Anatomy and Ultrastructure of Galls Induced by Neuroterus quercusbaccarum (Hymenoptera: Cynipidae) on Oak Leaves (Quercus robur).

Leszek Stanisław Jankiewicz,Agnieszka Marasek-Ciolakowska,Marzenna Guzicka

doi:10.3390/insects12100850

Leszek Stanisław Jankiewicz, Agnieszka Marasek-Ciolakowska + Show 1 more

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https://doi.org/10.3390/insects12100850

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Abstract

Simple SummaryGalls induced by insects are commonly found on oak leaves in temperate climates. Their induction and development are, however, still only partially known. Our aim was to present a detailed description of their anatomy and fine structure. Using scanning electron microscopy (SEM), we observed the wax cover of a gall and two types of openings on its surface: one similar to degenerated stomata and the other one that we called “large openings on epidermal protuberance”. Nutritive tissue underwent marked changes with time: in a young gall, the cellular walls were not visible, and a distinct cellular structure appeared only later. In the mound of the gall, there was a distinct subepidermal layer of cells containing dense cytoplasm. Tannins occurred in vacuoles or in cell walls in granular form or in compact formations. The leaf subtending the gall showed additional cell divisions and strong lignification of cell walls in the tissue surrounding the peduncle of the gall.The structure and ultrastructure of two developmental stages of the spangle gall induced by Neuroterus quercusbaccarum (Hymenoptera, Cynipidae) were investigated using light microscopy (LM), fluorescence microscopy (FM), and transmission (TEM) and scanning (SEM) electron microscopy. The general design of the gall structure was typical of Cynipidae, but some structural features distinguished the spangle gall. Previously undescribed, characteristic multicellular epidermal protuberances with large openings were observed in autumn on the surface of galls. These may facilitate the gas exchange between the atmosphere and the inside of the gall, thus assisting larval respiration. The larval chamber is surrounded by both a sclerenchymatous capsule and numerous cells containing calcium oxalate crystals that may both serve as protective barriers. In young galls, the nutritive tissue is a wall-less protoplasmic mass, potentially easily accessible to young larvae with delicate mandibles. Cell walls only develop at a later stage. The nutritive tissue was found to be rich in proteins and lipids, but starch grains were not observed. Cellular topology suggests that spangle galls grow by anticlinal division of marginal epidermal cells and periclinal division of subepidermal cells. Cellular proliferation (hyperplasia) also occurs in the leaf tissue near the connection with the gall peduncle, which eventually lignifies.

Highlights

IntroductionIndividual host plants are often attacked by different wasp species that manipulate plant morphogenesis, inducing the development of species-specific gall phenotypes
The discussion on the nature of plant galls has lasted for more than 100 years [1], and we still know very little about how this kind of neoformation is induced and developed [2,3,4,5,6].Investigations of gall anatomy and development are pivotal because they are likely to disclose important clues about still poorly known mechanisms of plant morphogenesis [3,7,8].Individual host plants are often attacked by different wasp species that manipulate plant morphogenesis, inducing the development of species-specific gall phenotypes
We proposed a novel interpretation for the mechanism of gall induction [23]: the species-specific response induced in the host plant by cynipid wasps is so complex as to suggest gene transfer from the insect to the plant

Summary

Introduction

Individual host plants are often attacked by different wasp species that manipulate plant morphogenesis, inducing the development of species-specific gall phenotypes. Cynipid galls are examples of induced plant development where an inducer controls plant-cell differentiation [11]. Complicated galls protect larvae and provide them with nutrients [10,12]. Nutrients such as lipids, proteins, and sugars are accumulated in cells of nutritive tissue lining the larval chambers. Proteins, and sugars are accumulated in cells of nutritive tissue lining the larval chambers Such cells, packed with nutrients, are not found anywhere else in the host plant [13]

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