Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

Abstract

α-SNAP [soluble NSF (N-ethylmaleimide–sensitive factor) attachment protein] and NSF proteins are conserved across eukaryotes and sustain cellular vesicle trafficking by mediating disassembly and reuse of SNARE protein complexes, which facilitate fusion of vesicles to target membranes. However, certain haplotypes of the Rhg1 (resistance to Heterodera glycines 1) locus of soybean possess multiple repeat copies of an α-SNAP gene (Glyma.18G022500) that encodes atypical amino acids at a highly conserved functional site. These Rhg1 loci mediate resistance to soybean cyst nematode (SCN; H. glycines), the most economically damaging pathogen of soybeans worldwide. Rhg1 is widely used in agriculture, but the mechanisms of Rhg1 disease resistance have remained unclear. In the present study, we found that the resistance-type Rhg1 α-SNAP is defective in interaction with NSF. Elevated in planta expression of resistance-type Rhg1 α-SNAPs depleted the abundance of SNARE-recycling 20S complexes, disrupted vesicle trafficking, induced elevated abundance of NSF, and caused cytotoxicity. Soybean, due to ancient genome duplication events, carries other loci that encode canonical (wild-type) α-SNAPs. Expression of these α-SNAPs counteracted the cytotoxicity of resistance-type Rhg1 α-SNAPs. For successful growth and reproduction, SCN dramatically reprograms a set of plant root cells and must sustain this sedentary feeding site for 2–4 weeks. Immunoblots and electron microscopy immunolocalization revealed that resistance-type α-SNAPs specifically hyperaccumulate relative to wild-type α-SNAPs at the nematode feeding site, promoting the demise of this biotrophic interface. The paradigm of disease resistance through a dysfunctional variant of an essential gene may be applicable to other plant–pathogen interactions.

Whole‐genome re‐sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad‐based resistance to soybean cyst nematode

“…It has been reported that the interaction of two or more alleles (epistasis) plays a major role in an organism's resistance to diseases and pests (Bayless et al ., ; Meksem et al ., ; Nagel, ). The rhg1 GmSNAP18 protein interacts with NSF (N‐ethylmaleimide–sensitive factor) protein and disturbs vesicle trafficking (Bayless et al ., , ). We discovered that soybean germplasm provided a wide range of SCN resistance controlled by natural variants (SNP and CNV) at both the rhg1 and Rhg4 loci.…”

Systematic Mutagenesis of Serine Hydroxymethyltransferase Reveals an Essential Role in Nematode Resistance

“…A recent report suggests that the rhg1 a-SNAP confers resistance by cytotoxic effects of the large-scale accumulation of the aberrant a-SNAP protein at the nematode feeding sites, which disrupts SNARE complexes and vesicle trafficking (Bayless et al, 2016). How GmSHMT08 conditions this process is not clear.…”

Characterization of the Soluble NSF Attachment Protein gene family identifies two members involved in additive resistance to a plant pathogen

“…However, the molecular mechanisms of how SNAP proteins mediate SCN resistance remain unclear. Recently, it has been described that elevated expression of resistance-type Rhg1 α-SNAP negatively affected the abundance of SNARE-recycling 20 S complexes, disrupting vesicle trafficking, and induced elevated abundance of NSF causing cytotoxicity27. However, expression of other loci encoding a canonical wild-type α-SNAPs counteracted the cytotoxicity of resistance-type Rhg1 α-SNAP27.…”

“…Recently, it has been described that elevated expression of resistance-type Rhg1 α-SNAP negatively affected the abundance of SNARE-recycling 20 S complexes, disrupting vesicle trafficking, and induced elevated abundance of NSF causing cytotoxicity27. However, expression of other loci encoding a canonical wild-type α-SNAPs counteracted the cytotoxicity of resistance-type Rhg1 α-SNAP27. Furthermore, a SCN gene encoding a bacterial-like protein containing a putative SNARE domain (HgSLP-1), an esophageal-gland protein that is secreted by the nematode during plant parasitism, has been suggested to physically interact with the Rhg1 α-SNAP in SCN resistance28.…”