Aboveground phytochemical responses to belowground herbivory in poplar trees and the consequence for leaf herbivore preference

Sandra Lackner,Tobias G Köllner,Nathalie D Lackus,Sybille B Unsicker,Christian Paetz

doi:10.1111/pce.13628

Sandra Lackner, Tobias G Köllner + Show 3 more

Open Access

https://doi.org/10.1111/pce.13628

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Abstract

Belowground (BG) herbivory can influence aboveground (AG) herbivore performance and food preference via changes in plant chemistry. Most evidence for this phenomenon derives from studies in herbaceous plants but studies in woody plants are scarce. Here we investigated whether and how BG herbivory on black poplar (Populus nigra) trees by Melolontha melolontha larvae influences the feeding preference of Lymantria dispar (gypsy moth) caterpillars. In a food choice assay, caterpillars preferred to feed on leaves from trees that had experienced attack by BG herbivores. Therefore, we investigated the effect of BG herbivory on the phytochemical composition of P. nigra trees alone and in combination with AG feeding by L. dispar caterpillars. BG herbivory did not increase systemic AG tree defences like volatile organic compounds, protease inhibitors and salicinoids. Jasmonates and salicylic acid were also not induced by BG herbivory in leaves but abscisic acid concentrations drastically increased together with proline and few other amino acids. Leaf coating experiments with amino acids suggest that proline might be responsible for the caterpillar feeding preference via presumptive phagostimulatory properties. This study shows that BG herbivory in poplar can modify the feeding preference of AG herbivores via phytochemical changes as a consequence of root-to-shoot signaling.

Highlights

The role of belowground (BG) herbivory for aboveground (AG) plant defence chemistry and associated effects on insect herbivores and higher trophic levels has gained increasing attention
In a food choice assay, L. dispar caterpillars preferred to feed on leaf discs from P. nigra trees that were previously infested BG with a M. melolontha larva over discs from non‐damaged control trees (Mann– Whitney U test: U = 4.021 p ≤ 0.001, Figure 1a)
To understand the molecular mechanisms underlying the preference of L. dispar caterpillars for black poplar leaves from BG infested trees, we characterized and compared the leaf phytochemistry including volatile emission, protease inhibitor activity and salicinoid accumulation in uninfested trees, in trees infested either BG with one M. melolontha larva or AG with L. dispar caterpillars, and in trees infested with both herbivores

Summary

| INTRODUCTION

The role of belowground (BG) herbivory for aboveground (AG) plant defence chemistry and associated effects on insect herbivores and higher trophic levels has gained increasing attention (reviewed by Bezemer & van Dam, 2005; van Dam, 2009; van Dam & Heil, 2011). An increase in plant defence hormones following root herbivory can lead to the production of secondary metabolites such as glucosinolates, benzoxazinoids, phenolics and alkaloids in systemic AG tissues (Papadopoulou & van Dam, 2016 and references therein). This defence induction can affect the preference and performance of AG herbivores (Brown & Gange, 1990; Poveda, Steffan‐ Dewenter, Scheu, & Tscharntke, 2003; Rasmann & Turlings, 2007). We measured volatile organic compounds, salicinoids, protease inhibitor activity, defence hormones, free sugars and free amino acids to elucidate which of these primary and secondary metabolites could be responsible for caterpillar food preference. A food choice assay in which we offered leaf discs of undamaged trees, that were either coated or uncoated with different amino acids, to L. dispar caterpillars suggests, that the originally observed preference for leaves of BG infested trees is most likely due to higher proline concentrations

| MATERIAL AND METHODS

| RESULTS AND DISCUSSION

| CONCLUSION