Histone deacetylation regulates de novo shoot regeneration

Haruka Temman; Takuya Sakamoto; Minoru Ueda; Kaoru Sugimoto; Masako Migihashi; Kazunari Yamamoto; Yayoi Tsujimoto-Inui; Hikaru Sato; Mio K Shibuta; Norikazu Nishino; Tomoe Nakamura; Hiroaki Shimada; Yukimi Y Taniguchi; Seiji Takeda; Mitsuhiro Aida; Takamasa Suzuki; Motoaki Seki; Sachihiro Matsunaga

doi:10.1093/pnasnexus/pgad002

Histone deacetylation regulates de novo shoot regeneration

PNAS Nexus. 2023 Jan 6;2(2):pgad002. doi: 10.1093/pnasnexus/pgad002. eCollection 2023 Feb.

Authors

Haruka Temman¹, Takuya Sakamoto¹, Minoru Ueda^{2

3}, Kaoru Sugimoto¹, Masako Migihashi⁴, Kazunari Yamamoto⁴, Yayoi Tsujimoto-Inui⁴, Hikaru Sato⁴, Mio K Shibuta⁵, Norikazu Nishino⁶, Tomoe Nakamura^{2

7}, Hiroaki Shimada⁷, Yukimi Y Taniguchi⁸, Seiji Takeda^{9

10}, Mitsuhiro Aida^{11

12}, Takamasa Suzuki¹³, Motoaki Seki^{2

3}, Sachihiro Matsunaga⁴

Affiliations

¹ Department of Applied Biological Science, Faculty of Science and Technology, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba 278-8510, Japan.
² Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro, Tsurumi, Yokohama, Kanagawa 230-0045, Japan.
³ Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan.
⁴ Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562, Japan.
⁵ Academic Assembly (Faculty of Science), Yamagata University, Kojirakawa, Yamagata 990-8560, Japan.
⁶ Graduate School of Life Science and Systems Engineering, Kyushu Institute of Technology, 2-4 Hibikino, Wakamatsu-ku, Kitakyushu-shi, Fukuoka 808-0196, Japan.
⁷ Department of Biological Science and Technology, Tokyo University of Science, 6-3-1 Niijuku, Katsushika-ku, Tokyo 125-8585, Japan.
⁸ School of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda, Hyogo 669-1337, Japan.
⁹ Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Shimogamo Hangi-cho, Sakyo-ku, Kyoto 60-8522, Japan.
¹⁰ Biotechnology Research Department, Kyoto Prefectural Agriculture Forestry and Fisheries Technology Centre, 74 Kitaina Yazuma Oji, Seika, Kyoto 619-0244, Japan.
¹¹ International Research Organization for Advanced Science and Technology, Kumamoto University, 2-39-1 Kurokami, Chuo-ku, Kumamoto 860-8555, Japan.
¹² International Research Center for Agricultural and Environmental Biology, Kumamoto University, 2-39-1 Kurokami, Chuo-ku, Kumamoto 860-855, Japan.
¹³ College of Bioscience and Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi 487-8501, Japan.

Abstract

During de novo plant organ regeneration, auxin induction mediates the formation of a pluripotent cell mass called callus, which regenerates shoots upon cytokinin induction. However, molecular mechanisms underlying transdifferentiation remain unknown. Here, we showed that the loss of HDA19, a histone deacetylase (HDAC) family gene, suppresses shoot regeneration. Treatment with an HDAC inhibitor revealed that the activity of this gene is essential for shoot regeneration. Further, we identified target genes whose expression was regulated through HDA19-mediated histone deacetylation during shoot induction and found that ENHANCER OF SHOOT REGENERATION 1 and CUP-SHAPED COTYLEDON 2 play important roles in shoot apical meristem formation. Histones at the loci of these genes were hyperacetylated and markedly upregulated in hda19. Transient ESR1 or CUC2 overexpression impaired shoot regeneration, as observed in hda19. Therefore, HDA19 mediates direct histone deacetylation of CUC2 and ESR1 loci to prevent their overexpression at the early stages of shoot regeneration.

Keywords: epigenetics; histone deacetylation; shoot regeneration; transdifferentiation.