The role of plant labile carbohydrates and nitrogen on wheat-aphid relations\xa0

Victor Sadras,Elisa Garzo,Sonia Medina,Aránzazu Moreno,Alberto Fereres,Julian Taylor,Carolina Vázquez

doi:10.1038/s41598-021-91424-8

Abstract

Interactions between plants and herbivores are key drivers of evolution and ecosystem complexity. We investigated the role of plant labile carbohydrates and nitrogen on wheat-aphid relations in a 22 factorial combining [CO2] and nitrogen supply. We measured life history traits (assay 1) and feeding behaviour (assay 2) of bird-cherry oat aphid (Rhopalosiphum padi L.) and English grain aphid (Sitobion avenae F.) forced to feed on single leaf laminae, and reproduction of R. padi in a setting where insects moved freely along the plant (assay 3). Experimental setting impacted aphid traits. Where aphids were constrained to single leaf, high nitrogen reduced their fitness and discouraged phloem feeding. Where aphids could move throughout the plant, high nitrogen enhanced their reproduction. Aphid responses to the interaction between nitrogen and [CO2] varied with experimental setting. The number of R. padi adults varied tenfold with plant growing conditions and correlated negatively with molar concentration of sugars in stem (assay 3). This finding has two implications. First, the common interpretation that high nitrogen favours insect fitness because protein-rich animal bodies have to build from nitrogen-poor plant food needs expanding to account for the conspicuous association between low nitrogen and high concentration of labile carbohydrates in plant, which can cause osmotic stress in aphids. Second, the function of labile carbohydrates buffering grain growth needs expanding to account for the osmotic role of carbohydrates in plant resistance to aphids.

Highlights

Interactions between plants and herbivores are key drivers of evolution and ecosystem complexity
At 21 days after sowing (DAS), we recorded treatment effects for the first time: leaves were longer under high nitrogen (p = 0.0032, s = 8.3) and high [ CO2] (p = 0.0007, s = 10.5), with no interaction between nitrogen and [CO2] (p = 0.70, s = 0.5) (Fig. 1A)
High nitrogen supply was detrimental for both aphid species in assays 1 and 2, where insects were forced to feed on single leaf laminae (Figs. 4 and 6)

Summary

Introduction

Interactions between plants and herbivores are key drivers of evolution and ecosystem complexity. The number of R. padi adults varied tenfold with plant growing conditions and correlated negatively with molar concentration of sugars in stem (assay 3). The common interpretation that high nitrogen favours insect fitness because protein-rich animal bodies have to build from nitrogen-poor plant food needs expanding to account for the conspicuous association between low nitrogen and high concentration of labile carbohydrates in plant, which can cause osmotic stress in aphids. The impact of elevated [CO2] interacting with temperature or nitrogen on insects, mediated by changes in plant phenotype, cannot be deduced from the effects of the individual factors[13,14]. Rhopalosiphum padi and Sitobion avenae, the focus of this study, are common pests of wheat worldwide with distinct niches whereby R. padi prefers the stem and basal leaves whilst S. avenae prefers the upper leaves and e ars[19]

Methods

Results

Discussion

Conclusion