Exogenous cellulase switches cell interdigitation to cell elongation in an RIC1-dependent manner in Arabidopsis thaliana cotyledon pavement cells

Takumi Higaki, Hisako Takigawa-Imamura, Kae Akita, Natsumaro Kutsuna, Ryo Kobayashi, Seiichiro Hasezawa, Takashi Miura

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Pavement cells in cotyledons and true leaves exhibit a jigsaw puzzle-like morphology in most dicotyledonous plants. Among the molecular mechanisms mediating cell morphogenesis, two antagonistic Rho-like GTPases regulate local cell outgrowth via cytoskeletal rearrangements. Analyses of several cell wall-related mutants suggest the importance of cell wall mechanics in the formation of interdigitated patterns. However, how these factors are integrated is unknown. In this study, we observed that the application of exogenous cellulase to hydroponically grown Arabidopsis thaliana cotyledons switched the interdigitation of pavement cells to the production of smoothly elongated cells. The cellulaseinduced inhibition of cell interdigitation was not observed in a RIC1 knockout mutant. This gene encodes a Rho-like GTPase-interacting protein important for localized cell growth suppression via microtubule bundling on concave cell interfaces. Additionally, to characterize pavement cell morphologies, we developed a mathematical model that considers the balance between cell and cell wall growth, restricted global cell growth orientation, and regulation of local cell outgrowth mediated by a Rho-like GTPase-cytoskeleton system. Our computational simulations fully support our experimental observations, and suggest that interdigitated patterns form because of mechanical buckling in the absence of Rho-like GTPase-dependent regulation of local cell outgrowth. Our model clarifies the cell wall mechanics influencing pavement cell morphogenesis.

Original languageEnglish
Pages (from-to)106-119
Number of pages14
JournalPlant and Cell Physiology
Volume58
Issue number1
DOIs
Publication statusPublished - Jan 1 2017

Fingerprint

Cellulase
Cotyledon
Arabidopsis
endo-1,4-beta-glucanase
cotyledons
cell growth
Arabidopsis thaliana
guanosinetriphosphatase
rho GTP-Binding Proteins
cells
Cell Wall
cell walls
mechanics
morphogenesis
Mechanics
Morphogenesis
Growth
knockout mutants
cytoskeleton
Magnoliopsida

All Science Journal Classification (ASJC) codes

  • Physiology
  • Plant Science
  • Cell Biology

Cite this

Exogenous cellulase switches cell interdigitation to cell elongation in an RIC1-dependent manner in Arabidopsis thaliana cotyledon pavement cells. / Higaki, Takumi; Takigawa-Imamura, Hisako; Akita, Kae; Kutsuna, Natsumaro; Kobayashi, Ryo; Hasezawa, Seiichiro; Miura, Takashi.

In: Plant and Cell Physiology, Vol. 58, No. 1, 01.01.2017, p. 106-119.

Research output: Contribution to journalArticle

@article{019dc31e6e5746309326f0c2f2091457,
title = "Exogenous cellulase switches cell interdigitation to cell elongation in an RIC1-dependent manner in Arabidopsis thaliana cotyledon pavement cells",
abstract = "Pavement cells in cotyledons and true leaves exhibit a jigsaw puzzle-like morphology in most dicotyledonous plants. Among the molecular mechanisms mediating cell morphogenesis, two antagonistic Rho-like GTPases regulate local cell outgrowth via cytoskeletal rearrangements. Analyses of several cell wall-related mutants suggest the importance of cell wall mechanics in the formation of interdigitated patterns. However, how these factors are integrated is unknown. In this study, we observed that the application of exogenous cellulase to hydroponically grown Arabidopsis thaliana cotyledons switched the interdigitation of pavement cells to the production of smoothly elongated cells. The cellulaseinduced inhibition of cell interdigitation was not observed in a RIC1 knockout mutant. This gene encodes a Rho-like GTPase-interacting protein important for localized cell growth suppression via microtubule bundling on concave cell interfaces. Additionally, to characterize pavement cell morphologies, we developed a mathematical model that considers the balance between cell and cell wall growth, restricted global cell growth orientation, and regulation of local cell outgrowth mediated by a Rho-like GTPase-cytoskeleton system. Our computational simulations fully support our experimental observations, and suggest that interdigitated patterns form because of mechanical buckling in the absence of Rho-like GTPase-dependent regulation of local cell outgrowth. Our model clarifies the cell wall mechanics influencing pavement cell morphogenesis.",
author = "Takumi Higaki and Hisako Takigawa-Imamura and Kae Akita and Natsumaro Kutsuna and Ryo Kobayashi and Seiichiro Hasezawa and Takashi Miura",
year = "2017",
month = "1",
day = "1",
doi = "10.1093/pcp/pcw183",
language = "English",
volume = "58",
pages = "106--119",
journal = "Plant and Cell Physiology",
issn = "0032-0781",
publisher = "Oxford University Press",
number = "1",

