Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana

The physiological mechanisms by which plants limit the growth of bacterial pathogens during gene-for-gene resistance are poorly understood. We characterized early events in the Arabidopsis thaliana–Pseudomonas syringae pathosystem to identify physiological changes for which the kinetics are consiste...

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Main Authors: Brian C. Freeman, Gwyn A. Beattie
Format: Article
Language:English
Published: The American Phytopathological Society 2009-07-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-22-7-0857
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author Brian C. Freeman
Gwyn A. Beattie
author_facet Brian C. Freeman
Gwyn A. Beattie
author_sort Brian C. Freeman
collection DOAJ
description The physiological mechanisms by which plants limit the growth of bacterial pathogens during gene-for-gene resistance are poorly understood. We characterized early events in the Arabidopsis thaliana–Pseudomonas syringae pathosystem to identify physiological changes for which the kinetics are consistent with bacterial growth restriction. Using a safranine-O dye solution to detect vascular activity, we demonstrated that A. thaliana Col-0 resistance to P. syringae pv. tomato DC3000 cells expressing avrRpm1 involved virtually complete cessation of vascular water movement into the infection site within only 3 h postinoculation (hpi), under the conditions tested. This vascular restriction preceded or was simultaneous with precipitous decreases in photosynthesis, stomatal conductance, and leaf transpiration, with the latter two remaining at detectable levels. Microscopic plant cell death was detected as early as 2 hpi. Interestingly, suppression of bacterial growth during AvrRpm1-mediated resistance was eliminated by physically blocking leaf water loss through the stomata without altering plant cell death and was nearly eliminated by incubating plants at high relative humidity. The majority of the population growth benefit from blocking leaf water loss occurred early after inoculation, i.e., between 4 and 8 hpi. Collectively, these results support a model in which A. thaliana suppresses P. syringae growth during gene-for-gene resistance, at least in part, by coupling restricted vascular flow to the infection site with water loss through partially open stomata; that is, the plants effectively starve the invading bacteria for water.
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spelling doaj.art-13fd3cadfefd41d49e5c580428c066922022-12-22T03:18:26ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062009-07-0122785786710.1094/MPMI-22-7-0857Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thalianaBrian C. FreemanGwyn A. BeattieThe physiological mechanisms by which plants limit the growth of bacterial pathogens during gene-for-gene resistance are poorly understood. We characterized early events in the Arabidopsis thaliana–Pseudomonas syringae pathosystem to identify physiological changes for which the kinetics are consistent with bacterial growth restriction. Using a safranine-O dye solution to detect vascular activity, we demonstrated that A. thaliana Col-0 resistance to P. syringae pv. tomato DC3000 cells expressing avrRpm1 involved virtually complete cessation of vascular water movement into the infection site within only 3 h postinoculation (hpi), under the conditions tested. This vascular restriction preceded or was simultaneous with precipitous decreases in photosynthesis, stomatal conductance, and leaf transpiration, with the latter two remaining at detectable levels. Microscopic plant cell death was detected as early as 2 hpi. Interestingly, suppression of bacterial growth during AvrRpm1-mediated resistance was eliminated by physically blocking leaf water loss through the stomata without altering plant cell death and was nearly eliminated by incubating plants at high relative humidity. The majority of the population growth benefit from blocking leaf water loss occurred early after inoculation, i.e., between 4 and 8 hpi. Collectively, these results support a model in which A. thaliana suppresses P. syringae growth during gene-for-gene resistance, at least in part, by coupling restricted vascular flow to the infection site with water loss through partially open stomata; that is, the plants effectively starve the invading bacteria for water.https://apsjournals.apsnet.org/doi/10.1094/MPMI-22-7-0857
spellingShingle Brian C. Freeman
Gwyn A. Beattie
Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
Molecular Plant-Microbe Interactions
title Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
title_full Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
title_fullStr Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
title_full_unstemmed Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
title_short Bacterial Growth Restriction During Host Resistance to Pseudomonas syringae Is Associated with Leaf Water Loss and Localized Cessation of Vascular Activity in Arabidopsis thaliana
title_sort bacterial growth restriction during host resistance to pseudomonas syringae is associated with leaf water loss and localized cessation of vascular activity in arabidopsis thaliana
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-22-7-0857
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