Leaf-galling phylloxera on grapes reprograms host metabolism and morphology

Endoparasitism by gall-forming insects dramatically alters the plant phenotype by altering growth patterns and modifying plant organs in ways that appear to directly benefit the gall former. Because these morphological and physiological changes are linked to the presence of the insect, the induced phenotype is said to function as an extension of the parasite, albeit by unknown mechanisms. Here we report the gall-forming aphid-like parasite phylloxera, Daktulosphaira vitifoliae, induces stomata on the adaxial surface of grape leaves where stomata typically do not occur. We characterized the function of the phylloxera-induced stomata by tracing transport of assimilated carbon. Because induction of stomata suggests a significant manipulation of primary metabolism, we also characterized the gall transcriptome to infer the level of global reconfiguration of primary metabolism and the subsequent changes in downstream secondary metabolism. Phylloxera feeding induced stomata formation in proximity to the insect and promoted the assimilation and importation of carbon into the gall. Gene expression related to water, nutrient, and mineral transport; glycolysis; and fermentation increased in leaf-gall tissues. This shift from an autotrophic to a heterotrophic profile occurred concurrently with decreased gene expression for nonmevalonate and terpenoid synthesis and increased gene expression in shikimate and phenylpropanoid biosynthesis, secondary metabolite systems that alter defense status in grapes. These functional insect-induced stomata thus comprise part of an extended phenotype, whereby D. vitifoliae globally reprograms grape leaf development to alter patterns of primary metabolism, nutrient mobilization, and defense investment in favor of the galling habit.