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Aphid Herbivory Drives Asymmetry in Carbon for Nutrient Exchange between Plants and an Arbuscular Mycorrhizal Fungus.

ABSTRACT: Associations formed between plants and arbuscular mycorrhizal (AM) fungi are characterized by the bi-directional exchange of fungal-acquired soil nutrients for plant-fixed organic carbon compounds. Mycorrhizal-acquired nutrient assimilation by plants may be symmetrically linked to carbon (C) transfer from plant to fungus or governed by sink-source dynamics. Abiotic factors, including atmospheric CO2 concentration ([CO2]), can affect the relative cost of resources traded between mutualists, thereby influencing symbiotic function. Whether biotic factors, such as insect herbivores that represent external sinks for plant C, impact mycorrhizal function remains unstudied. By supplying 33P to an AM fungus (Rhizophagus irregularis) and 14CO2 to wheat, we tested the impact of increasing C sink strength (i.e., aphid herbivory) and increasing C source strength (i.e., elevated [CO2]) on resource exchange between mycorrhizal symbionts. Allocation of plant C to the AM fungus decreased dramatically following exposure to the bird cherry-oat aphid (Rhopalosiphum padi), with high [CO2] failing to alleviate the aphid-induced decline in plant C allocated to the AM fungus. Mycorrhizal-mediated uptake of 33P by plants was maintained regardless of aphid presence or elevated [CO2], meaning insect herbivory drove asymmetry in carbon for nutrient exchange between symbionts. Here, we provide direct evidence that external biotic C sinks can limit plant C allocation to an AM fungus without hindering mycorrhizal-acquired nutrient uptake. Our findings highlight the context dependency of resource exchange between plants and AM fungi and suggest biotic factors-individually and in combination with abiotic factors-should be considered as powerful regulators of symbiotic function.

SUBMITTER: Charters MD

PROVIDER: S-EPMC7237887 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Aphid Herbivory Drives Asymmetry in Carbon for Nutrient Exchange between Plants and an Arbuscular Mycorrhizal Fungus.

Charters Michael D MD Sait Steven M SM Field Katie J KJ

Current biology : CB 20200409 10

Associations formed between plants and arbuscular mycorrhizal (AM) fungi are characterized by the bi-directional exchange of fungal-acquired soil nutrients for plant-fixed organic carbon compounds. Mycorrhizal-acquired nutrient assimilation by plants may be symmetrically linked to carbon (C) transfer from plant to fungus or governed by sink-source dynamics. Abiotic factors, including atmospheric CO<sub>2</sub> concentration ([CO<sub>2</sub>]), can affect the relative cost of resources traded bet ...[more]

PMID: 32275877

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Project description:IntroductionThe hyphosphere of arbuscular mycorrhizal (AM) fungi is teeming with microbial life. Yet, the influence of nutrient availability or nutrient forms on the hyphosphere microbiomes is still poorly understood.MethodsHere, we examined how the microbial community (prokaryotic, fungal, protistan) was affected by the presence of the AM fungus Rhizophagus irregularis in the rhizosphere and the root-free zone, and how different nitrogen (N) and phosphorus (P) supplements into the root-free compartment influenced the communities.ResultsThe presence of AM fungus greatly affected microbial communities both in the rhizosphere and the root-free zone, with prokaryotic communities being affected the most. Protists were the only group of microbes whose richness and diversity were significantly reduced by the presence of the AM fungus. Our results showed that the type of nutrients AM fungi encounter in localized patches modulate the structure of hyphosphere microbial communities. In contrast we did not observe any effects of the AM fungus on (non-mycorrhizal) fungal community composition. Compared to the non-mycorrhizal control, the root-free zone with the AM fungus (i.e., the AM fungal hyphosphere) was enriched with Alphaproteobacteria, some micropredatory and copiotroph bacterial taxa (e.g., Xanthomonadaceae and Bacteroidota), and the poorly characterized and not yet cultured Acidobacteriota subgroup GP17, especially when phytate was added. Ammonia-oxidizing Nitrosomonas and nitrite-oxidizing Nitrospira were significantly suppressed in the presence of the AM fungus in the root-free compartment, especially upon addition of inorganic N. Co-occurrence network analyses revealed that microbial communities in the root-free compartment were complex and interconnected with more keystone species when AM fungus was present, especially when the root-free compartment was amended with phytate.ConclusionOur study showed that the form of nutrients is an important driver of prokaryotic and eukaryotic community assembly in the AM fungal hyphosphere, despite the assumed presence of a stable and specific AM fungal hyphoplane microbiome. Predictable responses of specific microbial taxa will open the possibility of using them as co-inoculants with AM fungi, e.g., to improve crop performance.

Project description:Roots of most terrestrial plants form symbiotic associations (mycorrhiza) with soil- borne arbuscular mycorrhizal fungi (AMF). Many studies show that mycorrhizal colonization enhances plant resistance against pathogenic fungi. However, the mechanism of mycorrhiza-induced disease resistance remains equivocal. In this study, we found that mycorrhizal inoculation with AMF Funneliformis mosseae significantly alleviated tomato (Solanum lycopersicum Mill.) early blight disease caused by Alternaria solani Sorauer. AMF pre-inoculation led to significant increases in activities of β-1,3-glucanase, chitinase, phenylalanine ammonia-lyase (PAL) and lipoxygenase (LOX) in tomato leaves upon pathogen inoculation. Mycorrhizal inoculation alone did not influence the transcripts of most genes tested. However, pathogen attack on AMF-inoculated plants provoked strong defense responses of three genes encoding pathogenesis-related proteins, PR1, PR2, and PR3, as well as defense-related genes LOX, AOC, and PAL, in tomato leaves. The induction of defense responses in AMF pre-inoculated plants was much higher and more rapid than that in un-inoculated plants in present of pathogen infection. Three tomato genotypes: a Castlemart wild-type (WT) plant, a jasmonate (JA) biosynthesis mutant (spr2), and a prosystemin-overexpressing 35S::PS plant were used to examine the role of the JA signaling pathway in AMF-primed disease defense. Pathogen infection on mycorrhizal 35S::PS plants led to higher induction of defense-related genes and enzymes relative to WT plants. However, pathogen infection did not induce these genes and enzymes in mycorrhizal spr2 mutant plants. Bioassays showed that 35S::PS plants were more resistant and spr2 plants were more susceptible to early blight compared with WT plants. Our finding indicates that mycorrhizal colonization enhances tomato resistance to early blight by priming systemic defense response, and the JA signaling pathway is essential for mycorrhiza-primed disease resistance.

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Aphid Herbivory Drives Asymmetry in Carbon for Nutrient Exchange between Plants and an Arbuscular Mycorrhizal Fungus.

Publications

Aphid Herbivory Drives Asymmetry in Carbon for Nutrient Exchange between Plants and an Arbuscular Mycorrhizal Fungus.

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