GRAS transcription factors regulate cell division planes in moss overriding the default rule

• Published in: Proceedings of the National Academy of Sciences - PNAS 2023-01, Vol.120 (4), p.e2210632120
• Main Authors: Ishikawa, Masaki, Fujiwara, Ayaka, Kosetsu, Ken, Horiuchi, Yuta, Kamamoto, Naoya, Umakawa, Naoyuki, Tamada, Yosuke, Zhang, Liechi, Matsushita, Katsuyoshi, Palfalvi, Gergo, Nishiyama, Tomoaki, Kitasaki, Sota, Masuda, Yuri, Shiroza, Yoshiki, Kitagawa, Munenori, Nakamura, Toru, Cui, Hongchang, Hiwatashi, Yuji, Kabeya, Yukiko, Shigenobu, Shuji, Aoyama, Tsuyoshi, Kato, Kagayaki, Murata, Takashi, Fujimoto, Koichi, Benfey, Philip N, Hasebe, Mitsuyasu, Kofuji, Rumiko
• Format: Article
• Language: English
• Subjects: Algae; Arabidopsis - genetics; Arabidopsis Proteins - metabolism; Bacteria; Biological Sciences; Cell division; Cell Division - genetics; Cell walls; Evolution; Flowering; Flowering plants; Gene Expression Regulation, Plant; Leaves; Mosses; Orientation; Plant cells; Plant Roots - metabolism; Plants (botany); Regulatory mechanisms (biology); Soil bacteria; Soil microorganisms; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Veins (plant anatomy)
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2210632120

Plant cells are surrounded by a cell wall and do not migrate, which makes the regulation of cell division orientation crucial for development. Regulatory mechanisms controlling cell division orientation may have contributed to the evolution of body organization in land plants. The GRAS family of transcription factors was transferred horizontally from soil bacteria to an algal common ancestor of land plants. ( ) and ( ) genes in this family regulate formative periclinal cell divisions in the roots of flowering plants, but their roles in nonflowering plants and their evolution have not been studied in relation to body organization. Here, we show that cell autonomously inhibits formative periclinal cell divisions indispensable for leaf vein formation in the moss , and SHR expression is positively and negatively regulated by and the GRAS member , respectively. While precursor cells of a leaf vein lacking SHR usually follow the geometry rule of dividing along the division plane with the minimum surface area, SHR overrides this rule and forces cells to divide nonpericlinally. Together, these results imply that these bacterially derived GRAS transcription factors were involved in the establishment of the genetic regulatory networks modulating cell division orientation in the common ancestor of land plants and were later adapted to function in flowering plant and moss lineages for their specific body organizations.