The syntaxin 31-induced gene, LESION SIMULATING DISEASE1 (LSD1), functions in<i>Glycine max</i>defense to the root parasite<i>Heterodera glycines</i>

Pant, Shankar R.; Krishnavajhala, Aparna; McNeece, Brant T.; Lawrence, Gary W.; Klink, Vincent P.

doi:10.4161/15592324.2014.977737

Cited by 18 publications

(38 citation statements)

References 98 publications

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“…A study of virulent SCN populations that had recently evolved to reproduce on soybeans carrying high-copy Rhg1 haplotypes demonstrated allelic imbalance of a SNARE-like effector protein in the nematode (44). Other recent reports suggest that a naturally occurring truncated soybean α-SNAP enhances SCN resistance through increasing transcription of a Golgi-localized SNARE, syntaxin-31 (45,46). The amino acid sequence of that truncated α-SNAP indicates it is encoded by Glyma.11G234500 on chromosome 11, and hence potential functional overlaps with Rhg1-encoded α-SNAPs on chromosome 18 are unclear (9).…”

Section: Discussionmentioning

confidence: 99%

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

Bayless

Smith

Song

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

154

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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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Section: Discussionmentioning

confidence: 99%

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

Bayless

Smith

Song

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

154

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“…Prior experiments have demonstrated the functioning of the G. max syntaxin 31 (Gm-SYP38), which is homologous to the S. cerevisiae suppressors of the erd2-deletion 5 protein (Sed5p), in the root during its resistance to H. glycines parasitism (Hardwick & Pelham 1992;Sanderfoot et al 2000;Pant et al 2014Pant et al , 2015a. The results of those experiments have led to the development of a model predicting the involvement of other SNARE genes including the G. max homolog of PEN1 Pant et al 2014).…”

Section: Discussionmentioning

confidence: 99%

“…In the analysis presented here, these opposite outcomes are engineered resistance in the normally H. glycines-susceptible G. max [Williams 82/PI 518671] and engineered impairment of resistance in the normally H. glycines-resistant G. max [Peking/PI 548402] (Pant et al 2014(Pant et al , 2015a. A control experiment targeting coatomer zeta (Cζ) has been designed to prove the specificity of the pRAP vector system (Kuge et al 1993;Klink et al 2009b;Matsye et al 2012;Matthews et al 2013).…”

Section: Demonstration Of the Specificity Of The Prap Vector Systemmentioning

confidence: 99%

“…The objective of using the complimentary approaches of gene overexpression and RNAi in studying a developmental process is that the combined opposite outcomes, respectfully, are hallmarks of the involvement of the gene in the process (Zhou et al 2005;Baena-González et al 2007;Pant et al 2014;Sun et al 2014;Dóczi et al 2015). In the analysis presented here, these opposite outcomes are engineered resistance in the normally H. glycines-susceptible G. max [Williams 82/PI 518671] and engineered impairment of resistance in the normally H. glycines-resistant G. max [Peking/PI 548402] (Pant et al 2014(Pant et al , 2015a.…”

Section: Demonstration Of the Specificity Of The Prap Vector Systemmentioning

confidence: 99%

“…Little information exists for an involvement of these genes in plant resistance to root pathogens except for the identification of a natural variant of α-SNAP functioning in some capacity in the defense of Glycine max (soybean) to its root pathogen the parasitic nematode Heterodera glycines (Matsye et al 2012). In this pathosystem, the overexpression of the α-SNAP variant is accompanied by elevated transcript levels of syntaxin 31 which resides on the cis face of the Golgi apparatus (Hardwick & Pelham 1992;Lupashin et al 1997;Bubeck et al 2008;Matsye et al 2012;Pant et al 2014). Therefore, SNARE components function in the defense of G. max to H. glycines parasitism and are co-regulated.…”

Section: Introductionmentioning

confidence: 99%

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Co-regulation of theGlycine maxsoluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor (SNARE)-containing regulon occurs during defense to a root pathogen

