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Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis
Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance traits to their progeny. However, the evolutionary and ecological significance of transgenerational induced resistance (t-IR) is poorly understood because a clear understanding of how parents i...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952753/ https://www.ncbi.nlm.nih.gov/pubmed/33719325 http://dx.doi.org/10.3389/fpls.2021.644999 |
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author | López Sánchez, Ana Pascual-Pardo, David Furci, Leonardo Roberts, Michael R. Ton, Jurriaan |
author_facet | López Sánchez, Ana Pascual-Pardo, David Furci, Leonardo Roberts, Michael R. Ton, Jurriaan |
author_sort | López Sánchez, Ana |
collection | PubMed |
description | Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance traits to their progeny. However, the evolutionary and ecological significance of transgenerational induced resistance (t-IR) is poorly understood because a clear understanding of how parents interpret environmental cues in relation to the effectiveness, stability, and anticipated ecological costs of t-IR is lacking. Here, we have used a full factorial design to study the specificity, costs, and transgenerational stability of t-IR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and salinity. We show that t-IR in response to infection by biotrophic or necrotrophic pathogens is effective against pathogens of the same lifestyle. This pathogen-mediated t-IR is associated with ecological costs, since progeny from biotroph-infected parents were more susceptible to both necrotrophic pathogens and salt stress, whereas progeny from necrotroph-infected parents were more susceptible to biotrophic pathogens. Hence, pathogen-mediated t-IR provides benefits when parents and progeny are in matched environments but is associated with costs that become apparent in mismatched environments. By contrast, soil salinity failed to mediate t-IR against salt stress in matched environments but caused non-specific t-IR against both biotrophic and necrotrophic pathogens in mismatched environments. However, the ecological relevance of this non-specific t-IR response remains questionable as its induction was offset by major reproductive costs arising from dramatically reduced seed production and viability. Finally, we show that the costs and transgenerational stability of pathogen-mediated t-IR are proportional to disease pressure experienced by the parents, suggesting that plants use disease severity as an environmental proxy to adjust investment in t-IR. |
format | Online Article Text |
id | pubmed-7952753 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-79527532021-03-13 Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis López Sánchez, Ana Pascual-Pardo, David Furci, Leonardo Roberts, Michael R. Ton, Jurriaan Front Plant Sci Plant Science Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance traits to their progeny. However, the evolutionary and ecological significance of transgenerational induced resistance (t-IR) is poorly understood because a clear understanding of how parents interpret environmental cues in relation to the effectiveness, stability, and anticipated ecological costs of t-IR is lacking. Here, we have used a full factorial design to study the specificity, costs, and transgenerational stability of t-IR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and salinity. We show that t-IR in response to infection by biotrophic or necrotrophic pathogens is effective against pathogens of the same lifestyle. This pathogen-mediated t-IR is associated with ecological costs, since progeny from biotroph-infected parents were more susceptible to both necrotrophic pathogens and salt stress, whereas progeny from necrotroph-infected parents were more susceptible to biotrophic pathogens. Hence, pathogen-mediated t-IR provides benefits when parents and progeny are in matched environments but is associated with costs that become apparent in mismatched environments. By contrast, soil salinity failed to mediate t-IR against salt stress in matched environments but caused non-specific t-IR against both biotrophic and necrotrophic pathogens in mismatched environments. However, the ecological relevance of this non-specific t-IR response remains questionable as its induction was offset by major reproductive costs arising from dramatically reduced seed production and viability. Finally, we show that the costs and transgenerational stability of pathogen-mediated t-IR are proportional to disease pressure experienced by the parents, suggesting that plants use disease severity as an environmental proxy to adjust investment in t-IR. Frontiers Media S.A. 2021-02-26 /pmc/articles/PMC7952753/ /pubmed/33719325 http://dx.doi.org/10.3389/fpls.2021.644999 Text en Copyright © 2021 López Sánchez, Pascual-Pardo, Furci, Roberts and Ton. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science López Sánchez, Ana Pascual-Pardo, David Furci, Leonardo Roberts, Michael R. Ton, Jurriaan Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title | Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title_full | Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title_fullStr | Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title_full_unstemmed | Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title_short | Costs and Benefits of Transgenerational Induced Resistance in Arabidopsis |
title_sort | costs and benefits of transgenerational induced resistance in arabidopsis |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7952753/ https://www.ncbi.nlm.nih.gov/pubmed/33719325 http://dx.doi.org/10.3389/fpls.2021.644999 |
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