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Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas

Climate forecasts show that in many regions the temporal distribution of precipitation events will become less predictable. Root traits may play key roles in dealing with changes in precipitation predictability, but their functional plastic responses, including transgenerational processes, are scarc...

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Autores principales: March-Salas, Martí, Scheepens, J. F., van Kleunen, Mark, Fitze, Patrick S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9703072/
https://www.ncbi.nlm.nih.gov/pubmed/36452110
http://dx.doi.org/10.3389/fpls.2022.998169
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author March-Salas, Martí
Scheepens, J. F.
van Kleunen, Mark
Fitze, Patrick S.
author_facet March-Salas, Martí
Scheepens, J. F.
van Kleunen, Mark
Fitze, Patrick S.
author_sort March-Salas, Martí
collection PubMed
description Climate forecasts show that in many regions the temporal distribution of precipitation events will become less predictable. Root traits may play key roles in dealing with changes in precipitation predictability, but their functional plastic responses, including transgenerational processes, are scarcely known. We investigated root trait plasticity of Papaver rhoeas with respect to higher versus lower intra-seasonal and inter-seasonal precipitation predictability (i.e., the degree of temporal autocorrelation among precipitation events) during a four-year outdoor multi-generation experiment. We first tested how the simulated predictability regimes affected intra-generational plasticity of root traits and allocation strategies of the ancestors, and investigated the selective forces acting on them. Second, we exposed three descendant generations to the same predictability regime experienced by their mothers or to a different one. We then investigated whether high inter-generational predictability causes root trait differentiation, whether transgenerational root plasticity existed and whether it was affected by the different predictability treatments. We found that the number of secondary roots, root biomass and root allocation strategies of ancestors were affected by changes in precipitation predictability, in line with intra-generational plasticity. Lower predictability induced a root response, possibly reflecting a fast-acquisitive strategy that increases water absorbance from shallow soil layers. Ancestors’ root traits were generally under selection, and the predictability treatments did neither affect the strength nor the direction of selection. Transgenerational effects were detected in root biomass and root weight ratio (RWR). In presence of lower predictability, descendants significantly reduced RWR compared to ancestors, leading to an increase in performance. This points to a change in root allocation in order to maintain or increase the descendants’ fitness. Moreover, transgenerational plasticity existed in maximum rooting depth and root biomass, and the less predictable treatment promoted the lowest coefficient of variation among descendants’ treatments in five out of six root traits. This shows that the level of maternal predictability determines the variation in the descendants’ responses, and suggests that lower phenotypic plasticity evolves in less predictable environments. Overall, our findings show that roots are functional plastic traits that rapidly respond to differences in precipitation predictability, and that the plasticity and adaptation of root traits may crucially determine how climate change will affect plants.
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spelling pubmed-97030722022-11-29 Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas March-Salas, Martí Scheepens, J. F. van Kleunen, Mark Fitze, Patrick S. Front Plant Sci Plant Science Climate forecasts show that in many regions the temporal distribution of precipitation events will become less predictable. Root traits may play key roles in dealing with changes in precipitation predictability, but their functional plastic responses, including transgenerational processes, are scarcely known. We investigated root trait plasticity of Papaver rhoeas with respect to higher versus lower intra-seasonal and inter-seasonal precipitation predictability (i.e., the degree of temporal autocorrelation among precipitation events) during a four-year outdoor multi-generation experiment. We first tested how the simulated predictability regimes affected intra-generational plasticity of root traits and allocation strategies of the ancestors, and investigated the selective forces acting on them. Second, we exposed three descendant generations to the same predictability regime experienced by their mothers or to a different one. We then investigated whether high inter-generational predictability causes root trait differentiation, whether transgenerational root plasticity existed and whether it was affected by the different predictability treatments. We found that the number of secondary roots, root biomass and root allocation strategies of ancestors were affected by changes in precipitation predictability, in line with intra-generational plasticity. Lower predictability induced a root response, possibly reflecting a fast-acquisitive strategy that increases water absorbance from shallow soil layers. Ancestors’ root traits were generally under selection, and the predictability treatments did neither affect the strength nor the direction of selection. Transgenerational effects were detected in root biomass and root weight ratio (RWR). In presence of lower predictability, descendants significantly reduced RWR compared to ancestors, leading to an increase in performance. This points to a change in root allocation in order to maintain or increase the descendants’ fitness. Moreover, transgenerational plasticity existed in maximum rooting depth and root biomass, and the less predictable treatment promoted the lowest coefficient of variation among descendants’ treatments in five out of six root traits. This shows that the level of maternal predictability determines the variation in the descendants’ responses, and suggests that lower phenotypic plasticity evolves in less predictable environments. Overall, our findings show that roots are functional plastic traits that rapidly respond to differences in precipitation predictability, and that the plasticity and adaptation of root traits may crucially determine how climate change will affect plants. Frontiers Media S.A. 2022-11-14 /pmc/articles/PMC9703072/ /pubmed/36452110 http://dx.doi.org/10.3389/fpls.2022.998169 Text en Copyright © 2022 March-Salas, Scheepens, van Kleunen and Fitze https://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
March-Salas, Martí
Scheepens, J. F.
van Kleunen, Mark
Fitze, Patrick S.
Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title_full Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title_fullStr Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title_full_unstemmed Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title_short Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas
title_sort precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of papaver rhoeas
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9703072/
https://www.ncbi.nlm.nih.gov/pubmed/36452110
http://dx.doi.org/10.3389/fpls.2022.998169
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