Are Gall Insects Large Rhizobia?

Abstract

Plants are subject to attack by a range of insect herbivores including those producing galls. Gall formation is a remarkable process in which the insect becomes the new organiser of plant development: normal cellular differentiation is inhibited, and the growth of the tissue is altered to produce characteristic and often bizarre structures (Meyer 1987, Shorthouse and Rohfritsch 1992). In addition to gall-forming insects, there are other organisms which attack plants causing tumour production: the bacteria from the Rhizobium group, which cause nodules on plant roots, and the bacterium Agrobacterium tumefaciens, which causes crown gall, are examples. Molecular techniques have allowed the mechanisms by which these organisms induce growth deformations in plants to be elucidated, and phenolic compounds have been found to be a fundamental component of the tumour-forming process in both systems. Traditionally phenolic compounds have been viewed as being important in defending plants against attack; in the case of attack by parasitic tumour-forming agents, however, phenolics appear to have a rather different role. In these systems, phenolic compounds are used by the invading organisms as indicators of susceptible host plants, and they also mediate the manipulation of plant growth by the attacking organism because they are able to affect plant gene expression and to alter plant hormone activity. Galls are particularly close associations between an attacking insect and a plant; the gall insect appears to overwhelm the plant's defences in a unique way. Gall insects may be more similar, in terms of their effects on plant defences such as phenolic compounds, to other tumour-forming organisms than they are to other insects. Here I examine the idea that since phenolic compounds are important in mediating the interactions between plants and tumour-forming bacteria and may have a role in the regulation of plant growth, the same physiological mechanisms may be operating in gall formation. The essential question is: Do gall-formers use phenolic compounds to control plant growth and development as other tumour-forming organisms have been shown to do? Evidence to support this idea is indirect. Very little work has been carried out on the mechanisms of gall formation at the molecular level. It is, however, worth attempting to gather such evidence since consideration of the important advances in understanding of other plant tumour-inducing processes made by plant physiologists could give entomologists some clues to the changes in plant physiology and gene expression required to initiate galls. Although many entomologists and ecologists are familiar with the idea of phenolic compounds being involved in the defence of plants against attack by insects (and other organisms), fewer have considered these compounds as signals which mediate interactions between plants and invading organisms, including insects. Perhaps most entomologists are unlikely to have regarded gall insects as large rhizobia! At this point it is important to clarify that whilst Rhizobium/plant associations are mutualistic, no implication is made here that galling is a mutualism, merely that gall insects may have adopted a similar physiological methodology to control plant growth as rhizobia have.