Expansins facilitate cell expansion by mediating pH-dependent cell wall (CW) loosening. However, the role of expansins in controlling CW biomechanical properties in specific tissues and organs remains elusive. We monitored hormonal responsiveness and spatial specificity of expression and localization of expansins predicted to be the direct targets of cytokinin signaling in Arabidopsis (Arabidopsis thaliana). We found EXPANSIN1 (EXPA1) homogenously distributed throughout the CW of columella/lateral root cap, while EXPA10 and EXPA14 localized predominantly at 3-cell boundaries in the epidermis/cortex in various root zones. EXPA15 revealed cell-type-specific combination of homogenous vs. 3-cell boundaries localization. By comparing Brillouin frequency shift and AFM-measured Young's modulus, we demonstrated Brillouin light scattering (BLS) as a tool suitable for non-invasive in vivo quantitative assessment of CW viscoelasticity. Using both BLS and AFM, we showed that EXPA1 overexpression upregulated CW stiffness in the root transition zone (TZ). The dexamethasone-controlled EXPA1 overexpression induced fast changes in the transcription of numerous CW-associated genes, including several EXPAs and XYLOGLUCAN:XYLOGLUCOSYL TRANSFERASEs (XTHs), and associated with rapid pectin methylesterification determined by in situ Fourier-transform infrared spectroscopy in the root TZ. The EXPA1-induced CW remodeling is associated with the shortening of the root apical meristem, leading to root growth arrest. Based on our results, we propose that expansins control root growth by a delicate orchestration of CW biomechanical properties, possibly regulating both CW loosening and CW remodeling.

CEITEC Central European Institute of Technology Masaryk University Brno 625 00 Czech Republic

Department of Experimental Biology Faculty of Science Masaryk University Brno 625 00 Czech Republic

Department of Natural Sciences Novosibirsk State University Novosibirsk 630073 Russia

Department of Pathological Physiology Faculty of Medicine Masaryk University Brno 625 00 Czech Republic

Division of Anatomy Centre for Anatomy and Cell Biology Medical University of Vienna Vienna 1090 Austria

Genomics Core Facility European Molecular Biology Laboratory Heidelberg 69117 Germany

INRAE Versailles Grignon 78026 France

Institute of Cytology and Genetics Siberian Branch of Russian Academy of Sciences Novosibirsk 630090 Russia

National Centre for Biomolecular Research Faculty of Science Masaryk University Brno 625 00 Czech Republic

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