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Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines

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Abstract

A Glycine max syntaxin 31 homolog (Gm-SYP38) was identified as being expressed in nematode-induced feeding structures known as syncytia undergoing an incompatible interaction with the plant parasitic nematode Heterodera glycines. The observed Gm-SYP38 expression was consistent with prior gene expression analyses that identified the alpha soluble NSF attachment protein (Gm-α-SNAP) resistance gene because homologs of these genes physically interact and function together in other genetic systems. Syntaxin 31 is a protein that resides on the cis face of the Golgi apparatus and binds α-SNAP-like proteins, but has no known role in resistance. Experiments presented here show Gm-α-SNAP overexpression induces Gm-SYP38 transcription. Overexpression of Gm-SYP38 rescues G. max [Williams 82/PI 518671], genetically rhg1 −/−, by suppressing H. glycines parasitism. In contrast, Gm-SYP38 RNAi in the rhg1 +/+ genotype G. max [Peking/PI 548402] increases susceptibility. Gm-α-SNAP and Gm-SYP38 overexpression induce the transcriptional activity of the cytoplasmic receptor-like kinase BOTRYTIS INDUCED KINASE 1 (Gm-BIK1-6) which is a family of defense proteins known to anchor to membranes through a 5′ MGXXXS/T(R) N-myristoylation sequence. Gm-BIK1-6 had been identified previously by RNA-seq experiments as expressed in syncytia undergoing an incompatible reaction. Gm-BIK1-6 overexpression rescues the resistant phenotype. In contrast, Gm-BIK1-6 RNAi increases parasitism. The analysis demonstrates a role for syntaxin 31-like genes in resistance that until now was not known.

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Acknowledgments

This publication was made possible by the start-up support of Mississippi State University and the Department of Biological Sciences (DBS). The authors thank Dr. Larry Heatherly, the Mississippi Soybean Promotion Board and the soybean growers in the state of Mississippi for their continued support. The work is supported jointly between the College of Arts and Sciences (DBS) and the Mississippi Agricultural and Forestry Experimental Station (MAFES). The authors thank George Hopper, Reuben Moore and Wes Burger (MAFES) whose support has made the work possible. Dr. Scott Willard, Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology (BMEP) at Mississippi State University provided greenhouse space. Additional greenhouse space was provided by Dr. Mike Phillips and managed through Eric Laiche of the Department of Plant and Soil Sciences at Mississippi State University. The authors thank Dr. Giselle Thibaudeau and Amanda Lawrence, Imaging and Analytical Technologies Center, Mississippi State University for imaging expertise and technical suggestions. Postdoctoral research support was provided to Aparna Krishnavajhala, through a competitive Special Research Initiative grant awarded by MAFES. Yixiu Pinnix (BMEP) provided technical support. Undergraduate research support was provided by Nishi Sunthwal, Christina Jones, Suchit Salian, Priyanka Gadre, Dollie Welch, Kim Anderson, John Clune, Hannah Burson, Chase Robinson, Brittany Ginn and Meghan Calhoun (DBS) and by James McKibben, Cody Roman and Micah Schneider (BMEP). The Shackouls Honors College is acknowledged. Further support was provided by the Office of Research and Economic Development, Mississippi State University through a competitive Research Initiation Program grant. The authors acknowledge Clarissa Balbalian, (BMEP) and Dr. Tom Allen, Delta Research and Extension Center (MAFES), Stoneville, MS for support during the course of the work. VPK acknowledges Dr. Ben Matthews and Dr. Perry Cregan at the USDA-ARS (Beltsville, MD) for support throughout the process that led to the present work. Dr. Katheryn Lawrence, Auburn University graciously provided support related to the work.

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  1. Department of Biological Sciences, Mississippi State University, Mississippi State, MS, 39762, USA

    Shankar R. Pant, Prachi D. Matsye, Brant T. McNeece, Keshav Sharma, Aparna Krishnavajhala & Vincent P. Klink

  2. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, 39762, USA

    Aparna Krishnavajhala & Gary W. Lawrence

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  1. Shankar R. Pant
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11103_2014_172_MOESM1_ESM.tif

Effect of G. max SYP38 and BIK1-6 RNAi on root growth. For all experiments, * = statistically significant p < 0.05. Control, roots transformed with the pRAP17 RNAi vector. SYP38-RNAi (n = 19); SYP38-RNAi roots, p = 0.499081; BIK1-6-RNAi (n = 19); BIK1-RNAi roots, p = 0.354595. Note: RNAi had no statistically significant effect (TIFF 4118 kb)

11103_2014_172_MOESM2_ESM.tif

RNAi of G. max SYP38 and BIK1-6 results in susceptibility to parasitism by H. glycines. For all experiments, * = statistically significant p < 0.05. SYP38-RNAi-R1 (n = 19); SYP38-RNAi-R1, FI = 1,200.00; p value = 0.009937*. SYP38-RNAi-R2 (n = 15); SYP38-RNAi-R2, FI = 1,538.00; p value = 0.00197416*. SYP38-RNAi-R3 (n = 11); SYP38-RNAi-R3, FI = 1063.64; p value = 0.0298544*. BIK1-6-RNAi-R1 (n = 19); BIK1-RNAi-R1, FI = 600.00; p value = 0.0174306*. BIK1-6-RNAi-R2 (n = 7); BIK1-RNAi-R2, FI = 1628.58; p value = 0.0175829*. BIK1-6-RNAi-R3 (n = 12); BIK1-RNAi-R3, FI = 1063.64; p value = 0.0348612* (TIFF 5883 kb)

11103_2014_172_MOESM3_ESM.tif

Signal peptide prediction for GmXTH43. Signal peptide was predicted using SignalP-4.1 (http://www.cbs.dtu.dk/services/SignalP/) on default (Petersen et al. 2011) (TIFF 1673 kb)

11103_2014_172_MOESM4_ESM.docx

N-glycosylation prediction for Gm-XTH43. N-glycosylation prediction using NetNGlyc 1.0 Server (http://www.cbs.dtu.dk/services/NetNGlyc/) on default. N-glycosylation was predicted for Gm-XTH43 (DOCX 18 kb)

11103_2014_172_MOESM5_ESM.docx

Gm-BIK1 paralogs having the MGXXXS/T N-myristoylation consensus sequence (highlighted in cyan). Accessions identified from http://phytozome.net/ (DOCX 18 kb)

PCR and qPCR primers (XLSX 14 kb)

11103_2014_172_MOESM7_ESM.xlsx

G. max homologs. SYP38, XTH43, NPR1-2, EDS1-2 and BIK1-6. Number scheme is based on chromosome positions, starting at nucleotide 1 on chromosome 1 and ending on the final nucleotide on chromosome 20. Accessions were identified at http://phytozome.net/ (XLSX 14 kb)

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Pant, S.R., Matsye, P.D., McNeece, B.T. et al. Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines . Plant Mol Biol 85, 107–121 (2014). https://doi.org/10.1007/s11103-014-0172-2

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