Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects.

Christoph Brütting,Ian T Baldwin,Martin Schäfer,Cristina Maria Crava,Meredith C Schuman,Nora Adam,Stefan Meldau

doi:10.7554/elife.36268

Abstract

Endophytic insects provide the textbook examples of herbivores that manipulate their host plant's physiology, putatively altering source/sink relationships by transferring cytokinins (CK) to create 'green islands' that increase the nutritional value of infested tissues. However, unambiguous demonstrations of CK transfer are lacking. Here we show that feeding by the free-living herbivore Tupiocoris notatus on Nicotiana attenuata is characterized by stable nutrient levels, increased CK levels and alterations in CK-related transcript levels in attacked leaves, in striking similarity to endophytic insects. Using 15N-isotope labeling, we demonstrate that the CK N6-isopentenyladenine (IP) is transferred from insects to plants via their oral secretions. In the field, T. notatus preferentially attacks leaves with transgenically increased CK levels; plants with abrogated CK-perception are less tolerant of T. notatus feeding damage. We infer that this free-living insect uses CKs to manipulate source/sink relationships to increase food quality and minimize the fitness consequences of its feeding.

Highlights

Insect herbivores are under constant pressure from their host plants: they must adapt to toxic or anti-digestive defense compounds whose levels often dramatically increase in response to insect feeding; and their food source has low nitrogen to carbon ratios and a dietary value which decreases as leaves mature and senesce
T. notatus feeding elevated the levels of jasmonic acid (JA), its precursor cis-(+)À12-oxophytodienoic acid (OPDA) and its bioactive isoleucine conjugate (JA-Ile) (Figure 1f–h)
JA and JA-Ile levels triggered by T. notatus feeding remained elevated for up to six days when mirids were confined to feed on a single leaf (Figure 1—figure supplement 1a–c)

Summary

Introduction

Insect herbivores are under constant pressure from their host plants: they must adapt to toxic or anti-digestive defense compounds whose levels often dramatically increase in response to insect feeding; and their food source has low nitrogen to carbon ratios and a dietary value which decreases as leaves mature and senesce. Some herbivorous insects have developed strategies to overcome the low nutritional contents of their host plants and have evolved specialized mechanisms to tolerate, or even co-opt toxic plant defense metabolites for their own uses, in an apparent evolutionary arms race (Strong et al, 1984; Despres et al, 2007; Heckel, 2014). Phytophagous insects can be categorized as either endophytic or free-living depending on the relationships that they establish with their host plant. This distinction is not binary and many transitional forms exist even within the same taxa. Free-living insects are mobile on their host plants, moving among plants, and frequently among different plant species.

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