Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.
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Abstract:Gall inducers are favoured as biocontrol agents of weeds because they tend to have a narrow host range. Six insect and one nematode gall inducer used in Canada are described in terms of their biology, gall morphology, gall physiology, and effectiveness in weed control. The species differ in plant organ attacked, requirement for moisture, whether the galls are induced by secretions or by severing xylem, and effectiveness, which in part relates to the ability of the gall to import nutrients. The most powerful galls divert assimilates from other sinks via a gall's vascular system joined to that of their host. One of our examples also has mechanisms to compensate for reduction of turgor during drought. Two of the gall inducers enhance their nutrient supply by severing xylem in a plant nutrient sink. One, in the short-term sink of a thistle capitulum, obtains about a quarter of its assimilates at the expense of other capitula. The other, in the long-term sink of a rosette root, approximately halves seed production. Hypotheses are presented to explain various aspects of gall development and function.
Diplolepis nodulosa (Beutenmüller) induces small, single-chambered, prosoplasmic galls in stems of Rosa blanda Ait. Gall initiation begins when adult females deposit a single egg into the procambium of R. blanda buds. Pith cells at the distal pole of the egg lyse forming a chamber into which the hatching larva enters. Cells lining the chamber differentiate into nutritive cells, which serve as the larval food. Gall growth is characterized by the proliferation of parenchymatous nutritive cells causing gall enlargement. A separate gall vasculature does not form, but instead, gall tissues are irrigated by the existing stem vasculature. Maturation begins when gall tissues cease proliferating and differentiate into distinct layers concentrically arranged around the larval chamber. The innermost layer is composed of cytoplasmically dense nutritive tissue, followed by parenchymatous nutritive tissue, sclerenchyma, cortex, and epidermis. Parenchymatous nutritive tissue differentiates into nutritive tissue and is consumed by the larva. Galls of D. nodulosa are susceptible to anatomical modification by the phytophagous inquiline Periclistus pirata (Osten Sacken). Galls attacked by P. pirata become enlarged and multichambered, with little resemblance to inducer-inhabited galls. Periclistus pirata kill the larva of D. nodulosa at oviposition and deposit several eggs per host gall. Inquiline-occupied galls may contain the eggs of several females. Nutritive tissue induced by D. nodulosa disintegrates. Growth of attacked galls occurs prior to hatching of P. pirata eggs. At egg hatch, the gall appears as an enlarged hollow sphere and larvae disperse over the chamber surface and feed on parenchymatous tissue. Feeding induces tissue proliferation, which surrounds each larva within its own chamber. As galls mature, cells surrounding each larval chamber lignify forming a sclerenchyma sheath. Cells inside the sclerenchyma sheath differentiate into nutritive cells and are consumed by the inquiline larvae.Key words: Rosa, Cynipidae, gall, developmental morphology, inquiline.
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