Plant Root-Exudates Recruit Hyperparasitic Bacteria of Phytonematodes by Altered Cuticle Aging: Implications for Biological Control Strategies.

Sharad Mohan,Supradip Saha,K Kiran Kumar,Vivek Sutar,Keith G Davies,Janet Rowe

doi:10.3389/fpls.2020.00763

Abstract

Phytonematodes are globally important functional components of the belowground ecology in both natural and agricultural soils; they are a diverse group of which some species are economically important pests, and environmentally benign control strategies are being sought to control them. Using eco-evolutionary theory, we test the hypothesis that root-exudates of host plants will increase the ability of a hyperparasitic bacteria, Pasteuria penetrans and other closely related bacteria, to infect their homologous pest nematodes, whereas non-host root exudates will not. Plant root-exudates from good hosts, poor hosts and non-hosts were characterized by gas chromatography-mass spectrometry (GC/MS) and we explore their interaction on the attachment of the hyperparasitic bacterial endospores to homologous and heterologous pest nematode cuticles. Although GC/MS did not identify any individual compounds as responsible for changes in cuticle susceptibility to endospore adhesion, standardized spore binding assays showed that Pasteuria endospore adhesion decreased with nematode age, and that infective juveniles pre-treated with homologous host root-exudates reduced the aging process and increased attachment of endospores to the nematode cuticle, whereas non-host root-exudates did not. We develop a working model in which plant root exudates manipulate the nematode cuticle aging process, and thereby, through increased bacterial endospore attachment, increase bacterial infection of pest nematodes. This we suggest would lead to a reduction of plant-parasitic nematode burden on the roots and increases plant fitness. Therefore, by the judicious manipulation of environmental factors produced by the plant root and by careful crop rotation this knowledge can help in the development of environmentally benign control strategies.

Highlights

Belowground biodiversity plays a key role in determining ecological and evolutionary outcomes to terrestrial ecosystems, and nematodes, which are globally abundant, play a key function in determining local patterns of soil fertility (Bargett and Van Der Putten, 2014; Van Den Hoogen et al, 2019)
There was no statistical significant difference between root-knot nematode (RKN) and pigeon pea cyst nematode (PPCN) in the number of endospores adhering to the cuticles of either RKN and PPCN at any one time point (Figure 2); over time there was a reduction from over 15 spores J2−1 at T0 to approximately 12 spores J2−1 at T7 and 5 spores J2−1 at T14; this reduction was statistically significant (ANOVA P < 0.001) and shows that as the cuticles of both species of infective juveniles mature over time they become less susceptible to endospore adhesion
We show that plant root exudates from a host plant changed the susceptibility of the nematode cuticle to endospore adhesion by affecting the natural cuticle maturation process; these changes led to hyperparasitic recruitment in the homologous system using host root exudates, whereas in the heterologous system, using non-host root exudates, this was not the case

Summary

Introduction

Belowground biodiversity plays a key role in determining ecological and evolutionary outcomes to terrestrial ecosystems, and nematodes, which are globally abundant, play a key function in determining local patterns of soil fertility (Bargett and Van Der Putten, 2014; Van Den Hoogen et al, 2019). Plant-parasitic nematodes are an important component of the root herbivore community where multitrophic interactions between their host plant and their natural enemies determine plant productivity in both natural and economically important agricultural systems (Van Der Putten et al, 2006). Soil bacteria are another abundant and diverse group of soil microorganism important in ecosystem processes that remain largely functionally and taxonomically uncharacterized because the majority are uncultivatable in the laboratory (Lok, 2015; Delgado-Baquerizo et al, 2018). We explore a belowground tri-trophic interaction between plant hosts, their nematode parasites using homologous and heterologous bacterial endospore forming hyperparasites, Pasteuria spp. with the view to develop new crop protection strategies for phytonematodes

Methods

Results

Conclusion