Aphids can acquire the nitrogen delivered to plants by arbuscular mycorrhizal fungi

Abstract

Above‐ and below‐ground organisms can interact by altering the quality of shared host plants. Arbuscular mycorrhizal fungi (AMF) influence plant nutrient uptake, including nitrogen (N) acquisition. Under low N and phosphorus conditions, AMF delivery of N from organic sources not immediately available to the plant can have large impacts on plant N status, a limiting nutrient in the aphid diet. This study investigated the effect of AMF colonisation upon aphid number and determined the consequences of AMF directly accessing an organic nutrient patch that the plant cannot. We hypothesised that AMF colonisation of plants will increase plant and aphid N status, plant performance and aphid number, but only when the AMF had direct access to the added organic patch. Barley plants hosting the grain aphid Sitobion avenae were colonised by the AMF, Funneliformis mosseae, or no AMF. A two‐compartment microcosm was used to separate the plant roots from a 15N‐labelled organic patch in a second compartment. AMF‐colonised plants, but without access to the second compartment, were used to examine the effect of AMF colonisation on aphid number. In a separate treatment, and to determine whether AMF access to a plant inaccessible N source modified the effect of AMF colonisation on aphid number, AMF hyphae were permitted access to the second compartment containing an organic patch. As a control for AMF accessing a larger substrate volume, AMF were allowed access to a second compartment without an organic patch. When the AMF accessed the organic patch, more N from the patch was delivered to the plant resulting in a higher grain N concentration although plant growth was depressed. More N from the patch was also delivered to the aphids, but the N status of the aphid remained unchanged. Regardless of the level of access to the organic patch, AMF colonisation did not affect aphid number. Our data show that by accessing N sources not readily available to plants, AMF can indirectly deliver N to above‐ground organisms, a finding which has major implications for N‐transfer between higher trophic levels. A plain language summary is available for this article.

Effect of Different Combinations of Phosphorus and Nitrogen Fertilization on Arbuscular Mycorrhizal Fungi and Aphids in Wheat

“…Previous studies on the effects of soil nutrients on insects reported that N enhances the population density of aphids because nitrogen in plants induces more amino acids [ 71 ], which positively affect aphids [ 72 ], and our results in this study are in line with these previous findings. Wilkinson et al (2019) reported that AMF can deliver N from organic sources to the plant, but has no effect on aphid number [ 73 ]. The reason may be that there are more secondary metabolites in plants with high AMF colonization [ 74 ], such as flavonoids and phenolics, which could provide strong resistance against aphids [ 75 , 76 , 77 ].…”

Is it time to include legumes in plant silicon research?

“…NanoSIMS (Nanoscale Secondary Ion Mass Spectrometry), for example, may be particularly useful for detecting silicon quantitatively (Nuñez, Renslow, Cliff, & Anderton, 2017) in legume tissues, including measuring silicon deposition inside root nodules. Fourth, to understand whether silicon influences the carbon and nitrogen exchange in legume–rhizobia symbioses, exogenous addition of isotopic labelling of 15 N and 13 C could be applied to measure how much of the externally supplied labelled nitrogen and carbon end up in the host and in the nodules respectively (see the technique in Wilkinson, Ferrari, Hartley, & Hodge, 2019).…”

The Role of Plant-Associated Microbes in Mediating Host-Plant Selection by Insect Herbivores

“…Beneficial microbes often alter plant growth or pest resistance traits that affect the performance and preference of insect herbivores. Microbes, like rhizobia or AMF, that increase plant nutrient acquisition, can also increase the nutritional quality of these plants for insect herbivores [29,30]. Moreover, the aptly named PGPR and fungi that enhance plant growth can provide greater amounts of available food resources for insect herbivores [31].…”