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

Michael D Charters,Steven M Sait,Katie J Field

doi:10.1016/j.cub.2020.02.087

Abstract

SummaryAssociations 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.

Highlights

More than 80% of land plants associate with arbuscular mycorrhizal (AM) fungi [1], forming mycorrhizal associations in plants with roots and mycorrhiza-like associations in plants without roots [2]
AM colonization can increase the C sink strength of roots compared to their non-mycorrhizal counterparts [9], with plant hosts supplying AM fungi with up to 30% of their carbon fixed through photosynthesis [10] as sugars and/or lipids [11]
We investigated the effect of manipulating the source and sink strengths of plant C resources on carbon for nutrient exchange between wheat and a cooperative [18], widely distributed AM fungus (Rhizophagus irregularis) [32], which both have economic, ecological, and societal relevance

Summary

Introduction

More than 80% of land plants associate with arbuscular mycorrhizal (AM) fungi [1], forming mycorrhizal associations in plants with roots and mycorrhiza-like associations in plants without roots [2]. These intimate symbioses are ancient, dating back to the origins of land plants [3], and are usually considered to be mutualistic. AM colonization can increase the C sink strength of roots compared to their non-mycorrhizal counterparts [9], with plant hosts supplying AM fungi with up to 30% of their carbon fixed through photosynthesis [10] as sugars and/or lipids [11]. [CO2] can be a powerful environmental variable affecting plant C source strength for AM fungi

Methods

Findings

Discussion

Conclusion