Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines

Abstract

Plant parasitic nematodes respond to root exudates to locate their host roots. In our studies second stage juveniles of Heterodera glycines, the soybean cyst nematode (SCN), quickly migrated to soybean roots in Pluronic F-127 gel. Roots of soybean and non-host Arabidopsis treated with the ethylene (ET)-synthesis inhibitor aminoethoxyvinylglycine (AVG) were more attractive to SCN than untreated roots, and significantly more nematodes penetrated into roots. Moreover, Arabidopsis ET insensitive mutants (ein2, ein2-1, ein2-5, ein3-1, ein5-1, and ein6) were more attractive than wild-type plants. Conversely, the constitutive triple-response mutant ctr1-1, was less attractive to SCN. While ET receptor gain-of-function mutant ein4-1 attracted more SCN than the wild-type, there were no significant differences in attractiveness between another gain-of-function ET receptor mutant, etr1-3, or the loss-of-function mutants etr1-7 and ers1-3 and the wild type. Expression of the reporter construct EBS: β-glucuronidase (GUS) was detected in Arabidopsis root tips as early as 6 h post infection, indicating that ET signaling was activated in Arabidopsis early by SCN infection. These results suggest that an active ET signaling pathway reduces root attractiveness to SCN in a way similar to that reported for root-knot nematodes, but opposite to that suggested for the sugar beet cyst nematode Heterodera schachtii.

ETHYLENE RESPONSE FACTOR (ERF) genes modulate plant root exudate composition and the attraction of plant parasitic nematodes

“…Our data indicate that M. incognita and G. pallida regulate their behaviour ex planta in response to ERF-E2, but not ERF-E3. This corroborates our hypothesis that one or more ERF gene products regulate root exudate composition, phenocopying the enhanced attraction of PPNs observed following the inhibition of ethylene synthesis (Hu et al, 2017;Fudali et al, 2013). Our data also demonstrate that M. incognita and G. pallida use developmentally regulated signalling processes in the host plant to coordinate host selection behaviour ex planta.…”

“…For this line of research to develop robust and durable new sources of PPN resistance, it will be important to establish the behavioural impact that such interventions have on geographically coincident species, as well as different populations of a given species (Cox et al, 2019b). Nonetheless, our data indicate that ERF-E2 knockdown phenocopies the enhanced attraction of certain PPN species, which is also observed following the inhibition of ethylene signalling (Hu et al, 2017;Fudali et al, 2013). It is possible that other ERF genes contribute to this interaction (positively or negatively), which necessitates further investigation.…”

“…ERF proteins belong to the APETALA2/ERF transcription factor family, and regulate ethylene-responsive genes through binding to GCC-box elements (Mizoi et al, 2012). Ethylene is linked to various aspects of host-PPN interactions (Warmerdam et al, 2019;Piya et al, 2019;Wubben et al, 2004;Wubben et al, 2001), and Inhibition of ethylene signalling enhances attraction of the root knot nematode Meloidogyne hapla, and the cyst nematode Heterodera glycines to plant roots (Hu et al, 2017;Fudali et al, 2013). This indicates that constitutive receptor-mediated activation of CTR1 and negative regulation of ERF genes in the absence of ethylene, promotes attraction of PPNs.…”

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

“…Chemical and genetic manipulations of ethylene biosynthesis in Arabidopsis and tomato have shown that ethylene biosynthesis is required for susceptibility to rootknot and cyst nematodes (Glazer et al, 1985;Goverse et al, 2000;Wubben et al, 2001). Arabidopsis mutants deficient in ethylene signalling are more attractive to infective cyst nematodes and root-knot nematodes (Fudali et al, 2013;Hu et al, 2017). However, giant cells induced by M. javanica in tomato plants treated with an inhibitor of ethylene biosynthesis [aminoethoxyvinylglycine (AVG)] show significantly reduced cellular hypertrophy (Glazer et al, 1985).…”

Impacts of Root Metabolites on Soil Nematodes

“…Roots of soybean and Arabidopsis treated with ethylene synthesis inhibitor attracted more Soybean cyst nematodes (Heterodera glycines), and significantly more nematodes penetrated the roots of ethylene synthesis inhibited plants. On the other hand, ethylene insensitive mutants roots of Arabidopsis accessions were more attractive to H. glycines than the wild type (Hu et al, 2017). Ethylene-overproducing A. thaliana mutants roots were hypersusceptible to beet cyst nematode (Heterodera schachtii), and ethylene-insensitive mutants were less susceptible to H. schachtii (Wubben et al, 2001).…”