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Title: Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis

Abstract

The leaf epidermis is a biomechanical shell that influences the size and shape of the organ. Its morphogenesis is a multiscale process in which nanometer-scale cytoskeletal protein complexes, individual cells, and groups of cells pattern growth and define macroscopic leaf traits. Interdigitated growth of neighboring cells is an evolutionarily conserved developmental strategy. Understanding how signaling pathways and cytoskeletal proteins pattern cell walls during this form of tissue morphogenesis is an important research challenge. The cellular and molecular control of a lobed cell morphology is currently thought to involve PIN-FORMED (PIN)-type plasma membrane efflux carriers that generate subcellular auxin gradients. Auxin gradients were proposed to function across cell boundaries to encode stable offset patterns of cortical microtubules and actin filaments between adjacent cells. Many models suggest that long-lived microtubules along the anticlinal cell wall generate local cell wall heterogeneities that restrict local growth and specify the timing and location of lobe formation. Here we used Arabidopsis reverse genetics and multivariate long-term time-lapse imaging to test current cell shape control models. We found that neither PIN proteins nor microtubules along the anticlinal wall predict the patterns of lobe formation. In fields of lobing cells, anticlinal microtubules are not correlated with cell shapemore » and are unstable at the time scales of cell expansion. Our analyses indicate that anticlinal microtubules have multiple functions in pavement cells, and that lobe initiation is likely controlled by complex interactions among cell geometry, cell wall stress patterns, and transient microtubule networks that span the anticlinal and periclinal walls.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1412826
Report Number(s):
NREL/JA-2700-70631
Journal ID: ISSN 0032-0889
DOE Contract Number:  
AC36-08GO28308
Resource Type:
Journal Article
Resource Relation:
Journal Name: Plant Physiology (Bethesda); Journal Volume: 175; Journal Issue: 4
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; pavement cells; microtubules; cell shape

Citation Formats

Belteton, Samuel, Sawchuk, Megan G., Donohoe, Bryon S., Scarpella, Enrico, and Szymanski, Daniel B. Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis. United States: N. p., 2017. Web. doi:10.1104/pp.17.01554.
Belteton, Samuel, Sawchuk, Megan G., Donohoe, Bryon S., Scarpella, Enrico, & Szymanski, Daniel B. Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis. United States. doi:10.1104/pp.17.01554.
Belteton, Samuel, Sawchuk, Megan G., Donohoe, Bryon S., Scarpella, Enrico, and Szymanski, Daniel B. Thu . "Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis". United States. doi:10.1104/pp.17.01554.
@article{osti_1412826,
title = {Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis},
author = {Belteton, Samuel and Sawchuk, Megan G. and Donohoe, Bryon S. and Scarpella, Enrico and Szymanski, Daniel B.},
abstractNote = {The leaf epidermis is a biomechanical shell that influences the size and shape of the organ. Its morphogenesis is a multiscale process in which nanometer-scale cytoskeletal protein complexes, individual cells, and groups of cells pattern growth and define macroscopic leaf traits. Interdigitated growth of neighboring cells is an evolutionarily conserved developmental strategy. Understanding how signaling pathways and cytoskeletal proteins pattern cell walls during this form of tissue morphogenesis is an important research challenge. The cellular and molecular control of a lobed cell morphology is currently thought to involve PIN-FORMED (PIN)-type plasma membrane efflux carriers that generate subcellular auxin gradients. Auxin gradients were proposed to function across cell boundaries to encode stable offset patterns of cortical microtubules and actin filaments between adjacent cells. Many models suggest that long-lived microtubules along the anticlinal cell wall generate local cell wall heterogeneities that restrict local growth and specify the timing and location of lobe formation. Here we used Arabidopsis reverse genetics and multivariate long-term time-lapse imaging to test current cell shape control models. We found that neither PIN proteins nor microtubules along the anticlinal wall predict the patterns of lobe formation. In fields of lobing cells, anticlinal microtubules are not correlated with cell shape and are unstable at the time scales of cell expansion. Our analyses indicate that anticlinal microtubules have multiple functions in pavement cells, and that lobe initiation is likely controlled by complex interactions among cell geometry, cell wall stress patterns, and transient microtubule networks that span the anticlinal and periclinal walls.},
doi = {10.1104/pp.17.01554},
journal = {Plant Physiology (Bethesda)},
number = 4,
volume = 175,
place = {United States},
year = {Thu Nov 30 00:00:00 EST 2017},
month = {Thu Nov 30 00:00:00 EST 2017}
}