A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response

In this paper, we present a detailed and comprehensive mathematical model of active and passive ion and water transport in plant roots. Two key features are the explicit consideration of the separate, but interconnected, apoplastic, and symplastic transport pathways for ions and water, and the inclu...

Full description

Bibliographic Details
Main Authors: Kylie J. Foster, Stanley J. Miklavcic
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.01326/full
id doaj-88c25c71cc274e87a83b7d23850c0145
record_format Article
spelling doaj-88c25c71cc274e87a83b7d23850c01452020-11-25T00:13:30ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-07-01810.3389/fpls.2017.01326261996A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress ResponseKylie J. FosterStanley J. MiklavcicIn this paper, we present a detailed and comprehensive mathematical model of active and passive ion and water transport in plant roots. Two key features are the explicit consideration of the separate, but interconnected, apoplastic, and symplastic transport pathways for ions and water, and the inclusion of both active and passive ion transport mechanisms. The model is used to investigate the respective roles of the endodermal Casparian strip and suberin lamellae in the salt stress response of plant roots. While it is thought that these barriers influence different transport pathways, it has proven difficult to distinguish their separate functions experimentally. In particular, the specific role of the suberin lamellae has been unclear. A key finding based on our simulations was that the Casparian strip is essential in preventing excessive uptake of Na+ into the plant via apoplastic bypass, with a barrier efficiency that is reflected by a sharp gradient in the steady-state radial distribution of apoplastic Na+ across the barrier. Even more significantly, this function cannot be replaced by the action of membrane transporters. The simulations also demonstrated that the positive effect of the Casparian strip of controlling Na+ uptake, was somewhat offset by its contribution to the osmotic stress component: a more effective barrier increased the detrimental osmotic stress effect. In contrast, the suberin lamellae were found to play a relatively minor, even non-essential, role in the overall response to salt stress, with the presence of the suberin lamellae resulting in only a slight reduction in Na+ uptake. However, perhaps more significantly, the simulations identified a possible role of suberin lamellae in reducing plant energy requirements by acting as a physical barrier to preventing the passive leakage of Na+ into endodermal cells. The model results suggest that more and particular experimental attention should be paid to the properties of the Casparian strip when assessing the salt tolerance of different plant varieties and species. Indeed, the Casparian strip appears to be a more promising target for plant breeding and plant genetic engineering efforts than the suberin lamellae for the goal of improving salt tolerance.http://journal.frontiersin.org/article/10.3389/fpls.2017.01326/fullCasparian stripsuberin lamellaesalt toleranceapoplastic and symplastic transportosmotic stress
collection DOAJ
language English
format Article
sources DOAJ
author Kylie J. Foster
Stanley J. Miklavcic
spellingShingle Kylie J. Foster
Stanley J. Miklavcic
A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
Frontiers in Plant Science
Casparian strip
suberin lamellae
salt tolerance
apoplastic and symplastic transport
osmotic stress
author_facet Kylie J. Foster
Stanley J. Miklavcic
author_sort Kylie J. Foster
title A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
title_short A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
title_full A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
title_fullStr A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
title_full_unstemmed A Comprehensive Biophysical Model of Ion and Water Transport in Plant Roots. I. Clarifying the Roles of Endodermal Barriers in the Salt Stress Response
title_sort comprehensive biophysical model of ion and water transport in plant roots. i. clarifying the roles of endodermal barriers in the salt stress response
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2017-07-01
description In this paper, we present a detailed and comprehensive mathematical model of active and passive ion and water transport in plant roots. Two key features are the explicit consideration of the separate, but interconnected, apoplastic, and symplastic transport pathways for ions and water, and the inclusion of both active and passive ion transport mechanisms. The model is used to investigate the respective roles of the endodermal Casparian strip and suberin lamellae in the salt stress response of plant roots. While it is thought that these barriers influence different transport pathways, it has proven difficult to distinguish their separate functions experimentally. In particular, the specific role of the suberin lamellae has been unclear. A key finding based on our simulations was that the Casparian strip is essential in preventing excessive uptake of Na+ into the plant via apoplastic bypass, with a barrier efficiency that is reflected by a sharp gradient in the steady-state radial distribution of apoplastic Na+ across the barrier. Even more significantly, this function cannot be replaced by the action of membrane transporters. The simulations also demonstrated that the positive effect of the Casparian strip of controlling Na+ uptake, was somewhat offset by its contribution to the osmotic stress component: a more effective barrier increased the detrimental osmotic stress effect. In contrast, the suberin lamellae were found to play a relatively minor, even non-essential, role in the overall response to salt stress, with the presence of the suberin lamellae resulting in only a slight reduction in Na+ uptake. However, perhaps more significantly, the simulations identified a possible role of suberin lamellae in reducing plant energy requirements by acting as a physical barrier to preventing the passive leakage of Na+ into endodermal cells. The model results suggest that more and particular experimental attention should be paid to the properties of the Casparian strip when assessing the salt tolerance of different plant varieties and species. Indeed, the Casparian strip appears to be a more promising target for plant breeding and plant genetic engineering efforts than the suberin lamellae for the goal of improving salt tolerance.
topic Casparian strip
suberin lamellae
salt tolerance
apoplastic and symplastic transport
osmotic stress
url http://journal.frontiersin.org/article/10.3389/fpls.2017.01326/full
work_keys_str_mv AT kyliejfoster acomprehensivebiophysicalmodelofionandwatertransportinplantrootsiclarifyingtherolesofendodermalbarriersinthesaltstressresponse
AT stanleyjmiklavcic acomprehensivebiophysicalmodelofionandwatertransportinplantrootsiclarifyingtherolesofendodermalbarriersinthesaltstressresponse
AT kyliejfoster comprehensivebiophysicalmodelofionandwatertransportinplantrootsiclarifyingtherolesofendodermalbarriersinthesaltstressresponse
AT stanleyjmiklavcic comprehensivebiophysicalmodelofionandwatertransportinplantrootsiclarifyingtherolesofendodermalbarriersinthesaltstressresponse
_version_ 1725393872698212352