TY - JOUR

T1 - Hormone-regulated expansins: expression, localization, and cell wall biomechanics in Arabidopsis root growth

AU - Samalova, Marketa

AU - Melnikava, Alesia

AU - Elsayad, Kareem

AU - Peaucelle, Alexis

AU - Gahurova, Evelina

AU - Gumulec, Jaromir

AU - Spyroglou, Ioannis

AU - Zemlyanskaya, Elena V

AU - Ubogoeva, Elena V

AU - Balkova, Darina

AU - Demko, Martin

AU - Blavet, Nicolas

AU - Alexiou, Panagiotis

AU - Benes, Vladimir

AU - Mouille, Gregory

AU - Hejatko, Jan

N1 - M.S. has received funding from the Czech Science Foundation, project No. 22-17501S. The work was further supported by the Ministry of Education, Youth and Sports of CR from the European Regional Development Fund-Project “Centre for Experimental Plant Biology”: No. CZ.02.1.01/0.0/0.0/16_019/ 0000738, LTAUSA18161 and the Czech Science Foundation (19-24753S). K.E. acknowledges support from the City of Vienna and the Austrian Ministry of Science (Vision 2020). The work of E.V.Z. and E.V.U. was supported by the Russian Science Foundation (20-14-00140) and the Russian State Budgetary Project (FWNR-2022-0006). We acknowledge Plant Sciences, Bioinformatics, and Cellular Imaging CFs at CEITEC MU supported by MEYS CR (LM2018129). © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.

PY - 2024/1

Y1 - 2024/1

N2 - 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 three-cell boundaries in the epidermis/cortex in various root zones. EXPA15 revealed cell type-specific combination of homogenous vs. three-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. 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 transition zone. The EXPA1-induced CW remodeling associated with 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.

AB - 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 three-cell boundaries in the epidermis/cortex in various root zones. EXPA15 revealed cell type-specific combination of homogenous vs. three-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. 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 transition zone. The EXPA1-induced CW remodeling associated with 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.

KW - Arabidopsis Proteins/genetics

KW - Arabidopsis/metabolism

KW - Biomechanical Phenomena

KW - Cell Wall/metabolism

KW - Gene Expression Regulation, Plant

KW - Hormones/metabolism

KW - Meristem/metabolism

KW - Plant Roots/metabolism

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85181561895&origin=inward&txGid=2fc015e9d850653e911aef81c67c3139

UR - https://www.mendeley.com/catalogue/37765ce0-5861-3a0a-a471-64167bc74765/

U2 - 10.1093/plphys/kiad228

DO - 10.1093/plphys/kiad228

M3 - Article

C2 - 37073485

VL - 194

SP - 209

EP - 228

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 1

ER -