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Edited by Sheng Yang He, Michigan State University, East Lansing, MI, and approved October 5, 2016 (received for review June 28, 2016)
Significance
The Rhg1 resistance locus of soybean helps control one of the most damaging diseases in world agriculture. We found that Rhg1 (resistance to Heterodera glycines 1)-mediated resistance utilizes an unusual mechanism. Resistant soybeans carry a dysfunctional variant of the housekeeping protein α-SNAP [soluble NSF (N-ethylmaleimide–sensitive factor) attachment protein]. Rhg1 resistance-type α-SNAPs interact poorly with NSF and disrupt vesicle trafficking. High levels of resistance-type α-SNAPs interfere with wild-type α-SNAP activities, yet are functionally balanced in most tissues by sufficient wild-type α-SNAP levels. However, the biotrophic plant–pathogen interface is disabled by localized hyperaccumulation of resistance-type α-SNAPs. This study suggests a paradigm of resistance conferred by a dysfunctional version of a core cellular housekeeping protein.
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.
Footnotes
↵1Present address: Texas A&M AgriLife Research, Department of Plant Pathology & Microbiology, Texas A&M University System, Dallas, TX 75252.
↵2Present address: Department of Biomedical Engineering, University of Wisconsin–Madison, Madison, WI 53706.
- ↵3To whom correspondence should be addressed. Email: afbent{at}wisc.edu.
Author contributions: A.M.B., J.M.S., J.S., P.H.M., A.T., B.K.A., and A.F.B. designed research; A.M.B., J.M.S., J.S., P.H.M., A.T., and B.K.A. performed research; A.M.B., J.M.S., J.S., P.H.M., A.T., B.K.A., and A.F.B. analyzed data; and A.M.B., J.M.S., and A.F.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1610150113/-/DCSupplemental.
- Adam M. Baylessa,
- John M. Smitha,
- Junqi Songa,1,
- Patrick H. McMinna,2,
- Alice Teilleta,
- Benjamin K. Augustb, and
- Andrew F. Benta,3
- aDepartment of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706;
- bUniversity of Wisconsin School of Medicine and Public Health Electron Microscopy Facility, University of Wisconsin–Madison, Madison, WI 53706
Edited by Sheng Yang He, Michigan State University, East Lansing, MI, and approved October 5, 2016 (received for review June 28, 2016)
Significance
The Rhg1 resistance locus of soybean helps control one of the most damaging diseases in world agriculture. We found that Rhg1 (resistance to Heterodera glycines 1)-mediated resistance utilizes an unusual mechanism. Resistant soybeans carry a dysfunctional variant of the housekeeping protein α-SNAP [soluble NSF (N-ethylmaleimide–sensitive factor) attachment protein]. Rhg1 resistance-type α-SNAPs interact poorly with NSF and disrupt vesicle trafficking. High levels of resistance-type α-SNAPs interfere with wild-type α-SNAP activities, yet are functionally balanced in most tissues by sufficient wild-type α-SNAP levels. However, the biotrophic plant–pathogen interface is disabled by localized hyperaccumulation of resistance-type α-SNAPs. This study suggests a paradigm of resistance conferred by a dysfunctional version of a core cellular housekeeping protein.
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.
- plant disease resistance
- α-SNAP
- soybean cyst nematode
- Rhg1
Footnotes
↵1Present address: Texas A&M AgriLife Research, Department of Plant Pathology & Microbiology, Texas A&M University System, Dallas, TX 75252.
↵2Present address: Department of Biomedical Engineering, University of Wisconsin–Madison, Madison, WI 53706.
- ↵3To whom correspondence should be addressed. Email: afbent{at}wisc.edu.
Author contributions: A.M.B., J.M.S., J.S., P.H.M., A.T., B.K.A., and A.F.B. designed research; A.M.B., J.M.S., J.S., P.H.M., A.T., and B.K.A. performed research; A.M.B., J.M.S., J.S., P.H.M., A.T., B.K.A., and A.F.B. analyzed data; and A.M.B., J.M.S., and A.F.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1610150113/-/DCSupplemental.
Disease resistance by impairment of α-SNAP
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