Transcriptome Dynamics of Epidermal Reprogramming during Direct Shoot Regeneration in Torenia fournieri

Author:

Morinaka Hatsune12,Mamiya Akihito13ORCID,Tamaki Hiroaki14,Iwamoto Akitoshi5,Suzuki Takamasa6ORCID,Kawamura Ayako2,Ikeuchi Momoko27,Iwase Akira2ORCID,Higashiyama Tetsuya89,Sugimoto Keiko2,Sugiyama Munetaka19ORCID

Affiliation:

1. Botanical Gardens, Graduate School of Science, The University of Tokyo, 3-7-1 Hakusan, Bunkyo-ku, Tokyo 112-0001, Japan

2. Center for Sustainable Resource Science, RIKEN, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan

3. Department of Biology, Graduate School of Science, Kobe University, Rokkodai-cho 1-1, Nada-ku, Kobe, Hyogo 657-8501, Japan

4. Health and Crop Sciences Research Laboratory, Sumitomo Chemical Co. Ltd., 4-2-1 Takatsukasa, Takarazuka, Hyogo 665-8555, Japan

5. Department of Biological Science, Faculty of Science, Kanagawa University, 2946 Tsuchiya, Hiratsuka 259-1293, Japan

6. Department of Biological Chemistry, College of Bioscience Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi 487-8501, Japan

7. Department of Biology, Faculty of Science, Niigata University, 8050 Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan

8. Institute of Transformative Bio-Molecules (WPI-ITbM), Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan

9. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

Abstract

abstract Shoot regeneration involves reprogramming of somatic cells and de novo organization of shoot apical meristems (SAMs). In the best-studied model system of shoot regeneration using Arabidopsis, regeneration is mediated by the auxin-responsive pluripotent callus formation from pericycle or pericycle-like tissues according to the lateral root development pathway. In contrast, shoot regeneration can be induced directly from fully differentiated epidermal cells of stem explants of Torenia fournieri (Torenia), without intervening the callus mass formation in culture with cytokinin; yet, its molecular mechanisms remain unaddressed. Here, we characterized this direct shoot regeneration by cytological observation and transcriptome analyses. The results showed that the gene expression profile rapidly changes upon culture to acquire a mixed signature of multiple organs/tissues, possibly associated with epidermal reprogramming. Comparison of transcriptomes between three different callus-inducing cultures (callus induction by auxin, callus induction by wounding and protoplast culture) of Arabidopsis and the Torenia stem culture identified genes upregulated in all the four culture systems as candidates of common factors of cell reprogramming. These initial changes proceeded independently of cytokinin, followed by cytokinin-dependent, transcriptional activations of nucleolar development and cell cycle. Later, SAM regulatory genes became highly expressed, leading to SAM organization in the foci of proliferating cells in the epidermal layer. Our findings revealed three distinct phases with different transcriptomic and regulatory features during direct shoot regeneration from the epidermis in Torenia, which provides a basis for further investigation of shoot regeneration in this unique culture system.

Funder

Japan Society for the Promotion of Science

Exploratory Research for Advanced Technology

Japan Science Society

Publisher

Oxford University Press (OUP)

Subject

Cell Biology,Plant Science,Physiology,General Medicine

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