Cynipid wasps systematically reprogram host metabolism and restructure cell walls in developing galls

Abstract

Many insects have evolved the ability to manipulate plant growth to generate extraordinary structures called galls in which insect larva can develop while being sheltered within and feeding on the plant. In particular, Cynipid (Hymenoptera: Cynipidae) wasps have evolved to form some of the most morphologically complex galls known and generate an astonishing array of gall shapes, colors, and sizes. However, the biochemical basis underlying these remarkable cellular and developmental transformations remains poorly understood. A key determinant in plant cellular development is the deposition of the cell wall to dictate the physical form and physiological function of newly developing cells, tissues, and organs. However, it is unclear to what degree cell walls are restructured to initiate and support the formation of new gall tissue. Here, we characterize the molecular alterations underlying gall development using a combination of metabolomic, histological, and biochemical techniques to elucidate how leaf cells are reprogrammed to form galls. Strikingly, gall development involves an exceptionally coordinated spatial deposition of lignin and xylan to form de novo gall vasculature. Our results highlight how Cynipid wasps can radically change the metabolite profile and restructure the cell wall to enable the formation of galls, providing new insights into the mechanism of gall induction and the extent to which plants can be entirely reprogrammed to form novel structures and organs.

Exploring the diversity of galls on Artemisia indica induced by Rhopalomyia species through morphological and transcriptome analyses

“…Host plants generate galls in response to physical stimuli such as oviposition or feeding and chemical signals such as secreted short peptides, proteins, and phytohormones (Hirano et al, 2024; Korgaonkar et al, 2021; Mapes & Davies, 2001; Straka et al, 2010; Tooker & De Moraes, 2011; Yamaguchi et al, 2012). Transcriptome and metabolome analyses of developing or mature galls have identified genes and molecules potentially playing roles in the maintenance of the gall structure (Bailey et al, 2015; Chen et al, 2018; Markel et al, 2024; Schultz et al, 2019). Many insect‐induced galls resemble ectopic fruits, and some accumulate high concentrations of nutrients including amino acids (Koyama et al, 2004; Suzuki et al, 2009).…”