Sharma

Pant

McNeece

et al. 2016

Journal of Plant Interactions

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Genes functioning in membrane fusion were originally identified genetically in Saccharomyces cerevisiae and are found in all eukaryotes. Components of the unit, soluble N-ethylmaleimidesensitive fusion protein attachment protein receptor (SNARE), function in the plant genetic model Arabidopsis thaliana during its defense to shoot pathogens. Regarding defense, little is understood about SNARE in roots or its regulation. Experiments in Glycine max (soybean) have provided an opportunity to perform such studies, revealing that SNARE genes are expressed under natural conditions in root cells undergoing defense to parasitism by the nematode Heterodera glycines. Presented here, the G. max homolog of S. cerevisiae suppressor of sec1 (SSO1), identified genetically in A. thaliana as PENETRATION1 (PEN1) and named in its genomic annotation as syntaxin 121 (SYP121) functions in the resistance of G. max to H. glycines. Genetic experiments demonstrate Gm-SYP121 is co-expressed with homologs of other SNARE genes exhibiting measurable transcript levels in infected cells undergoing resistance. These genes include synaptosomal-associated protein 25, homologous to A. thaliana SNAP33 (SNAP-25/SNAP33/SEC9); mammalian uncoordinated-18 (MUNC18/SEC1); synaptotagmin/tricalbin-3 (SYT/TCB3); synaptobrevin/vesicle associated membrane protein/YKT6/SEC22 (SYB/VAMP/YKT6/SEC22); N-ethylmaleimide-sensitive fusion protein (NSF/SEC18) and alpha-soluble N-ethylmaleimide-sensitive fusion protein associated protein (α-SNAP/SEC17). Experiments show each SNARE component functions in resistance. In contrast, a coatomer zeta/ retrieval3 (Cζ/RET3) homolog known to function in retrograde transport within and between the Golgi and endoplasmic reticulum does not appear to function in resistance. Experiments show that SNARE is co-regulated along with a β-glucosidase having homology to PEN2 and an ATP binding cassette transporter exhibiting homology to PEN3. ARTICLE HISTORY

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GILP family: a stress-responsive group of plant proteins containing a LITAF motif

Cabreira-Cagliari

Fagundes

Dias

et al. 2017

Funct Integr Genomics

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Lipopolysaccharide-induced tumor necrosis factor-α (LITAF) is a membrane protein that is highly dependent on correct location to exert transcription factor activity and protein quality control. In humans, LITAF, PIG7 (p53-inducible gene 7), and SIMPLE (small integral membrane protein of the lysosome/late endosome) refer to the same gene, which acts as a tumor suppressor. Several studies have shown that the transcription factor activity and nuclear translocation of LITAF protein are critical for the induction of several immune cells via classical pathways. In plants, LITAF protein corresponds to the plasma membrane protein AtGILP (Arabidopsis thaliana GSH-induced LITAF domain protein). The conservation of LITAF proteins across species and their putative role is still unclear. In this study, we investigate the LITAF-containing proteins, which we call GILP proteins, in Viridiplantae. We identified a total of 59 genes in 46 species, whose gene copies range from one to three. Phylogenetic analysis showed that multiple copies were originated via block duplication posteriorly to monocot and eudicot separation. Analysis of the LITAF domain of GILP proteins allowed the identification of a putative domain signature in Viridiplantae, containing a CXXCX41HXCPXC motif. The subcellular location for the majority of GILP proteins was predicted to be in the plasma membrane, based on a transmembrane domain positioned within the LITAF domain. In silico analysis showed that the GILP genes are neither tissue-specific nor ubiquitously expressed, being responsive to stress conditions. Finally, investigation of the GILP protein network resulted in the identification of genes whose families are known to be involved with biotic and/or abiotic stress responses. Together, the expression modulation of GILP genes associated with their plasma membrane location suggests that they could act in the signaling of biotic/abiotic stress response in plants.

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The syntaxin 31-induced gene, LESION SIMULATING DISEASE1 (LSD1), functions inGlycine maxdefense to the root parasiteHeterodera glycines

Cited by 18 publications

References 98 publications

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

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

Co-regulation of theGlycine maxsoluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor (SNARE)-containing regulon occurs during defense to a root pathogen

GILP family: a stress-responsive group of plant proteins containing a LITAF motif

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