Tree Response to Herbivory Is Affected by Endogenous Rhythmic Growth and Attenuated by Cotreatment With a Mycorrhizal Fungus

Abstract

Herbivores and mycorrhizal fungi interactively influence growth, resource utilization, and plant defense responses. We studied these interactions in a tritrophic system comprising Quercus robur, the herbivore Lymantria dispar, and the ectomycorrhizal fungus Piloderma croceum under controlled laboratory conditions at the levels of gene expression and carbon and nitrogen (C/N) allocation. Taking advantage of the endogenous rhythmic growth displayed by oak, we thereby compared gene transcript abundances and resource shifts during shoot growth with those during the alternating root growth flushes. During root flush, herbivore feeding on oak leaves led to an increased expression of genes related to plant growth and enriched gene ontology terms related to cell wall, DNA replication, and defense. C/N-allocation analyses indicated an increased export of resources from aboveground plant parts to belowground. Accordingly, the expression of genes related to the transport of carbohydrates increased upon herbivore attack in leaves during the root flush stage. Inoculation with an ectomycorrhizal fungus attenuated these effects but, instead, caused an increased expression of genes related to the production of volatile organic compounds. We conclude that oak defense response against herbivory is strong in root flush at the transcriptomic level but this response is strongly inhibited by inoculation with ectomycorrhizal fungi and it is extremely weak at shoot flush.

Local Responses and Systemic Induced Resistance Mediated by Ectomycorrhizal Fungi

“…These studies suggest that the resistance induced by EMF is context-dependent. This idea is also supported by recent transcriptome analyses showing that host defense gene expression of leaves can be diminished when the tree roots are colonized by EMF and depends on the specific host-EMF combination (Maboreke et al, 2016;Bacht et al, 2019;Bouffaud et al, 2020).…”

Ectomycorrhizal fungus supports endogenous rhythmic growth and corresponding resource allocation in oak during various below- and aboveground biotic interactions

“…5 . This includes interactions with the leaf herbivore Lymantria dispar and the root interacting springtail Protaphorura armata 17 , 18 . Data from oak beneficial organisms, i.e.…”

“…Collembola can also feed on EMF mycelium and inhibit EM formation 34 , but since the grazing may stimulate compensatory growth of the hyphae, mycelial biomass may not decrease but even increase due to moderate grazing 29 , 35 . Finally, some reports show that leaf herbivory inhibits EM formation 36 , 37 , but it may also speed up assimilate transport to roots 18 , 38 . In sum, this suggests that consumers cause changes in root growth and resource allocation, and affect the mycelium of the EMF and its interactions with fine roots.…”

“…Previous analyses of oak gene expression had been conducted with mycorrhiza helper 21 , root parasite 22 , springtail 17 , and leaf herbivore 18 . These analyses showed strong gene expression responses with > 1000 differentially expressed genes, with enriched GO terms in up-regulated genes for plant defence and stress, but enriched GO terms in down-regulated genes for depleted cell growth and cell proliferation.…”

“…By stable isotope labelling experiments it was shown that this leads to an increased 13 C and 15 N excess in aboveground plant compartments, and by gene expression analysis it was detected that the expression of growth related genes is triggered in leaves 17 . With the same methods it was shown that the aboveground herbivory by gypsy moth ( Lymantria dispar ) reduces 13 C and 15 N allocation to sink leaves, but enhances 15 N allocation to source leaves, accompanied by an enhanced expression of genes related to the transport of carbohydrates in leaves 18 . In contrast to the herbivores, mycorrhiza helper bacterium causes a complex, not entirely beneficial or detrimental response in the oak system.…”