ABA signaling converts stem cell fate by substantiating a tradeoff between cell polarity, growth and cell cycle progression and abiotic stress responses in the moss Physcomitrium patens

Marcel Pascal Beier; Chiyo Jinno; Natsumi Noda; Kohei Nakamura; Sumio Sugano; Yutaka Suzuki; Tomomichi Fujita

doi:10.3389/fpls.2023.1303195

ABA signaling converts stem cell fate by substantiating a tradeoff between cell polarity, growth and cell cycle progression and abiotic stress responses in the moss Physcomitrium patens

Front Plant Sci. 2023 Nov 29:14:1303195. doi: 10.3389/fpls.2023.1303195. eCollection 2023.

Authors

Marcel Pascal Beier^#^{1

2}, Chiyo Jinno^#³, Natsumi Noda¹, Kohei Nakamura³, Sumio Sugano⁴, Yutaka Suzuki⁴, Tomomichi Fujita¹

Affiliations

¹ Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo, Hokkaido, Japan.
² Institute for the Advancement of Higher Education, Hokkaido University, Sapporo, Hokkaido, Japan.
³ Division of Life Science, Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido, Japan.
⁴ Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan.

^# Contributed equally.

Abstract

Abscisic acid (ABA)-mediated abiotic stress tolerance causes plant growth inhibition. Under such stress conditions, some mosses generate de novo stress-resistant stem cells, also called brood cells or brachycytes, that do not exist under normal conditions. However, the cell physiological basis of the growth inhibition and the stem cell formation is not well understood. Here, we show that the ABA-induced growth inhibition of the moss Physcomitrium patens apical protonemal cells (protonemal stem cells) is mediated through a shift from asymmetric to symmetric cell division. This change of the cell division mode, and consequently change of stem cell activity, is substantiated by dampening cell polarity and cell proliferative activity through the altered distribution of cytoskeletal elements, the mitotic spindle and the vacuole, which results in the production of stress-resistant stem cells. Alteration of the cell physiological data is supported by the results of RNAseq analysis indicating rapid changes in both cell polarity and cell cycle regulation, while long-term treatments with ABA for 5 to 10 days impact mainly the transcriptional and translational regulation. The regulation of cell polarity and cell cycle genes suggests growth arrest mediated by small GTPases (ROPs) and their guanine exchange factors (ROPGEFs) and by cyclin and cyclin-dependent-kinase complex, respectively. Our data suggest that a tradeoff relationship between growth ability and abiotic stress response in the moss is substantiated by ABA signaling to suppress cell polarity and asymmetric cell growth and may play a pivotal role in stem cell fate conversion to newly produced stress-resistant stem cells.

Keywords: Physcomitrium patens; abscisic acid (ABA); cell cycle; cell division; cell polarity; stress response.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by The Sasakawa Scientific Research Grant (Grant Numbers 2021-4043) from The Japan Science Society and Hokkaido University Ambitious Doctoral Fellowship (Information Science/AI) (to CJ), and MEXT/JSPS KAKENHI Grant Numbers JP 221S0002, JP20570030, JP23657027, JP23012002, JP18H04829, and JP20H04878 (to TF).