Kanazawa University led group clarify that genes transferred from bacteria were the key to plants emerging onto the land

An international collaborative research team consisting of Assistant Professor Rumiko Kofuji and former graduate student Ayaka Fujiwara of the Institute of Science and Engineering, Kanazawa University, Assistant Professor Masaki Ishikawa and Professor Mitsuyasu Hasebe of the Division of Evolutionary Biology, National Institute for Basic Biology, Associate Professor Koichi Fujimoto and doctoral student Naoya Kamamoto of the Graduate School of Science, Osaka University, Professor Philip N. Benfey of Duke University in the US and their colleagues has used a moss, Physcomitrium patens, to clarify that three types of gene (members of the GRAS family that were transferred to the genomic DNA of the ancestors of land plants from bacteria in the soil) cause periclinal division only in certain cells by manipulating cell division orientation in each cell, forming the water‐conducting tissues (vessels, etc.) that made it possible for plants to emerge onto the land.

Terrestrial plants form thick structures adapted to the land environment, including water‐conducting tissues, through periclinal division. This periclinal division was thought to be one of the driving forces behind plants emerging onto the land, but the mechanism that brought about periclinal division during the evolutionary process of plants was unclear.

The leaves of the moss Physcomitrium patens have water‐conducting tissues that are created through periclinal division in their center. The research team discovered that the SHR gene, a member of the GRAS family that controls periclinal division in thale cress, also exists in this moss and investigated the activity of this gene. As a result, they clarified that SHR proteins created by the SHR gene are present in young leaf cells that do not undergo periclinal division, while SHR proteins are not present in the cells of the two central layers that do undergo periclinal division.

Meanwhile, when the team used genetic modification to remove SHR genes, meaning that SHR proteins could not be created, periclinal division occurred in cells that normally do not undergo this kind of division. Conversely, when SHR genes were active in all cells, periclinal division did not occur even in the central cells, leaving leaves formed only of a single layer of cells without a midrib (the thick vein that runs through the center of a leaf). From this, the team learned that the mechanism that ensures SHR proteins are active in certain cells and not in others is needed to form a midrib.

They also found that SCR genes and LAS genes, members of the same GRAS family, regulate the activity of SHR genes. When the team used genetic modification to disrupt SCR genes, the SHR genes in cells that should have created the lamina ceased their activity, periclinal division occurred and the midrib thickened. On the other hand, when the LAS genes were disrupted, SHR genes were active in the two central cell layers and the midrib was unable to form.

Thus, it has become clear that SHR genes, SCR genes and LAS genes come together to create cells in which periclinal division occurs and those in which it does not, leading to the formation of a thick midrib containing water‐conducting tissues in the central part of the leaf, and altering the orientation of the division so that it broadens the leaf area on both sides.

Kofuji commented, 'We think that investigating the activity of GRAS genes could provide clues that will help us clarify how the diverse bodies of plants evolved. It is also possible that controlling the mechanism behind the activity of these genes will enable us to create crops with modified body thickness.'

■ Periclinal division: Plant cells are surrounded by hard cell walls and cannot move, so the way they divide determines the later formation of the plant's body. Division that occurs in parallel to the surface of the plant's body is known as periclinal division. The role of periclinal division is to make the plant's body thicker, as well as to create water‐conducting tissue (such as the veins through which water passes) in the center of the plant.

Journal Information
Publication: Proceedings of the National Academy of Sciences of the United States of America (PNAS)
Title: GRAS transcription factors regulate cell division planes in moss overriding the default rule
DOI: 10.1073/pnas.2210632120