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Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

BACKGROUND: Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is particularly relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. Previous studies of the wild to...

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Autores principales: He, Jun, Halitschke, Rayko, Schuman, Meredith C., Baldwin, Ian T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8404343/
https://www.ncbi.nlm.nih.gov/pubmed/34461825
http://dx.doi.org/10.1186/s12870-021-03179-z
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author He, Jun
Halitschke, Rayko
Schuman, Meredith C.
Baldwin, Ian T.
author_facet He, Jun
Halitschke, Rayko
Schuman, Meredith C.
Baldwin, Ian T.
author_sort He, Jun
collection PubMed
description BACKGROUND: Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is particularly relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. Previous studies of the wild tobacco N. attenuata have found associations between the diurnal timing of volatile emissions, and daytime predation of herbivores by their natural enemies. RESULTS: Here, we investigated the role of light in regulating two biosynthetic groups of volatiles, terpenoids and green leaf volatiles (GLVs), which dominate the herbivore-induced bouquet of N. attenuata. Light deprivation strongly suppressed terpenoid emissions while enhancing GLV emissions, albeit with a time lag. Silencing the expression of photoreceptor genes did not alter terpenoid emission rhythms, but silencing expression of the phytochrome gene, NaPhyB1, disordered the emission of the GLV (Z)-3-hexenyl acetate. External abscisic acid (ABA) treatments increased stomatal resistance, but did not truncate the emission of terpenoid volatiles (recovered in the headspace). However, ABA treatment enhanced GLV emissions and leaf internal pools (recovered from tissue), and reduced internal linalool pools. In contrast to the pattern of diurnal terpenoid emissions and nocturnal GLV emissions, transcripts of herbivore-induced plant volatile (HIPV) biosynthetic genes peaked during the day. The promotor regions of these genes were populated with various cis-acting regulatory elements involved in light-, stress-, phytohormone- and circadian regulation. CONCLUSIONS: This research provides insights into the complexity of the mechanisms involved in the regulation of HIPV bouquets, a mechanistic complexity which rivals the functional complexity of HIPVs, which includes repelling herbivores, calling for body guards, and attracting pollinators. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03179-z.
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spelling pubmed-84043432021-08-31 Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco He, Jun Halitschke, Rayko Schuman, Meredith C. Baldwin, Ian T. BMC Plant Biol Research BACKGROUND: Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is particularly relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. Previous studies of the wild tobacco N. attenuata have found associations between the diurnal timing of volatile emissions, and daytime predation of herbivores by their natural enemies. RESULTS: Here, we investigated the role of light in regulating two biosynthetic groups of volatiles, terpenoids and green leaf volatiles (GLVs), which dominate the herbivore-induced bouquet of N. attenuata. Light deprivation strongly suppressed terpenoid emissions while enhancing GLV emissions, albeit with a time lag. Silencing the expression of photoreceptor genes did not alter terpenoid emission rhythms, but silencing expression of the phytochrome gene, NaPhyB1, disordered the emission of the GLV (Z)-3-hexenyl acetate. External abscisic acid (ABA) treatments increased stomatal resistance, but did not truncate the emission of terpenoid volatiles (recovered in the headspace). However, ABA treatment enhanced GLV emissions and leaf internal pools (recovered from tissue), and reduced internal linalool pools. In contrast to the pattern of diurnal terpenoid emissions and nocturnal GLV emissions, transcripts of herbivore-induced plant volatile (HIPV) biosynthetic genes peaked during the day. The promotor regions of these genes were populated with various cis-acting regulatory elements involved in light-, stress-, phytohormone- and circadian regulation. CONCLUSIONS: This research provides insights into the complexity of the mechanisms involved in the regulation of HIPV bouquets, a mechanistic complexity which rivals the functional complexity of HIPVs, which includes repelling herbivores, calling for body guards, and attracting pollinators. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03179-z. BioMed Central 2021-08-30 /pmc/articles/PMC8404343/ /pubmed/34461825 http://dx.doi.org/10.1186/s12870-021-03179-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
He, Jun
Halitschke, Rayko
Schuman, Meredith C.
Baldwin, Ian T.
Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title_full Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title_fullStr Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title_full_unstemmed Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title_short Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
title_sort light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8404343/
https://www.ncbi.nlm.nih.gov/pubmed/34461825
http://dx.doi.org/10.1186/s12870-021-03179-z
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