V-Morph_Unravelling how the mechanical regulation of local variability shapes reproducible plant organs

• Applicants: Professor Dr. Arezki Boudaoud; Dr. Olivier Hamant; Professorin Dr. Dorota Kwiatkowska; Dr. Richard S Smith
• Subject Area: Plant Cell and Developmental Biology ; Plant Biochemistry and Biophysics ; Biophysics
• Term: from 2018 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 355722357

• Final Report Year: 2022

Final Report Abstract

Significant loss in agricultural products is caused by increasingly variable environments and the vulnerability of crops to pathogen attacks or extreme environmental conditions. In addition, the agroindustry and the final market often require crops with a high level of homogeneity. This raises the question of resilience: How to produce robust and homogeneous crops? Here we addressed the corresponding key question in developmental biology: How do organs form with consistent sizes and shapes? Indeed, many organs and organisms have a remarkably consistent shape, yet at the cellular level, cell growth and shape can be highly variable, as exemplified by the robustness of flower morphology in a given species. We considered the outermost floral organ, the sepal in the model species Arabidopsis thaliana, and we addressed the mechanical basis of its robustness in shape and size. We performed a multiscale analysis of variability in organ morphogenesis, from subcellular scale to organ scale, with a focus on cell wall and cell growth. We identified molecular regulators of cell-to-cell variability and organ robustness, based on a directed a directed genetic screen among mutants altered in cell wall and in mechanosensing. We analysed in detail the effect of two mutations, one altering the guidance of cellulose synthase, and one altering transcriptional noise and response to mechanical stress. This allowed us to establish links between cell-to-cell variability and organ robustness. During the course of the project, we developed approaches to quantify growth at subcellular scale and to measure tissue mechanics. Altogether, our work contributes to unravelling the role of tissue mechanics and mechanical responses in the robustness of morphogenesis.

Publications

• Raman Spectroscopy in Nonwoody Plants. Methods in Molecular Biology, 83-107. Springer New York.
  Borowska-Wykręt, Dorota & Dulski, Mateusz
  
• Deformation of a cell monolayer due to osmotic treatment: a case study of onion scale epidermis. Botany, 98(1), 21-36.
  Natonik-Białoń, Sandra; Borowska-Wykręt, Dorota; Mosca, Gabriella; Grelowski, Michał; Wrzalik, Roman; Smith, Richard S. & Kwiatkowska, Dorota
  
• Cellular Fourier analysis for geometrically disordered materials. Physical Review Research, 3(2).
  Fruleux, Antoine & Boudaoud, Arezki
  
• Structure, Assembly and Function of Cuticle from Mechanical Perspective with Special Focus on Perianth. International Journal of Molecular Sciences, 22(8), 4160.
  Skrzydeł, Joanna; Borowska-Wykręt, Dorota & Kwiatkowska, Dorota
  
• How Cell Geometry and Cellular Patterning Influence Tissue Stiffness. International Journal of Molecular Sciences, 23(10), 5651.
  Majda, Mateusz; Trozzi, Nicola; Mosca, Gabriella & Smith, Richard S.
  
• Paf1C denoises transcription and growth patterns to achieve organ shape reproducibility. Cold Spring Harbor Laboratory.
  Trinh, Duy-Chi; Martin, Marjolaine; Bald, Lotte; Maizel, Alexis; Trehin, Christophe & Hamant, Olivier
  
• Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE-SYNTHASE INTERACTIVE1. Cold Spring Harbor Laboratory.
  Mollier, Corentin; Skrzydeł, Joanna; Borowska-Wykręt, Dorota; Majda, Mateusz; Bayle, Vincent; Battu, Virginie; Totozafy, Jean-Chrisologue; Dulski, Mateusz; Fruleux, Antoine; Wrzalik, Roman; Mouille, Grégory; Smith, Richard S.; Monéger, Françoise; Kwiatkowska, Dorota & Boudaoud, Arezki
  
• Using positional information to provide context for biological image analysis with MorphoGraphX 2.0. eLife, 11.
  Strauss, Sören; Runions, Adam; Lane, Brendan; Eschweiler, Dennis; Bajpai, Namrata; Trozzi, Nicola; Routier-Kierzkowska, Anne-Lise; Yoshida, Saiko; Rodrigues, da Silveira Sylvia; Vijayan, Athul; Tofanelli, Rachele; Majda, Mateusz; Echevin, Emillie; Le Gloanec, Constance; Bertrand-Rakusova, Hana; Adibi, Milad; Schneitz, Kay; Bassel, George W.; Kierzkowski, Daniel ... & Smith, Richard S.