Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites

Abstract

Soil fauna activities are probably more important than currently acknowledged in determining individual plant response to stresses and overall plant diversity. Here we demonstrate that the positive effect of earthworms on rice could be the result of a systemic effect on plant physiology. Moreover, this effect could improve tolerance to stressors such as parasitic nematodes. In a controlled experiment, an 82% decrease in the production of infested plants was suppressed when earthworms were present. Earthworms had no direct effect on nematode population size. In their presence, however, root biomass was not affected by nematodes and the expected inhibition of photosynthesis was suppressed. In the leaves, the expression of three stress-responsive genes (coding for lipoxygenase, phospholipase D and cysteine protease) was modulated by the presence of belowground invertebrate activities. We document conflicting systemic effects of parasitic nematodes and beneficial earthworms, although we cannot precisely identify the mechanism involved. These results reveal the importance of non-trophic belowground/aboveground interactions for plant health and response to stresses.