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Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers

Flowers are critical for angiosperm reproduction and the production of food, fiber, and pharmaceuticals, yet for unknown reasons, they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a...

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Autores principales: Carins-Murphy, Madeline R, Cochard, Hervé, Deans, Ross M, Gracie, Alistair J, Brodribb, Timothy J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469517/
https://www.ncbi.nlm.nih.gov/pubmed/37325893
http://dx.doi.org/10.1093/plphys/kiad349
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author Carins-Murphy, Madeline R
Cochard, Hervé
Deans, Ross M
Gracie, Alistair J
Brodribb, Timothy J
author_facet Carins-Murphy, Madeline R
Cochard, Hervé
Deans, Ross M
Gracie, Alistair J
Brodribb, Timothy J
author_sort Carins-Murphy, Madeline R
collection PubMed
description Flowers are critical for angiosperm reproduction and the production of food, fiber, and pharmaceuticals, yet for unknown reasons, they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a vascular system that has a low capacity to supply water and is prone to failure under water stress. These characteristics may render reproductive structures more susceptible than leaves to runaway cavitation—an uncontrolled feedback cycle between rising water stress and declining water transport efficiency that can rapidly lead to lethal tissue desiccation. We provide modeling and empirical evidence to demonstrate that flower damage in the perennial crop pyrethrum (Tanacetum cinerariifolium), in the form of irreversible desiccation, corresponds with runaway cavitation in the flowering stem after a combination of heat and water stress. We show that tissue damage is linked to greater evaporative demand during high temperatures rather than direct thermal stress. High floral transpiration dramatically reduced the soil water deficit at which runaway cavitation was triggered in pyrethrum flowering stems. Identifying runaway cavitation as a mechanism leading to heat damage and reproductive losses in pyrethrum provides different avenues for process-based modeling to understand the impact of climate change on cultivated and natural plant systems. This framework allows future investigation of the relative susceptibility of diverse plant species to reproductive failure under hot and dry conditions.
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spelling pubmed-104695172023-09-01 Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers Carins-Murphy, Madeline R Cochard, Hervé Deans, Ross M Gracie, Alistair J Brodribb, Timothy J Plant Physiol Research Article Flowers are critical for angiosperm reproduction and the production of food, fiber, and pharmaceuticals, yet for unknown reasons, they appear particularly sensitive to combined heat and drought stress. A possible explanation for this may be the co-occurrence of leaky cuticles in flower petals and a vascular system that has a low capacity to supply water and is prone to failure under water stress. These characteristics may render reproductive structures more susceptible than leaves to runaway cavitation—an uncontrolled feedback cycle between rising water stress and declining water transport efficiency that can rapidly lead to lethal tissue desiccation. We provide modeling and empirical evidence to demonstrate that flower damage in the perennial crop pyrethrum (Tanacetum cinerariifolium), in the form of irreversible desiccation, corresponds with runaway cavitation in the flowering stem after a combination of heat and water stress. We show that tissue damage is linked to greater evaporative demand during high temperatures rather than direct thermal stress. High floral transpiration dramatically reduced the soil water deficit at which runaway cavitation was triggered in pyrethrum flowering stems. Identifying runaway cavitation as a mechanism leading to heat damage and reproductive losses in pyrethrum provides different avenues for process-based modeling to understand the impact of climate change on cultivated and natural plant systems. This framework allows future investigation of the relative susceptibility of diverse plant species to reproductive failure under hot and dry conditions. Oxford University Press 2023-06-16 /pmc/articles/PMC10469517/ /pubmed/37325893 http://dx.doi.org/10.1093/plphys/kiad349 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. 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 Research Article
Carins-Murphy, Madeline R
Cochard, Hervé
Deans, Ross M
Gracie, Alistair J
Brodribb, Timothy J
Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title_full Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title_fullStr Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title_full_unstemmed Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title_short Combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
title_sort combined heat and water stress leads to local xylem failure and tissue damage in pyrethrum flowers
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469517/
https://www.ncbi.nlm.nih.gov/pubmed/37325893
http://dx.doi.org/10.1093/plphys/kiad349
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