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Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions

BACKGROUND AND AIMS: The ability to avoid drought-induced embolisms in the xylem is one of the essential traits for plants to survive periods of water shortage. Over the past three decades, hydraulic studies have been focusing on trees, which limits our ability to understand how herbs tolerate droug...

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Autores principales: Thonglim, Ajaree, Delzon, Sylvain, Larter, Maximilian, Karami, Omid, Rahimi, Arezoo, Offringa, Remko, Keurentjes, Joost J B, Balazadeh, Salma, Smets, Erik, Lens, Frederic
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8324034/
https://www.ncbi.nlm.nih.gov/pubmed/33216143
http://dx.doi.org/10.1093/aob/mcaa196
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author Thonglim, Ajaree
Delzon, Sylvain
Larter, Maximilian
Karami, Omid
Rahimi, Arezoo
Offringa, Remko
Keurentjes, Joost J B
Balazadeh, Salma
Smets, Erik
Lens, Frederic
author_facet Thonglim, Ajaree
Delzon, Sylvain
Larter, Maximilian
Karami, Omid
Rahimi, Arezoo
Offringa, Remko
Keurentjes, Joost J B
Balazadeh, Salma
Smets, Erik
Lens, Frederic
author_sort Thonglim, Ajaree
collection PubMed
description BACKGROUND AND AIMS: The ability to avoid drought-induced embolisms in the xylem is one of the essential traits for plants to survive periods of water shortage. Over the past three decades, hydraulic studies have been focusing on trees, which limits our ability to understand how herbs tolerate drought. Here we investigate the embolism resistance in inflorescence stems of four Arabidopsis thaliana accessions that differ in growth form and drought response. We assess functional traits underlying the variation in embolism resistance amongst the accessions studied using detailed anatomical observations. METHODS: Vulnerability to xylem embolism was evaluated via vulnerability curves using the centrifuge technique and linked with detailed anatomical observations in stems using light microscopy and transmission electron microscopy. KEY RESULTS: The data show significant differences in stem P(50,) varying 2-fold from −1.58 MPa in the Cape Verde Island accession to −3.07 MPa in the woody soc1 ful double mutant. Out of all the anatomical traits measured, intervessel pit membrane thickness (T(PM)) best explains the differences in P(50), as well as P(12) and P(88). The association between embolism resistance and T(PM) can be functionally explained by the air-seeding hypothesis. There is no evidence that the correlation between increased woodiness and increased embolism resistance is directly related to functional aspects. However, we found that increased woodiness is strongly linked to other lignification characters, explaining why mechanical stem reinforcement is indirectly related to increased embolism resistance. CONCLUSIONS: The woodier or more lignified accessions are more resistant to embolism than the herbaceous accessions, confirming the link between increased stem lignification and increased embolism resistance, as also observed in other lineages. Intervessel pit membrane thickness and, to a lesser extent, theoretical vessel implosion resistance and vessel wall thickness are the missing functional links between stem lignification and embolism resistance.
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spelling pubmed-83240342021-08-02 Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions Thonglim, Ajaree Delzon, Sylvain Larter, Maximilian Karami, Omid Rahimi, Arezoo Offringa, Remko Keurentjes, Joost J B Balazadeh, Salma Smets, Erik Lens, Frederic Ann Bot Original Articles BACKGROUND AND AIMS: The ability to avoid drought-induced embolisms in the xylem is one of the essential traits for plants to survive periods of water shortage. Over the past three decades, hydraulic studies have been focusing on trees, which limits our ability to understand how herbs tolerate drought. Here we investigate the embolism resistance in inflorescence stems of four Arabidopsis thaliana accessions that differ in growth form and drought response. We assess functional traits underlying the variation in embolism resistance amongst the accessions studied using detailed anatomical observations. METHODS: Vulnerability to xylem embolism was evaluated via vulnerability curves using the centrifuge technique and linked with detailed anatomical observations in stems using light microscopy and transmission electron microscopy. KEY RESULTS: The data show significant differences in stem P(50,) varying 2-fold from −1.58 MPa in the Cape Verde Island accession to −3.07 MPa in the woody soc1 ful double mutant. Out of all the anatomical traits measured, intervessel pit membrane thickness (T(PM)) best explains the differences in P(50), as well as P(12) and P(88). The association between embolism resistance and T(PM) can be functionally explained by the air-seeding hypothesis. There is no evidence that the correlation between increased woodiness and increased embolism resistance is directly related to functional aspects. However, we found that increased woodiness is strongly linked to other lignification characters, explaining why mechanical stem reinforcement is indirectly related to increased embolism resistance. CONCLUSIONS: The woodier or more lignified accessions are more resistant to embolism than the herbaceous accessions, confirming the link between increased stem lignification and increased embolism resistance, as also observed in other lineages. Intervessel pit membrane thickness and, to a lesser extent, theoretical vessel implosion resistance and vessel wall thickness are the missing functional links between stem lignification and embolism resistance. Oxford University Press 2020-11-20 /pmc/articles/PMC8324034/ /pubmed/33216143 http://dx.doi.org/10.1093/aob/mcaa196 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (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 Original Articles
Thonglim, Ajaree
Delzon, Sylvain
Larter, Maximilian
Karami, Omid
Rahimi, Arezoo
Offringa, Remko
Keurentjes, Joost J B
Balazadeh, Salma
Smets, Erik
Lens, Frederic
Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title_full Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title_fullStr Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title_full_unstemmed Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title_short Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions
title_sort intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of arabidopsis thaliana accessions
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8324034/
https://www.ncbi.nlm.nih.gov/pubmed/33216143
http://dx.doi.org/10.1093/aob/mcaa196
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