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, certa...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 47; pp. E7375 - E7382 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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United States
National Academy of Sciences
22.11.2016
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Series | PNAS Plus |
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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. |
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AbstractList | 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. 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. 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. |
Author | Teillet, Alice McMinn, Patrick H. Song, Junqi Bent, Andrew F. August, Benjamin K. Bayless, Adam M. Smith, John M. |
Author_xml | – sequence: 1 givenname: Adam M. surname: Bayless fullname: Bayless, Adam M. organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 2 givenname: John M. surname: Smith fullname: Smith, John M. organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 3 givenname: Junqi surname: Song fullname: Song, Junqi organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 4 givenname: Patrick H. surname: McMinn fullname: McMinn, Patrick H. organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 5 givenname: Alice surname: Teillet fullname: Teillet, Alice organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 6 givenname: Benjamin K. surname: August fullname: August, Benjamin K. organization: University of Wisconsin School of Medicine and Public Health Electron Microscopy Facility, University of Wisconsin–Madison, Madison, WI 53706 – sequence: 7 givenname: Andrew F. surname: Bent fullname: Bent, Andrew F. organization: Department of Plant Pathology, University of Wisconsin–Madison, Madison, WI 53706 |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27821740$$D View this record in MEDLINE/PubMed |
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Cites_doi | 10.1038/nature02076 10.1126/science.aaa5267 10.1038/nrm2002 10.1101/gr.849004 10.1094/MPMI-18-0593 10.1146/annurev.phyto.43.011205.141140 10.1016/j.pbi.2011.03.012 10.1111/mec.13138 10.1091/mbc.7.5.693 10.1073/pnas.1115146109 10.1074/jbc.M111.278358 10.1104/pp.114.235952 10.1007/s11103-012-9932-z 10.1016/j.pbi.2008.04.003 10.1038/nsmb.1451 10.1091/mbc.e07-05-0498 10.1146/annurev.phyto.43.040204.140218 10.1146/annurev-cellbio-100913-013439 10.1016/S0092-8674(00)80512-7 10.1104/pp.011742 10.1038/nature14148 10.1038/nmeth.2019 10.1093/pcp/pcu046 10.1186/1471-2229-11-5 10.1073/pnas.1211757110 10.1146/annurev-phyto-080614-115928 10.1371/journal.pgen.1005200 10.1074/jbc.M113.489807 10.1007/s00122-016-2779-y 10.1104/pp.110.171785 10.1126/science.1236011 10.1371/journal.pone.0145601 10.1007/978-1-59745-196-3_6 10.1038/nature08670 10.2135/cropsci2004.1121 10.1073/pnas.1506409112 10.1111/tpj.13240 10.4161/15592324.2014.977737 10.1007/s00425-013-1923-z 10.1094/MPMI-05-12-0128-CR 10.1038/30006 10.1083/jcb.139.4.875 10.1091/mbc.e03-02-0097 10.1097/00001756-200105250-00015 10.1126/science.1228746 10.1073/pnas.1505665112 10.1038/ng1302 10.1111/j.1462-5822.2008.01238.x 10.1016/j.febslet.2007.03.032 10.1046/j.1365-313X.1999.00552.x 10.1094/PHP-2008-0118-01-RS 10.1105/tpc.12.11.2201 10.1104/pp.110.167536 |
