Functional insect-induced stomata

Epidermal leaf peels show Vitis leaves are hypostomatal, having no stomata on the adaxial side (A), but gall formation generates stomata in increasing density at closer proximity to the gall (out of picture Lower Right; B). Abaxial tissue without or adjacent to galls have similar stomata patterning (Table 1).

 

Leaf-galling Phylloxera on grapes reprograms host metabolism and morphology

by Nabity P. D., Haus M. J., Berenbaum M. R., DeLucia E. H. (2013)

Paul D. Nabity, Miranda J. Haus, May R. Berenbaum, Evan H. DeLucia,

=====

in PNAS 2013 October, 110 (41) 16663-16668 – https://doi.org/10.1073/pnas.1220219110 – 

http://www.pnas.org/content/110/41/16663.full

Graphical representation of the transcriptional shift from autotrophic to heterotrophic metabolism within a gall cell, for inter- and intracellular metabolic processes (glycolysis, fermentation, respiration) and the corresponding downstream transcriptional shift in secondary metabolism. Each orange or blue box represents a unique differentially expressed transcript encoding a protein/enzyme. Green boxes represent metabolites, yellow boxes represent metabolites specifically involved in cell wall synthesis, and pink boxes represent processes. The blue arrow links the up-regulation of glycolysis with corresponding downstream secondary metabolic processes, whereas the orange arrow links the down-regulation of Calvin cycle products with reduced transcript abundance of its corresponding secondary metabolic processes.

Significance

Some herbivorous insects induce galls, abnormal structures, in their host plants, benefiting the gall-forming parasite by providing nutritive tissue. The gall-forming insect phylloxera induces stomata, openings through which plants regulate water and CO₂, on the upper surface of grape leaves where they typically do not occur. Carbon uptake and transpiration by induced stomata facilitate nutrient acquisition by gall tissue and phylloxera. Moreover, gall formation reprograms the host-leaf transcriptome to increase transcripts associated with sucrose mobilization and glycolysis and decrease defense-related transcripts. Thus, stomata induction by phylloxera reconfigures leaves to increase carbon gain, to partially offset negative impacts of gall formation.

Abstract

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.