisa、Shirasu Ken、Yamaguchi Nobutoshi、Ito Toshiro
  • Journal Title: Plant, Cell & Environment Volume: - Issue: 7 Pages: 2198-2214
  • DOI: 10.1111/pce.13547
  • Peer Reviewed / Open Access
• [Journal Article] Chromatin-mediated feed-forward auxin biosynthesis in floral meristem determinacy. (2018)
  • Author(s): Yamaguchi, N., Huang, J., Tatsumi, Y., Abe, M., Sugano, S. S., Kojima, M., Takebayashi, Y., Kiba, T., Yokoyama, R., Nishitani, K., Sakakibara, H., and Ito, T.
  • Journal Title: Nature Commun. Volume: 9 Issue: 1 Pages: 5290-5290
  • DOI: 10.1038/s41467-018-07763-0
  • NAID: 120006549567
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis. (2018)
  • Author(s): Xu, Y., Prunet, N., Gan, E-S., Wang, Y., Stewart, D., Wellmer, F., Huang, J., Yamaguchi, N., Tatsumi, Y., Kojima, M., Kiba, T., Sakakibara, H., Jack, T.P., Meyerowitz, E.M., Ito, T.
  • Journal Title: EMBO Journal Volume: - Issue: 11
  • DOI: 10.15252/embj.201797499
  • NAID: 120006478564
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Using CRISPR/Cas9 System to Introduce Targeted Mutation in Arabidopsis (2018)
  • Author(s): Ze Hong Lee, Nobutoshi Yamaguchi, Toshiro Ito
  • Journal Title: Plant Transcription Factors.Methods in molecular biology (Clifton, N.J.) Volume: 1830 Pages: 93-108
  • DOI: 10.1007/978-1-4939-8657-6_6
  • ISBN: 9781493986569, 9781493986576
  • Peer Reviewed
• [Journal Article] Gene Expression and Transcription Factor Binding Tests Using Mutated-Promoter Reporter Lines (2018)
  • Author(s): Nishizawa-Yokoi Ayako、Yamaguchi Nobutoshi
  • Journal Title: Methods in molecular biology (Clifton, N.J.) Volume: 2 Pages: 291-305
  • DOI: 10.1007/978-1-4939-8657-6_17
  • ISBN: 9781493986569, 9781493986576
  • Peer Reviewed