Signal Molecules Mediate the Impact of the Earthworm Aporrectodea caliginosa on Growth, Development and Defence of the Plant Arabidopsis thaliana

Abstract

Earthworms have generally a positive impact on plant growth, which is often attributed to a trophic mechanism: namely, earthworms increase the release of mineral nutrients from soil litter and organic matter. An alternative hypothesis has been proposed since the discovery of a signal molecule (Indole Acetic Acid) in earthworm faeces. In this study, we used methodologies developed in plant science to gain information on ecological mechanisms involved in plant-earthworm interaction, by looking at plant response to earthworm presence at a molecular level. First, we looked at plant overall response to earthworm faeces in an in vitro device where only signal molecules could have an effect on plant growth; we observed that earthworms were inducing positive or negative effects on different plant species. Then, using an Arabidopsis thaliana mutant with an impaired auxin transport, we demonstrated the potential of earthworms to stimulate root growth and to revert the dwarf mutant phenotype. Finally, we performed a comparative transcriptomic analysis of Arabidopsis thaliana in the presence and absence of earthworms; we found that genes modulated in the presence of earthworms are known to respond to biotic and abiotic stresses, or to the application of exogenous hormones. A comparison of our results with other studies found in databases revealed strong analogies with systemic resistance, induced by signal molecules emitted by Plant Growth Promoting Rhizobacteria and/or elicitors emitted by non-virulent pathogens. Signal molecules such as auxin and ethylene, which are considered as major in plant-microorganisms interactions, can also be of prior importance to explain plant-macroinvertebrates interactions. This could imply revisiting ecological theories which generally stress on the role of trophic relationships.

Plant-mediated links between detritivores and aboveground herbivores

“…Puga-Freitas et al (2012) proposed that signal molecules (such as indole acetic acid, IAA) may mediate the earthworm effects on plant growth. They also showed that earthworms change the expression of genes responsive to abiotic and biotic stress, and to the application of exogenous hormones.…”

Earthworms and Fusarium oxysporum: effect on strawberry plant growth and production

“…fragariae (related to fruit production) following the earthworm inoculation in this experiment was not expected, as normally the positive effects of these invertebrates in the soil negate the negative consequences of plants pathogens (DEMETRIO et al, 2017;LAFONT et Several surveys have reported positive effects of earthworms on plant growth (LAOSSI et al, 2010;PASHANASI et al, 1996;PUGA-FREITAS et al, 2012). This effect can occur in different ways, with increased available nitrogen probably the main factor in this phenomenon, due to the high uptake by the plants and typical low availability in the soil (AGREN et al, 2012).…”

“…The observed increases in T1 in relation to control represent around 1,000 kg per hectare (considering 24,000 strawberry plants hectare -1 ). (LAOSSI et al, 2010;PASHANASI et al, 1996;PUGA-FREITAS et al, 2012). This effect can occur in different ways, with increased available nitrogen probably the main factor in this phenomenon, due to the high uptake by the plants and typical low availability in the soil (AGREN et al, 2012).…”

Biocontrol of eyespot disease on two winter wheat cultivars by an anecic earthworm (Lumbricus terrestris)

“…Earthworms are known to modify the expression of genes involved in autolysis, enabling the plant to mobilize nutrients an energy rapidly in response to stress, and that of genes involved in the biosynthesis pathway of jasmonic acid, a plant hormone controlling defense mechanisms (Blouin et al, 2005). Indole acetic acid, from the auxin family, also seems to be involved in the effect of earthworms on plants: the dwarf phenotype of an auxin-transport mutant of Arabidopsis thaliana can be converted to the wild-type phenotype in the presence of earthworms (Puga-Freitas et al, 2012b) with IAA-containing casts (Muscolo et al, 1998;Quaggiotti et al, 2004). Far from being an exception, this modification of plant immunity and development through signal molecules appears to be a common feature of soil organisms, from microorganisms, to the micro-, meso-and macro-fauna (Puga-Freitas and .…”

“…We hypothesized that these effects might also result in a lower incidence of eyespot in the presence of earthworms. The mechanisms underlying this control of parasite incidence in the presence of earthworms may involve indirect effects due to improvements in the nutritional status of the plant in the presence of earthworms (Whalen and Parmelee, 2000) or direct effects on plant defense mechanisms and the induction of induced systemic resistance (Puga-Freitas et al, 2012b;Puga-Freitas and Blouin, 2015).…”