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Keywords | plant disease resistance soybean cyst nematode α-SNAP Rhg1 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 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. 1Present address: Texas A&M AgriLife Research, Department of Plant Pathology & Microbiology, Texas A&M University System, Dallas, TX 75252. Edited by Sheng Yang He, Michigan State University, East Lansing, MI, and approved October 5, 2016 (received for review June 28, 2016) 2Present address: Department of Biomedical Engineering, University of Wisconsin–Madison, Madison, WI 53706. |
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References | e_1_3_3_50_2 e_1_3_3_16_2 e_1_3_3_18_2 e_1_3_3_39_2 e_1_3_3_12_2 e_1_3_3_37_2 e_1_3_3_14_2 e_1_3_3_35_2 e_1_3_3_33_2 e_1_3_3_54_2 e_1_3_3_10_2 e_1_3_3_31_2 e_1_3_3_52_2 e_1_3_3_40_2 e_1_3_3_5_2 e_1_3_3_7_2 e_1_3_3_9_2 e_1_3_3_27_2 e_1_3_3_29_2 e_1_3_3_23_2 e_1_3_3_48_2 e_1_3_3_25_2 e_1_3_3_46_2 e_1_3_3_1_2 e_1_3_3_44_2 e_1_3_3_3_2 e_1_3_3_21_2 e_1_3_3_42_2 e_1_3_3_51_2 e_1_3_3_17_2 e_1_3_3_38_2 e_1_3_3_13_2 e_1_3_3_36_2 e_1_3_3_15_2 e_1_3_3_34_2 e_1_3_3_32_2 e_1_3_3_55_2 e_1_3_3_11_2 e_1_3_3_30_2 e_1_3_3_53_2 Donald PA (e_1_3_3_19_2) 2006; 38 Colgrove AL (e_1_3_3_22_2) 2008; 40 e_1_3_3_6_2 e_1_3_3_8_2 e_1_3_3_28_2 e_1_3_3_49_2 e_1_3_3_24_2 e_1_3_3_47_2 e_1_3_3_26_2 e_1_3_3_45_2 e_1_3_3_2_2 e_1_3_3_20_2 e_1_3_3_43_2 e_1_3_3_4_2 e_1_3_3_41_2 |
References_xml | – ident: e_1_3_3_4_2 doi: 10.1038/nature02076 – ident: e_1_3_3_13_2 doi: 10.1126/science.aaa5267 – ident: e_1_3_3_1_2 doi: 10.1038/nrm2002 – ident: e_1_3_3_55_2 doi: 10.1101/gr.849004 – ident: e_1_3_3_24_2 doi: 10.1094/MPMI-18-0593 – ident: e_1_3_3_37_2 doi: 10.1146/annurev.phyto.43.011205.141140 – ident: e_1_3_3_15_2 doi: 10.1016/j.pbi.2011.03.012 – ident: e_1_3_3_21_2 doi: 10.1111/mec.13138 – ident: e_1_3_3_25_2 doi: 10.1091/mbc.7.5.693 – ident: e_1_3_3_6_2 doi: 10.1073/pnas.1115146109 – ident: e_1_3_3_29_2 doi: 10.1074/jbc.M111.278358 – ident: e_1_3_3_9_2 doi: 10.1104/pp.114.235952 – ident: e_1_3_3_45_2 doi: 10.1007/s11103-012-9932-z – ident: e_1_3_3_17_2 doi: 10.1016/j.pbi.2008.04.003 – ident: e_1_3_3_2_2 doi: 10.1038/nsmb.1451 – ident: e_1_3_3_27_2 doi: 10.1091/mbc.e07-05-0498 – volume: 38 start-page: 76 year: 2006 ident: e_1_3_3_19_2 article-title: Assessing Heterodera glycines-resistant and susceptible cultivar yield response publication-title: J Nematol contributor: fullname: Donald PA – ident: e_1_3_3_16_2 doi: 10.1146/annurev.phyto.43.040204.140218 – ident: e_1_3_3_5_2 doi: 10.1146/annurev-cellbio-100913-013439 – ident: e_1_3_3_54_2 doi: 10.1016/S0092-8674(00)80512-7 – ident: e_1_3_3_52_2 doi: 10.1104/pp.011742 – ident: e_1_3_3_12_2 doi: 10.1038/nature14148 – ident: e_1_3_3_49_2 doi: 10.1038/nmeth.2019 – ident: e_1_3_3_3_2 doi: 10.1093/pcp/pcu046 – ident: e_1_3_3_41_2 doi: 10.1186/1471-2229-11-5 – ident: e_1_3_3_42_2 doi: 10.1073/pnas.1211757110 – ident: e_1_3_3_36_2 doi: 10.1146/annurev-phyto-080614-115928 – ident: e_1_3_3_50_2 doi: 10.1371/journal.pgen.1005200 – ident: e_1_3_3_11_2 doi: 10.1074/jbc.M113.489807 – ident: e_1_3_3_47_2 doi: 10.1007/s00122-016-2779-y – ident: e_1_3_3_31_2 doi: 10.1104/pp.110.171785 – ident: e_1_3_3_35_2 doi: 10.1126/science.1236011 – ident: e_1_3_3_44_2 doi: 10.1371/journal.pone.0145601 – ident: e_1_3_3_53_2 doi: 10.1007/978-1-59745-196-3_6 – ident: e_1_3_3_32_2 doi: 10.1038/nature08670 – ident: e_1_3_3_20_2 doi: 10.2135/cropsci2004.1121 – ident: e_1_3_3_14_2 doi: 10.1073/pnas.1506409112 – ident: e_1_3_3_48_2 doi: 10.1111/tpj.13240 – ident: e_1_3_3_46_2 doi: 10.4161/15592324.2014.977737 – ident: e_1_3_3_18_2 doi: 10.1007/s00425-013-1923-z – ident: e_1_3_3_40_2 doi: 10.1094/MPMI-05-12-0128-CR – ident: e_1_3_3_38_2 doi: 10.1038/30006 – ident: e_1_3_3_10_2 doi: 10.1083/jcb.139.4.875 – ident: e_1_3_3_26_2 doi: 10.1091/mbc.e03-02-0097 – ident: e_1_3_3_34_2 doi: 10.1097/00001756-200105250-00015 – ident: e_1_3_3_8_2 doi: 10.1126/science.1228746 – ident: e_1_3_3_39_2 doi: 10.1073/pnas.1505665112 – ident: e_1_3_3_33_2 doi: 10.1038/ng1302 – ident: e_1_3_3_7_2 doi: 10.1111/j.1462-5822.2008.01238.x – volume: 40 start-page: 39 year: 2008 ident: e_1_3_3_22_2 article-title: Correlation of female indices from virulence assays on inbred lines and field populations of Heterodera glycines publication-title: J Nematol contributor: fullname: Colgrove AL – ident: e_1_3_3_28_2 doi: 10.1016/j.febslet.2007.03.032 – ident: e_1_3_3_51_2 doi: 10.1046/j.1365-313X.1999.00552.x – ident: e_1_3_3_23_2 doi: 10.1094/PHP-2008-0118-01-RS – ident: e_1_3_3_30_2 doi: 10.1105/tpc.12.11.2201 – ident: e_1_3_3_43_2 doi: 10.1104/pp.110.167536 |
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Snippet | α-SNAP [soluble NSF (N-ethylmaleimide–sensitive factor) attachment protein] and NSF proteins are conserved across eukaryotes and sustain cellular vesicle... α-SNAP [soluble NSF (N-ethylmaleimide-sensitive factor) attachment protein] and NSF proteins are conserved across eukaryotes and sustain cellular vesicle... The Rhg1 resistance locus of soybean helps control one of the most damaging diseases in world agriculture. We found that Rhg1 (resistance to Heterodera... |
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SubjectTerms | Animals Biological Sciences Disease Resistance Glycine max - genetics Glycine max - metabolism Glycine max - parasitology Mutation N-Ethylmaleimide-Sensitive Proteins - metabolism Nematoda - physiology Plant Diseases - parasitology Plant Proteins - genetics Plant Proteins - metabolism PNAS Plus Protein Binding Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins - genetics Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins - metabolism Transport Vesicles - metabolism |
Title | Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1 |
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