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Aphid infestation in the phyllosphere affects primary metabolic profiles in the arbuscular mycorrhizal hyphosphere.

ABSTRACT: While effects of (a)biotic stress events in the phyllosphere have been studied intensively, possible influences of stress on the arbuscular mycorrhizal hyphosphere has scarcely been investigated. We hypothesised that stress challenge in the phyllosphere could alter primary metabolite profiles of the hyphosphere - the mycelial network connecting plants. Donor plants, connected to receiver plants by mycelial networks, were aphid-challenged during 84?h. Primary metabolite profiles in the hyphosphere were investigated. Gene-expression of plant defence gene PR1 was measured in one of the receiver plants during the challenge. Hexose levels in the hyphosphere increased when donor plants were aphid-challenged. This change in metabolic profile was influenced by leaf sampling from receiver plant. PR1 expression increased in donor plants 48?h after challenge, and consequently 60?h after, in receiver plants. We conclude that aphid infestation of donor plants modified primary carbon metabolism in the hyphosphere. Plant defence response in receiver plants, occurred 12?h after detection of response in the aphid-challenged donor plants. While this work is the first to reveal primary metabolic profiles of the AM hyphosphere, more work is needed to elucidate the possible role of transient changes of hexose metabolism in stress response and signalling processes in the hyphosphere of connected plants.

SUBMITTER: Cabral C

PROVIDER: S-EPMC6160425 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Aphid infestation in the phyllosphere affects primary metabolic profiles in the arbuscular mycorrhizal hyphosphere.

Cabral Carmina C Wollenweber Bernd B António Carla C Rodrigues Ana Margarida AM Ravnskov Sabine S

Scientific reports 20180927 1

While effects of (a)biotic stress events in the phyllosphere have been studied intensively, possible influences of stress on the arbuscular mycorrhizal hyphosphere has scarcely been investigated. We hypothesised that stress challenge in the phyllosphere could alter primary metabolite profiles of the hyphosphere - the mycelial network connecting plants. Donor plants, connected to receiver plants by mycelial networks, were aphid-challenged during 84 h. Primary metabolite profiles in the hyphospher ...[more]

PMID: 30262837

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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:IntroductionFitness of plants is affected by their symbiotic interactions with arbuscular mycorrhizal fungi (AMF), and such effects are highly dependent on the environmental context.MethodsIn the current study, we inoculated the nursery shrub species Artemisia ordosica with AMF species Funneliformis mosseae under contrasting levels of soil water and nutrients (diammonium phosphate fertilization), to assess their effects on plant growth, physiology and natural infestation by herbivores.ResultsOverall, plant biomass was synergistically enhanced by increasing soil water and soil nutrient levels. However, plant height was surprisingly repressed by AMF inoculation, but only under low water conditions. Similarly, plant biomass was also reduced by AMF but only under low water and nutrient conditions. Furthermore, AMF significantly reduced leaf phosphorus levels, that were strongly enhanced under high nutrient conditions, but had only minor effects on leaf chlorophyll and proline levels. Under low water and nutrient conditions, specific root length was enhanced, but average root diameter was decreased by AMF inoculation. The negative effects of AMF on plant growth at low water and nutrient levels may indicate that under these conditions AMF inoculation does not strongly contribute to nutrient and water acquisition. On the contrary, the AMF might have suppressed the direct pathway of water and nutrient absorption by the plant roots themselves despite low levels of mycorrhizal colonization. AMF inoculation reduced the abundance of the foliar herbivore Chrysolina aeruginosa on plants that had been grown on the low nutrient soil, but not on high nutrient soil. Fertilization enhanced the abundance of this herbivore but only in plants that had received the high water treatment. The lower abundance of the herbivore on AMF plants could be related to their decreased leaf P content. In conclusion, our results indicate that AMF negatively affect the growth of Artemisia ordosica but makes them less attractive to a dominant herbivore.DiscussionOur study highlights that plant responses to AMF depend not only on the environmental context, but that the direction of the responses can differ for different components of plant performance (growth vs. defense).

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Aphid infestation in the phyllosphere affects primary metabolic profiles in the arbuscular mycorrhizal hyphosphere.

Publications

Aphid infestation in the phyllosphere affects primary metabolic profiles in the arbuscular mycorrhizal hyphosphere.

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