Canonical and noncanonical ethylene signaling pathways that regulate Arabidopsis susceptibility to the cyst nematode Heterodera schachtii

Abstract

Plant-parasitic cyst nematodes successfully exploit various phytohormone signaling pathways to establish a new hormonal equilibrium that facilitates nematode parasitism. Although it is largely accepted that ethylene regulates plant responses to nematode infection, a mechanistic understanding of how ethylene shapes plant-nematode interactions remains largely unknown. In this study, we examined the involvement of various components regulating ethylene perception and signaling in establishing Arabidopsis susceptibility to the cyst nematode Heterodera schachtii using a large set of well-characterized single and higher order mutants. Our analyses revealed the existence of two pathways that separately engage ethylene with salicylic acid (SA) and cytokinin signaling during plant response to nematode infection. One pathway involves the canonical ethylene signaling pathway in which activation of ethylene signaling results in suppression of SA-based immunity. The second pathway involves the ethylene receptor ETR1, which signals independently of SA acid to affect immunity, instead altering cytokinin-mediated regulation of downstream components. Our results reveal important mechanisms through which cyst nematodes exploit components of ethylene perception and signaling to affect the balance of hormonal signaling through ethylene interaction with SA and cytokinin networks. This hormonal interaction overcomes plant defense and provokes a susceptible response.

Phytoparasitic Nematode Control of Plant Hormone Pathways

“…The attraction of H. glycines to roots of Arabidopsis (nonhost for SCN) is enhanced in ET-insensitive mutants and diminished in ET-overproducing mutants (Hu et al, 2017b). Recent work by Piya et al (2018) elucidates how ET perception in Arabidopsis can result in higher or lower susceptibility to H. schachtii (measured as the number of developing females), depending on the receptor and its downstream pathway. The canonical ET signaling pathway causes suppression of SA-based defense, resulting in higher susceptibility to the CN, fitting the idea that ET enhances CN infection.…”

“…The canonical ET signaling pathway causes suppression of SA-based defense, resulting in higher susceptibility to the CN, fitting the idea that ET enhances CN infection. The second pathway acts via the ETHYLENE RECEPTOR1, with ET inhibiting cytokinin signaling and thus reducing susceptibility to H. schachtii infection (Piya et al, 2018). Depending on the specific host-nematode interaction and timing or location of ET effects, cross talk with other hormone pathways could, therefore, have different effects on the host response to CN infection.…”

Ethylene Response Factor (ERF) genes modulate plant root exudate composition and the attraction of plant parasitic nematodes

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

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

“…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.…”