Disease resistance through impairment of α-SNAP-NSF interaction and vesicular trafficking by soybean Rhg1.
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.
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706.
Adam M
AM
Bayless
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706.
John M
JM
Smith
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706.
Junqi
J
Song
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706.
Patrick H
PH
McMinn
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706.
Alice
A
Teillet
University of Wisconsin School of Medicine and Public Health Electron Microscopy Facility, University of Wisconsin-Madison, Madison, WI 53706.
Benjamin K
BK
August
Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706; afbent@wisc.edu.
Andrew F
0000-0001-6610-9525
AF
Bent
D000818:Animals; D060467:Disease Resistance; D009154:Mutation; D052066:N-Ethylmaleimide-Sensitive Proteins / Q000378:metabolism*; D009348:Nematoda / Q000502:physiology; D010935:Plant Diseases / Q000469:parasitology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D011485:Protein Binding; D052067:Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins / Q000235:genetics / Q000378:metabolism*; D013025:Glycine max / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology; D022161:Transport Vesicles / Q000378:metabolism*
D010940:Plant Proteins; D052067:Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins; D052066:N-Ethylmaleimide-Sensitive Proteins
Rhg1; plant disease resistance; soybean cyst nematode; α-SNAP