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Structure and Biomechanics during Xylem Vessel Transdifferentiation in Arabidopsis thaliana

Roumeli, Eleftheria and Ginsberg, Leah and McDonald, Robin and Spigolon, Giada and Hendrickx, Rodinde and Ohtani, Misato and Demura, Taku and Ravichandran, Guruswami and Daraio, Chiara (2020) Structure and Biomechanics during Xylem Vessel Transdifferentiation in Arabidopsis thaliana. Plants, 9 (12). Art. No. 1715. ISSN 2223-7747. PMCID PMC7762020. doi:10.3390/plants9121715.

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Individual plant cells are the building blocks for all plantae and artificially constructed plant biomaterials, like biocomposites. Secondary cell walls (SCWs) are a key component for mediating mechanical strength and stiffness in both living vascular plants and biocomposite materials. In this paper, we study the structure and biomechanics of cultured plant cells during the cellular developmental stages associated with SCW formation. We use a model culture system that induces transdifferentiation of Arabidopsis thaliana cells to xylem vessel elements, upon treatment with dexamethasone (DEX). We group the transdifferentiation process into three distinct stages, based on morphological observations of the cell walls. The first stage includes cells with only a primary cell wall (PCW), the second covers cells that have formed a SCW, and the third stage includes cells with a ruptured tonoplast and partially or fully degraded PCW. We adopt a multi-scale approach to study the mechanical properties of cells in these three stages. We perform large-scale indentations with a micro-compression system in three different osmotic conditions. Atomic force microscopy (AFM) nanoscale indentations in water allow us to isolate the cell wall response. We propose a spring-based model to deconvolve the competing stiffness contributions from turgor pressure, PCW, SCW and cytoplasm in the stiffness of differentiating cells. Prior to triggering differentiation, cells in hypotonic pressure conditions are significantly stiffer than cells in isotonic or hypertonic conditions, highlighting the dominant role of turgor pressure. Plasmolyzed cells with a SCW reach similar levels of stiffness as cells with maximum turgor pressure. The stiffness of the PCW in all of these conditions is lower than the stiffness of the fully-formed SCW. Our results provide the first experimental characterization of the mechanics of SCW formation at single cell level.

Item Type:Article
Related URLs:
URLURL TypeDescription CentralArticle
Roumeli, Eleftheria0000-0002-2828-1428
Ginsberg, Leah0000-0001-9685-7014
Spigolon, Giada0000-0002-1704-8372
Ohtani, Misato0000-0001-5429-3310
Demura, Taku0000-0002-2499-4738
Ravichandran, Guruswami0000-0002-2912-0001
Daraio, Chiara0000-0001-5296-4440
Additional Information:© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( Received: 27 October 2020; Revised: 30 November 2020; Accepted: 3 December 2020; Published: 5 December 2020. We would like to acknowledge the contributions of Jenny Martinez, who conducted part of the micro-indentations in water, and Luca Bonanomi for helpful discussions. This work was supported in part by the Resnick Sustainability Institute at Caltech (C.D.) and by the MEXT KAKENHI Grant Numbers JP18H05484 and JP18H05489 (M.O. and T.D.). Author Contributions: Conceptualization, E.R., M.O., T.D. and C.D.; methodology, E.R.; data analysis, E.R., L.G., R.M., G.S.; data curation, E.R., L.G.; Writing—Original draft preparation, E.R., L.G.; Writing—Review and editing, E.R., L.G., R.M., G.S., R.H., M.O., T.D., G.R., and C.D.; visualization, E.R., L.G., R.M., G.S. All authors have read and agreed to the published version of the manuscript. The authors declare no conflict of interest.
Group:Resnick Sustainability Institute, GALCIT
Funding AgencyGrant Number
Resnick Sustainability InstituteUNSPECIFIED
Ministry of Education, Culture, Sports, Science and Technology (MEXT)JP18H05484
Ministry of Education, Culture, Sports, Science and Technology (MEXT)JP18H05489
Subject Keywords:plant biomechanics; turgor pressure; micro-compression; AFM; Arabidopsis thaliana; differentiation
Issue or Number:12
PubMed Central ID:PMC7762020
Record Number:CaltechAUTHORS:20201214-121033243
Persistent URL:
Official Citation:Roumeli, E.; Ginsberg, L.; McDonald, R.; Spigolon, G.; Hendrickx, R.; Ohtani, M.; Demura, T.; Ravichandran, G.; Daraio, C. Structure and Biomechanics during Xylem Vessel Transdifferentiation in Arabidopsis thaliana. Plants 2020, 9, 1715; DOI: 10.3390/plants9121715
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107067
Deposited By: Tony Diaz
Deposited On:14 Dec 2020 20:31
Last Modified:16 Nov 2021 18:59

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