Cytokinin-mediated leaf manipulation by a leafminer caterpillar

Abstract

A large number of hypotheses have been proposed to explain the adaptive significance and evolution of the endophagous-feeding mode, nutritional benefits being considered to be one of the main advantages. Leaf-mining insects should feed on most nutritional tissues and avoid tissues with high structural and/or biochemical plant defences. This selective feeding behaviour could furthermore be reinforced by manipulating the plant physiology, as suggested by the autumnal formation of 'green islands' around mining caterpillars in yellow leaves. The question we address here is how such metabolic manipulation occurs and what the nutritional consequences for the insect are. We report a large accumulation of cytokinins in the mined tissues which is responsible for the preservation of functional nutrient-rich green tissues at a time when leaves are otherwise turning yellow. The analogy with other plant manipulating organisms, in particular galling insects, is striking.

Are dominant plant species more susceptible to leaf‐mining insects? A case study at Saihanwula Nature Reserve, China

“…In an interesting manner, some leaf‐mining larvae remain alive in the green islands on the dry or fallen leaves of some deciduous trees in Saihanwula. This provides the larvae with enough food to complete their life cycle before winter (Giron, Kaiser, Imbault, & Casas, 2007; Kaiser, Huguet, Casas, Commin, & Giron, 2010; Liu et al., 2015). …”

Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment

“…A clear example of a CK-induced phenotype is the formation, after pathogen or insect attack, of spectacular green and metabolically active areas in otherwise yellow senescent leaves known as 'green-islands' (Engelbrecht et al 1969;Giron et al 2007;Kaiser et al 2010;Walters and McRoberts 2006;Walters et al 2008). In these islands, nutrientsmainly sugars -are redirected towards the infection site where host cell death is delayed.…”

“…Strategies adopted by a biotic invader that increase the "longevity" of leaves and create a favorable nutritional environment are thus expected to have crucial fitness consequences. This is particularly true for leaf-mining herbivorous insects that strictly rely on deciduous leaf resources for growth, development, and reproduction (Giron et al 2007;Kaiser et al 2010). While senescent autumnal leaves represent a poor and declining source of nutrients, the 'green-islands' induced by leaf-miners enable the insect to fulfill its nutritional requirement and to survive under adverse conditions (unpublished results).…”

“…While senescent autumnal leaves represent a poor and declining source of nutrients, the 'green-islands' induced by leaf-miners enable the insect to fulfill its nutritional requirement and to survive under adverse conditions (unpublished results). It also allows the insect to win a race against time and hence the completion of a supplementary generation (Engelbrecht et al 1969;Giron et al 2007;Kaiser et al 2010).…”

“…For the phytophagous leaf-mining moth Phyllonorycter blancardella, these 'green-islands' are characterized by an increased concentration in CKs leading to a favorable enriched nutritional environment due to an accurate CKmediated control of the overall sugar content (Giron et al 2007;Kaiser et al 2010;unpublished results). The moth relies on bacterial endosymbionts, most likely Wolbachia, to control the physiology of its host plant through manipulation of CK levels, thus increasing its fitness.…”