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Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics

Soil detritivores such as Collembola impact plant growth, tissue nutrient concentration and gene expression. Using a model system with pedunculate oak (Quercus robur) microcuttings that display a typical endogenous rhythmic growth with alternating shoot (SF) and root flushes (RF), we investigated th...

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Autores principales: Graf, Marcel, Bönn, Markus, Feldhahn, Lasse, Kurth, Florence, Grams, Thorsten E. E., Herrmann, Sylvie, Tarkka, Mika, Buscot, Francois, Scheu, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6458381/
https://www.ncbi.nlm.nih.gov/pubmed/31032040
http://dx.doi.org/10.1098/rsos.181869
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author Graf, Marcel
Bönn, Markus
Feldhahn, Lasse
Kurth, Florence
Grams, Thorsten E. E.
Herrmann, Sylvie
Tarkka, Mika
Buscot, Francois
Scheu, Stefan
author_facet Graf, Marcel
Bönn, Markus
Feldhahn, Lasse
Kurth, Florence
Grams, Thorsten E. E.
Herrmann, Sylvie
Tarkka, Mika
Buscot, Francois
Scheu, Stefan
author_sort Graf, Marcel
collection PubMed
description Soil detritivores such as Collembola impact plant growth, tissue nutrient concentration and gene expression. Using a model system with pedunculate oak (Quercus robur) microcuttings that display a typical endogenous rhythmic growth with alternating shoot (SF) and root flushes (RF), we investigated the transcriptomic response of oak with and without mycorrhiza (Piloderma croceum) to the presence of Collembola (Protaphorura armata), and linked it to changes in resource allocation by pulse labelling the plants with (13)C and (15)N. Collembola impacted Gene Ontology (GO) terms as well as plant morphology and elemental ratios with the effects varying markedly with developmental phases. During SF Collembola increased GO terms related to primary growth and this was mirrored in increased (13)C and (15)N excess in aboveground plant compartments. During RF, Collembola increased GO terms related to plant secondary metabolism and physical fortification. Further, Collembola presence resulted in an increase in plant defence-related GO terms suggesting that Collembola in the rhizosphere prime oak shoots against the attack by fungi or herbivores. Notably, the impact of Collembola on growth, resource allocation and oak gene expression was modified by presence of P. croceum. The results indicate that oaks clearly react to the presence of Collembola in the rhizosphere and respond in a complex way by changing the expression of genes of both primary and secondary metabolism, and this resulted in concomitant changes in plant morphology and physiology.
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spelling pubmed-64583812019-04-26 Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics Graf, Marcel Bönn, Markus Feldhahn, Lasse Kurth, Florence Grams, Thorsten E. E. Herrmann, Sylvie Tarkka, Mika Buscot, Francois Scheu, Stefan R Soc Open Sci Biology (Whole Organism) Soil detritivores such as Collembola impact plant growth, tissue nutrient concentration and gene expression. Using a model system with pedunculate oak (Quercus robur) microcuttings that display a typical endogenous rhythmic growth with alternating shoot (SF) and root flushes (RF), we investigated the transcriptomic response of oak with and without mycorrhiza (Piloderma croceum) to the presence of Collembola (Protaphorura armata), and linked it to changes in resource allocation by pulse labelling the plants with (13)C and (15)N. Collembola impacted Gene Ontology (GO) terms as well as plant morphology and elemental ratios with the effects varying markedly with developmental phases. During SF Collembola increased GO terms related to primary growth and this was mirrored in increased (13)C and (15)N excess in aboveground plant compartments. During RF, Collembola increased GO terms related to plant secondary metabolism and physical fortification. Further, Collembola presence resulted in an increase in plant defence-related GO terms suggesting that Collembola in the rhizosphere prime oak shoots against the attack by fungi or herbivores. Notably, the impact of Collembola on growth, resource allocation and oak gene expression was modified by presence of P. croceum. The results indicate that oaks clearly react to the presence of Collembola in the rhizosphere and respond in a complex way by changing the expression of genes of both primary and secondary metabolism, and this resulted in concomitant changes in plant morphology and physiology. The Royal Society 2019-03-06 /pmc/articles/PMC6458381/ /pubmed/31032040 http://dx.doi.org/10.1098/rsos.181869 Text en © 2019 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Biology (Whole Organism)
Graf, Marcel
Bönn, Markus
Feldhahn, Lasse
Kurth, Florence
Grams, Thorsten E. E.
Herrmann, Sylvie
Tarkka, Mika
Buscot, Francois
Scheu, Stefan
Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title_full Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title_fullStr Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title_full_unstemmed Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title_short Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics
title_sort collembola interact with mycorrhizal fungi in modifying oak morphology, c and n incorporation and transcriptomics
topic Biology (Whole Organism)
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6458381/
https://www.ncbi.nlm.nih.gov/pubmed/31032040
http://dx.doi.org/10.1098/rsos.181869
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