Impacts of aphid herbivory on mycorrhizal growth responses across three cultivars of wheat

Abstract

Societal Impact StatementThe Earth's population is projected to rise to 9.7 billion by 2050 resulting in mounting pressure to increase agricultural yields in a sustainable manner. Arbuscular mycorrhizal (AM) fungi may be important players in this agricultural transition given their capacity to improve soil and plant health. Benefits gained by crops hosting AM fungi can be cultivar-specific and also affected by insect herbivory, although the combined effect of these factors remains unclear. Here, we show that, in an economically and socially significant tri-partite system, there is interplay between crop cultivar, AM colonisation and aphid herbivory on plant growth and nutritional status. Summary• Arbuscular mycorrhizal (AM) fungi are critical components of the rhizosphere across nearly all terrestrial biomes. AM fungi associate with most plants, including major crops, usually increasing plant access to soil nutrients and enhancing defence against pests and pathogens in return for photosynthetic carbon (C).

Aboveground herbivory does not affect mycorrhiza-dependent nitrogen acquisition from soil but inhibits mycorrhizal network-mediated nitrogen interplant transfer in maize

“…These results are similar to the conclusion by Charters et al. that aboveground aphid infestation does not affect plant mycorrhiza-dependent P uptake ( Charters et al., 2020 ; Charters et al., 2022 ) but differs from that of Frew ( Frew and Price, 2019 ; Frew, 2021 ). The variability of these results highlights that host plant–AMF symbiosis and nutrient transfer might be influenced by a range of specific environmental factors, such as host and fungal species, the degree of stress or soil nutrient status ( Barto and Rillig, 2010 ).…”

“…However, the results of 15 N tracer experiments showed that this fraction of N uptake from soil solution by ERM was not affected by aboveground herbivory (Figures 3C, D, S7). These results are similar to the conclusion by Charters et al that aboveground aphid infestation does not affect plant mycorrhiza-dependent P uptake (Charters et al, 2020;Charters et al, 2022) but differs from that of Frew (Frew and Price, 2019;Frew, 2021). The variability of these results highlights that host plant-AMF symbiosis and nutrient transfer might be influenced by a range of specific environmental factors, such as host and fungal species, the…”

“…In this study, aboveground herbivory slightly inhibited mycorrhizal colonization in maize plants ( Figure 3B ). Other studies have shown that aboveground herbivory can either increase, decrease or have no effect on mycorrhizal colonization ( Charters et al., 2020 ; Frew, 2021 ; Charters et al., 2022 ). The well-established symbiotic relationship underlays plant mycorrhiza-dependent mineral nutrient uptake, so that reduced colonization caused by aboveground herbivory might, to some extent, affect N uptake by mycorrhizal maize from soil solutions via ERM.…”

“…This report demonstrated that nutrient exchange between AMF and host plants can be quantified in the presence of exogenous sap-sucking herbivores ( Merckx and Gomes, 2020 ). In addition, AMF colonization and AMF-mediated plant growth responses are not affected by aphid feeding or by N or P uptake ( Charters et al., 2022 ). The different effects of aboveground herbivory on mycorrhizae-mediated mineral nutrient uptake may be related to herbivorous types, AMF or plant species.…”

A snapshot of the transcriptome ofMedicago truncatula(Fabales: Fabaceae) shoots and roots in response to an arbuscular mycorrhizal fungus and the pea aphid (Acyrthosiphon pisum) (Hemiptera: Aphididae)

“…In tripartite interactions, AM fungi and aphids can impact each other via their shared host plant, and a wide range of aphid responses have been reported after feeding on mycorrhizal plants. In most cases, aphids benefit by feeding on mycorrhizal plants (Gange et al 1999, 2002, Babikova et al 2014, Gilbert and Johnson 2015, Simon et al 2017, Tomczak and Müller 2017, Maurya et al 2018, Wilkinson et al 2019, Stallmann and Schweiger 2021), but negative (Guerrieri et al 2004, Gehring and Bennett 2009, Babikova et al 2013, Gilbert and Johnson 2015, Garzo et al 2018, Maurya et al 2018, Stallmann and Schweiger 2021, Du et al 2022) or no impacts (Gehring and Bennett 2009, Rizzo et al 2020, Charters et al 2022) on aphids have also been observed. Aphids are pertinent to study because they extract photoassimilates, transmit viruses, and secrete salivary compounds that manipulate plant defense signaling for their own benefit (Edwards and Singh 2006, Hogenhout and Bos 2011, Pitino and Hogenhout 2013, Mondal 2017).…”