Modulation of plant cytokinin levels in the Wolbachia‐free leaf‐mining species Phyllonorycter mespilella

Abstract

As phytohormones lie at the very core of molecular mechanisms controlling the plant physiology and development, they have long been hypothesized to be involved in insect-induced plant manipulations. Cytokinins (CKs) are phytohormones now widely recognized to be utilized by leaf-mining and gall-inducing insects in the control of the physiology of their host plant. In some leaf-mining moth species, larvae can supply the hormones themselves, bacterial symbionts contributing to the production of CKs. Our objective was to investigate whether closely related leaf-miner species sharing the same ecological niche but differing in their Wolbachia infection status develop similar strategies to manipulate their host plant. An extensive identification and quantification of CKs has been used to elucidate physiological patterns relevant for the plant-insect interactions. Our results show that modulation of plant CK levels is impaired in the Wolbachia-free leaf-mining moth Phyllonorycter mespilella (H€ ubner) (Lepidoptera: Gracillariidae) contrasting with results previously observed in the closely related moth species Phyllonorycter blancardella (Fabricius) that produce and deliver CKs to the plant through an intricate interaction with Wolbachia. Our study suggests that mechanisms underlying colonization of the host plant and adaptation to fluctuating environmental conditions are different between the two leaf-miner species and that P. mespilella larvae most likely do not produce CKs. This species rather only buffers the degradation of CKs naturally occurring during the senescence of leaves leading to few active CKs being maintained at a sufficiently high level to induce and maintain a 'green island' phenotype (photosynthetically active green patches in otherwise senescing leaves). This study further provides converging experimental evidence pointing toward the influence of bacterial symbionts in the ability of leaf-mining moths to control the physiology of their host plant with consequences for their ecology and evolutionary diversification.

Role of Cytokinins for Interactions of Plants With Microbial Pathogens and Pest Insects

“…The detailed analyses of movement and source of CKs participated in plant feeding by leaf-mining insects has revealed that the insect symbiotic bacteria Wolbachia is inherently involved . This complicated plant-insect-microbe interaction is essential and the modulation of plant CK levels was shown to be impaired in the Wolbachia-free leaf feeding moth (Zhang et al, 2018).…”

Cytokinins Are Abundant and Widespread among Insect Species

“…By covering gall, we mean the plant tissue that envelopes the gall-inducing organism. Among fungi and insects that encounter senescing plant tissues, some species appear to employ CKs to induce yellowing plant tissues to "stay green" by the process of forming "green islands"-areas of photosynthetically active tissues in which the pathogenic organism can continue to feed and develop [17,[51][52][53][54][55][56][57]. In some instances, CKs have been shown to convert the site of attack into a mobilizing sink to which sugars are translocated where they may contribute to gall induction or just for the sustenance of the manipulating organism [18,28,45,[58][59][60].…”

“…The earliest studies used bioassays to confirm the presence of CKs in insects [66][67][68][69][70]. Since then, researchers have used either ELISA [52,54,55], or analytical chemistry [15][16][17]19,44,46,47,49,50,57], to estimate the concentrations of CKs in insects.…”

Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes

“…CKs also accumulate to high levels in mined tissues, despite low levels of plant CK-related gene expression. Very large amounts of CKs have also been found in many leaf-mining insects, including the leaf-mining moths Phyllonorycter mespilella and Phyllonorycter blancardella (Lepidoptera), and the production of these hormones by the insect may be linked to the presence of bacterial endosymbionts (75,144,146).…”