Mechanical forces in plant tissue matrix orient cell divisions via microtubule stabilization

• Published in: Developmental cell Vol. 59; no. 10; pp. 1333 - 1344.e4
• Main Authors: Hoermayer, Lukas, Montesinos, Juan Carlos, Trozzi, Nicola, Spona, Leonhard, Yoshida, Saiko, Marhava, Petra, Caballero-Mancebo, Silvia, Benková, Eva, Heisenberg, Carl-Philip, Dagdas, Yasin, Majda, Mateusz, Friml, Jiří
• Format: Journal Article
• Language: English
• Published: United States 20.05.2024
• Subjects: Arabidopsis - cytology; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biomechanical Phenomena; Botanik; Botany; Cell Biology; Cell Division - physiology; Cellbiologi; Cytoskeleton - metabolism; Developmental Biology; Microtubules - metabolism; Plant Roots - cytology; Plant Roots - growth & development; Plant Roots - metabolism; Utvecklingsbiologi; plant development; cell expansion; ablation; cell division; microscopy; microtubules; cell division plane; mechanical forces
• ISSN: 1534-5807; 1878-1551; 1878-1551
• DOI: 10.1016/j.devcel.2024.03.009

Plant morphogenesis relies exclusively on oriented cell expansion and division. Nonetheless, the mechanism(s) determining division plane orientation remain elusive. Here, we studied tissue healing after laser-assisted wounding in roots of Arabidopsis thaliana and uncovered how mechanical forces stabilize and reorient the microtubule cytoskeleton for the orientation of cell division. We identified that root tissue functions as an interconnected cell matrix, with a radial gradient of tissue extendibility causing predictable tissue deformation after wounding. This deformation causes instant redirection of expansion in the surrounding cells and reorientation of microtubule arrays, ultimately predicting cell division orientation. Microtubules are destabilized under low tension, whereas stretching of cells, either through wounding or external aspiration, immediately induces their polymerization. The higher microtubule abundance in the stretched cell parts leads to the reorientation of microtubule arrays and, ultimately, informs cell division planes. This provides a long-sought mechanism for flexible re-arrangement of cell divisions by mechanical forces for tissue reconstruction and plant architecture.