Abstract
It has been a long-standing question as to whether the interaction between gall-forming insects and their host plants is merely parasitic or whether it may also benefit the host. On its host Rhus chinensis, the aphid Schlechtendalia chinensis induces the formation of closed galls, referred to as horned galls. Typically, mature aphid populations comprise thousands of individuals, which is sufficient to cause the accumulation of high CO2 levels in galls (on average 8-fold higher and up to 16 times than atmospheric levels). Large aphid populations also excrete significant amounts of honeydew, a waste product high in sugars. Based on 13C isotope tracing and genomic analyses, we showed that aphid-derived carbon found in CO2 and honeydew was recycled in gall tissues via photosynthesis and glycometabolism. These results indicated that the aphid-gall system evolved in a manner that allowed nutrient recycling, where the gall provides nutrients to the growing aphid population, and in turn, aphid-derived carbon metabolites provide a resource for the growth of the gall. The metabolic efficiency of this self-circulating system indicates that the input needed from the host plant to maintain aphid population growth less than previously thought and possibly minimal. Aside from the recycling of nutrients, we also found that gall metabolites were transported to other parts of the host plant and is particularly beneficial for leaves growing adjacent to the gall. Taken together, galls in the S. chinensis–Rhus chinensis system are highly specialized structures that serve as a metabolic and nutrient exchange hub that benefits both the aphid and its host plant. As such, host plants provide both shelter and nutrients to protect and sustain aphid populations, and in return, aphid-derived metabolites are channeled back to the host plant and thus provide a certain degree of “metabolic compensation” for their caloric and structural needs.
Highlights
It has been long thought that gall-inducing insects reprogram the physiology of the host plant in a way that primarily benefits the growing insect colony (Larson and Whitham, 1991; Danks, 2002; Inbar et al, 2004; Koyama et al, 2004)
Because the surface of a gall is green, it was possible that the gall itself is photosynthetically active, in which case we would expect that interior CO2 could directly fuel photosynthesis in gall tissues
When we measured photosynthesis rates in the gall, we found that gall tissues had measurable levels of photosynthesis even though photosynthesis per unit of gall tissues was lower than that of leaves (Figures 2C,D)
Summary
It has been long thought that gall-inducing insects reprogram the physiology of the host plant in a way that primarily benefits the growing insect colony (Larson and Whitham, 1991; Danks, 2002; Inbar et al, 2004; Koyama et al, 2004). Very little is known about potential benefits that gall insects may provide to the host plant. Some studies have shown that the relationship between gall inducers and host plants is not merely a simple parasitic/defensive relationship. Studies have shown that the overall metabolism of the gall-bearing plants appears to remain unaffected, except for stress-related changes at and near the locations where galls have developed (Raman, 2011). These findings suggest a more complex interaction between a gall-inducing insect and its host plant, as opposed to a simple parasitic/defensive relationship
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