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

Abstract

International audienceSoil 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 nontrophic belowground/aboveground interactions for plant health and response to stresses

Plant-mediated links between detritivores and aboveground herbivores

“…While sulfur-containing glucosinolates were reduced by earthworms in Brassica oleracea leaves (Wurst et al, 2006), aliphatic glucosinolates were reduced and aromatic glucosinolates were enhanced in Sinapis alba (Lohmann et al, 2009). Blouin et al (2005) showed that earthworms can change stress-responsive gene expression (such as genes coding for lipoxygenase and cysteine protease) and make rice ( Oryza sativa ) plants more resistant to root-feeding nematodes.…”

Harmful or useful? A case study of the exotic peregrine earthworm morphospecies Pontoscolex corethrurus

“…Earthworms can have either a direct (e.g., by ingestion) or an indirect (i.e., by physical and chemical changes of soil properties) impact on plant-feeding nematodes (Blouin et al, 2005;Lafont et al, 2007;Senapati, 1992;Wurst, 2010). Under laboratory conditions, Boyer et al (2013) revealed a decrease in Heterodera sacchari and Pratylenchus zeae populations, two plant parasitic nematodes, in the presence of P. corethrurus.…”

Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana

“…According to some authors, the latter leads to the release of mineral nitrogen essentially and represents the major mechanism of action of earthworms responsible for increases in plant biomass production . It could explain how greater benefits on productivity have mostly been observed in poor soils (Brown et al, 2004). However, in an experimental system combining rice plants and the earthworm Millsonia anomala, increasing the availability of mineral nutrients did not suppressed the positive effect of the earthworm on plant growth (Blouin et al, 2006).…”

“…Since decaying earthworms were not a possible source of additional N (worms survival rates were 100%), the majority of the extra N was probably formed through mineralization of soil organic matter by gut-associated and cast-associated micro-organisms, in accordance with Brown's hypothesis that earthworms mostly increase plant growth through N mineralization . However, recent evidence have started an ongoing and fascinating debate of whether enhanced mineralization alone provides a full explanation for the growth stimulation (Brown et al, 2004;Scheu, 2003;Blouin et al, 2006).…”

“…Their mechanisms of action include changes in soil structure that affect root growth and water balance . Earthworms allow plants to better resist parasitic nematode attacks, either by decreasing nematode population density (Yeates, 1981;Senapati, 1992), by enhancing the capacity of plants to tolerate these parasites (Blouin et al, 2005;Lafont et al, 2007) or by stimulating microbes that are antagonistic to root pathogens (Clapperton et al, 2001). Mostly, earthworms are known to induce changes in nutrient spatiotemporal availability through fragmentation and burying of soil litter (Brown et al, 2000) and microbe-based mineralization of soil organic matter (Postma-Blaauw et al, 2006).…”