Cargando…

Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense

In addition to directly inducing physical and chemical defenses, herbivory experienced by plants in one generation can influence the expression of defensive traits in offspring. Plant defense phenotypes can be compromised by inbreeding, and there is some evidence that such adverse effects can extend...

Descripción completa

Detalles Bibliográficos
Autores principales: Nihranz, Chad T., Helms, Anjel M., Tooker, John F., Mescher, Mark C., De Moraes, Consuelo M., Stephenson, Andrew G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9595541/
https://www.ncbi.nlm.nih.gov/pubmed/36282832
http://dx.doi.org/10.1371/journal.pone.0274920
_version_ 1784815675827552256
author Nihranz, Chad T.
Helms, Anjel M.
Tooker, John F.
Mescher, Mark C.
De Moraes, Consuelo M.
Stephenson, Andrew G.
author_facet Nihranz, Chad T.
Helms, Anjel M.
Tooker, John F.
Mescher, Mark C.
De Moraes, Consuelo M.
Stephenson, Andrew G.
author_sort Nihranz, Chad T.
collection PubMed
description In addition to directly inducing physical and chemical defenses, herbivory experienced by plants in one generation can influence the expression of defensive traits in offspring. Plant defense phenotypes can be compromised by inbreeding, and there is some evidence that such adverse effects can extend to the transgenerational expression of induced resistance. We explored how the inbreeding status of maternal Solanum carolinense plants influenced the transgenerational effects of herbivory on the defensive traits and herbivore resistance of offspring. Manduca sexta caterpillars were used to damage inbred and outbred S. carolinense maternal plants and cross pollinations were performed to produced seeds from herbivore-damaged and undamaged, inbred and outbred maternal plants. Seeds were grown in the greenhouse to assess offspring defense-related traits (i.e., leaf trichomes, internode spines, volatile organic compounds) and resistance to herbivores. We found that feeding by M. sexta caterpillars on maternal plants had a positive influence on trichome and spine production in offspring and that caterpillar development on offspring of herbivore-damaged maternal plants was delayed relative to that on offspring of undamaged plants. Offspring of inbred maternal plants had reduced spine production, compared to those of outbred maternal plants, and caterpillars performed better on the offspring of inbred plants. Both herbivory and inbreeding in the maternal generation altered volatile emissions of offspring. In general, maternal plant inbreeding dampened transgenerational effects of herbivory on offspring defensive traits and herbivore resistance. Taken together, this study demonstrates that inducible defenses in S. carolinense can persist across generations and that inbreeding compromises transgenerational resistance in S. carolinense.
format Online
Article
Text
id pubmed-9595541
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-95955412022-10-26 Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense Nihranz, Chad T. Helms, Anjel M. Tooker, John F. Mescher, Mark C. De Moraes, Consuelo M. Stephenson, Andrew G. PLoS One Research Article In addition to directly inducing physical and chemical defenses, herbivory experienced by plants in one generation can influence the expression of defensive traits in offspring. Plant defense phenotypes can be compromised by inbreeding, and there is some evidence that such adverse effects can extend to the transgenerational expression of induced resistance. We explored how the inbreeding status of maternal Solanum carolinense plants influenced the transgenerational effects of herbivory on the defensive traits and herbivore resistance of offspring. Manduca sexta caterpillars were used to damage inbred and outbred S. carolinense maternal plants and cross pollinations were performed to produced seeds from herbivore-damaged and undamaged, inbred and outbred maternal plants. Seeds were grown in the greenhouse to assess offspring defense-related traits (i.e., leaf trichomes, internode spines, volatile organic compounds) and resistance to herbivores. We found that feeding by M. sexta caterpillars on maternal plants had a positive influence on trichome and spine production in offspring and that caterpillar development on offspring of herbivore-damaged maternal plants was delayed relative to that on offspring of undamaged plants. Offspring of inbred maternal plants had reduced spine production, compared to those of outbred maternal plants, and caterpillars performed better on the offspring of inbred plants. Both herbivory and inbreeding in the maternal generation altered volatile emissions of offspring. In general, maternal plant inbreeding dampened transgenerational effects of herbivory on offspring defensive traits and herbivore resistance. Taken together, this study demonstrates that inducible defenses in S. carolinense can persist across generations and that inbreeding compromises transgenerational resistance in S. carolinense. Public Library of Science 2022-10-25 /pmc/articles/PMC9595541/ /pubmed/36282832 http://dx.doi.org/10.1371/journal.pone.0274920 Text en © 2022 Nihranz et al 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 use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Nihranz, Chad T.
Helms, Anjel M.
Tooker, John F.
Mescher, Mark C.
De Moraes, Consuelo M.
Stephenson, Andrew G.
Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title_full Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title_fullStr Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title_full_unstemmed Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title_short Adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in Solanum carolinense
title_sort adverse effects of inbreeding on the transgenerational expression of herbivore-induced defense traits in solanum carolinense
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9595541/
https://www.ncbi.nlm.nih.gov/pubmed/36282832
http://dx.doi.org/10.1371/journal.pone.0274920
work_keys_str_mv AT nihranzchadt adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense
AT helmsanjelm adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense
AT tookerjohnf adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense
AT meschermarkc adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense
AT demoraesconsuelom adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense
AT stephensonandrewg adverseeffectsofinbreedingonthetransgenerationalexpressionofherbivoreinduceddefensetraitsinsolanumcarolinense