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From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development

Nematode migration, feeding site formation, withdrawal of plant assimilates, and activation of plant defence responses have a significant impact on plant growth and development. Plants display intraspecific variation in tolerance limits for root-feeding nematodes. Although disease tolerance has been...

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Autores principales: Willig, Jaap-Jan, Sonneveld, Devon, van Steenbrugge, Joris J M, Deurhof, Laurens, van Schaik, Casper C, Teklu, Misghina G, Goverse, Aska, Lozano-Torres, Jose L, Smant, Geert, Sterken, Mark G
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10540735/
https://www.ncbi.nlm.nih.gov/pubmed/37432651
http://dx.doi.org/10.1093/jxb/erad266
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author Willig, Jaap-Jan
Sonneveld, Devon
van Steenbrugge, Joris J M
Deurhof, Laurens
van Schaik, Casper C
Teklu, Misghina G
Goverse, Aska
Lozano-Torres, Jose L
Smant, Geert
Sterken, Mark G
author_facet Willig, Jaap-Jan
Sonneveld, Devon
van Steenbrugge, Joris J M
Deurhof, Laurens
van Schaik, Casper C
Teklu, Misghina G
Goverse, Aska
Lozano-Torres, Jose L
Smant, Geert
Sterken, Mark G
author_sort Willig, Jaap-Jan
collection PubMed
description Nematode migration, feeding site formation, withdrawal of plant assimilates, and activation of plant defence responses have a significant impact on plant growth and development. Plants display intraspecific variation in tolerance limits for root-feeding nematodes. Although disease tolerance has been recognized as a distinct trait in biotic interactions of mainly crops, we lack mechanistic insights. Progress is hampered by difficulties in quantification and laborious screening methods. We turned to the model plant Arabidopsis thaliana, since it offers extensive resources to study the molecular and cellular mechanisms underlying nematode–plant interactions. Through imaging of tolerance-related parameters, the green canopy area was identified as an accessible and robust measure for assessing damage due to cyst nematode infection. Subsequently, a high-throughput phenotyping platform simultaneously measuring the green canopy area growth of 960 A. thaliana plants was developed. This platform can accurately measure cyst nematode and root-knot nematode tolerance limits in A. thaliana through classical modelling approaches. Furthermore, real-time monitoring provided data for a novel view of tolerance, identifying a compensatory growth response. These findings show that our phenotyping platform will enable a new mechanistic understanding of tolerance to below-ground biotic stress.
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spelling pubmed-105407352023-09-30 From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development Willig, Jaap-Jan Sonneveld, Devon van Steenbrugge, Joris J M Deurhof, Laurens van Schaik, Casper C Teklu, Misghina G Goverse, Aska Lozano-Torres, Jose L Smant, Geert Sterken, Mark G J Exp Bot Technical Innovation Nematode migration, feeding site formation, withdrawal of plant assimilates, and activation of plant defence responses have a significant impact on plant growth and development. Plants display intraspecific variation in tolerance limits for root-feeding nematodes. Although disease tolerance has been recognized as a distinct trait in biotic interactions of mainly crops, we lack mechanistic insights. Progress is hampered by difficulties in quantification and laborious screening methods. We turned to the model plant Arabidopsis thaliana, since it offers extensive resources to study the molecular and cellular mechanisms underlying nematode–plant interactions. Through imaging of tolerance-related parameters, the green canopy area was identified as an accessible and robust measure for assessing damage due to cyst nematode infection. Subsequently, a high-throughput phenotyping platform simultaneously measuring the green canopy area growth of 960 A. thaliana plants was developed. This platform can accurately measure cyst nematode and root-knot nematode tolerance limits in A. thaliana through classical modelling approaches. Furthermore, real-time monitoring provided data for a novel view of tolerance, identifying a compensatory growth response. These findings show that our phenotyping platform will enable a new mechanistic understanding of tolerance to below-ground biotic stress. Oxford University Press 2023-07-11 /pmc/articles/PMC10540735/ /pubmed/37432651 http://dx.doi.org/10.1093/jxb/erad266 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Technical Innovation
Willig, Jaap-Jan
Sonneveld, Devon
van Steenbrugge, Joris J M
Deurhof, Laurens
van Schaik, Casper C
Teklu, Misghina G
Goverse, Aska
Lozano-Torres, Jose L
Smant, Geert
Sterken, Mark G
From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title_full From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title_fullStr From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title_full_unstemmed From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title_short From root to shoot: quantifying nematode tolerance in Arabidopsis thaliana by high-throughput phenotyping of plant development
title_sort from root to shoot: quantifying nematode tolerance in arabidopsis thaliana by high-throughput phenotyping of plant development
topic Technical Innovation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10540735/
https://www.ncbi.nlm.nih.gov/pubmed/37432651
http://dx.doi.org/10.1093/jxb/erad266
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