A novel family of secreted insect proteins linked to plant gall development

Abstract

In an elaborate form of inter-species exploitation, many insects hijack plant development to induce galls, novel plant organs resulting from dramatic reprograming of plant cell biology. Insects induce galls by introducing unidentified molecules into plants. Here we identify an aphid gene, determinant of gall color (dgc), that is genetically associated with variation in a gall phenotype, providing the first example of an insect gene implicated in gall development. Dgc encodes a BICYCLE protein, a new family of secreted proteins. Bicycle genes are strongly expressed specifically in galling aphid salivary glands, suggesting they control many aspects of gall development. Bicycle genes have experienced unusually strong diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.

Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics

“…1B), size of galls produced by the gall fly Eurosta is determined by genotypes of both fly and plant, and evolution of gall size is influenced in part by crossspecies selection imposed on Eurosta larvae by species at other trophic levels (Weis and Abrahamson 1986;Weis et al 1992;Abrahamson and Weis 1997). This type of interaction is common across gall-forming insects and their plant hosts; in Hormaphis aphids, variation in the bicycle gene has been linked to variation in gall size (Korgaonkar et al 2021). In many herbivore-plant interactions, physical damage to leaves induces upregulation of defensive compounds to deter further herbivory, which can be countered by matching physiological changes in the herbivore (Ohgushi 2005).…”

Chromosome‐level genome assembly for the horned‐gall aphid provides insights into interactions between gall‐making insect and its host plant

“…The gall midge Mayetiola destructor can inject effector proteins into tissues via its saliva during feeding, leading to the conversion of a whole wheat seedling into a gall (Aljbory et al, 2018;Wang et al, 2018). A novel family of insect-secreted proteins named BICYCLE has been identified in Hormaphis cornu, which induce gall formation on the leaves of witch hazel, Hamamelis virginiana (Korgaonkar et al, 2021). BICYCLE may regulate numerous aspects of gall development, due to their abundant expression in salivary glands specifically in gall aphids.…”

Spotlight on the Roles of Whitefly Effectors in Insect–Plant Interactions

“…Therefore, the classification of effectors can be highly context dependent and is often difficult based on only a few experiments. Effectors can also influence processes beyond plant immunity, such as altering plant development (MacLean et al, 2011;Sugio et al, 2011Sugio et al, , 2015 or initiating gall formation (Korgaonkar et al, 2020). There is special interest in effectors that have evolved for the purpose of modulating host plant responses, especially host defense responses (Shiraishi et al, 1992), and in the counteradaptations of plants to undo or bypass these modulations (Dangl, 1994).…”