}

TY - JOUR

T1 - Exogenous cellulase switches cell interdigitation to cell elongation in an RIC1-dependent manner in Arabidopsis thaliana cotyledon pavement cells

AU - Higaki, Takumi

AU - Takigawa-Imamura, Hisako

AU - Akita, Kae

AU - Kutsuna, Natsumaro

AU - Kobayashi, Ryo

AU - Hasezawa, Seiichiro

AU - Miura, Takashi

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Pavement cells in cotyledons and true leaves exhibit a jigsaw puzzle-like morphology in most dicotyledonous plants. Among the molecular mechanisms mediating cell morphogenesis, two antagonistic Rho-like GTPases regulate local cell outgrowth via cytoskeletal rearrangements. Analyses of several cell wall-related mutants suggest the importance of cell wall mechanics in the formation of interdigitated patterns. However, how these factors are integrated is unknown. In this study, we observed that the application of exogenous cellulase to hydroponically grown Arabidopsis thaliana cotyledons switched the interdigitation of pavement cells to the production of smoothly elongated cells. The cellulaseinduced inhibition of cell interdigitation was not observed in a RIC1 knockout mutant. This gene encodes a Rho-like GTPase-interacting protein important for localized cell growth suppression via microtubule bundling on concave cell interfaces. Additionally, to characterize pavement cell morphologies, we developed a mathematical model that considers the balance between cell and cell wall growth, restricted global cell growth orientation, and regulation of local cell outgrowth mediated by a Rho-like GTPase-cytoskeleton system. Our computational simulations fully support our experimental observations, and suggest that interdigitated patterns form because of mechanical buckling in the absence of Rho-like GTPase-dependent regulation of local cell outgrowth. Our model clarifies the cell wall mechanics influencing pavement cell morphogenesis.

AB - Pavement cells in cotyledons and true leaves exhibit a jigsaw puzzle-like morphology in most dicotyledonous plants. Among the molecular mechanisms mediating cell morphogenesis, two antagonistic Rho-like GTPases regulate local cell outgrowth via cytoskeletal rearrangements. Analyses of several cell wall-related mutants suggest the importance of cell wall mechanics in the formation of interdigitated patterns. However, how these factors are integrated is unknown. In this study, we observed that the application of exogenous cellulase to hydroponically grown Arabidopsis thaliana cotyledons switched the interdigitation of pavement cells to the production of smoothly elongated cells. The cellulaseinduced inhibition of cell interdigitation was not observed in a RIC1 knockout mutant. This gene encodes a Rho-like GTPase-interacting protein important for localized cell growth suppression via microtubule bundling on concave cell interfaces. Additionally, to characterize pavement cell morphologies, we developed a mathematical model that considers the balance between cell and cell wall growth, restricted global cell growth orientation, and regulation of local cell outgrowth mediated by a Rho-like GTPase-cytoskeleton system. Our computational simulations fully support our experimental observations, and suggest that interdigitated patterns form because of mechanical buckling in the absence of Rho-like GTPase-dependent regulation of local cell outgrowth. Our model clarifies the cell wall mechanics influencing pavement cell morphogenesis.

UR - http://www.scopus.com/inward/record.url?scp=85014091643&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85014091643&partnerID=8YFLogxK

U2 - 10.1093/pcp/pcw183

DO - 10.1093/pcp/pcw183

M3 - Article

C2 - 28011873

AN - SCOPUS:85014091643

VL - 58

SP - 106

EP - 119

JO - Plant and Cell Physiology

JF - Plant and Cell Physiology

SN - 0032-0781

IS - 1

ER -