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Soybean ( Glycine max (L.) Merr.) is an important crop that provides a sustainable source of protein and oil worldwide. Soybean cyst nematode ( Heterodera glycines Ichinohe) is a microscopic roundworm that feeds on the roots of soybean and is a major constraint to soybean production. This nematode causes more than US$1 billion in yield losses annually in the United States alone, making it the most economically important pathogen on soybean. Although planting of resistant cultivars forms the core management strategy for this pathogen, nothing is known about the nature of resistance. Moreover, the increase in virulent populations of this parasite on most known resistance sources necessitates the development of novel approaches for control.

Here we report the map-based cloning of a gene at the Rhg4 (for resistance to Heterodera glycines 4) locus, a major quantitative trait locus contributing to resistance to this pathogen. Mutation analysis, gene silencing and transgenic complementation confirm that the gene confers resistance. The gene encodes a serine hydroxymethyltransferase, an enzyme that is ubiquitous in nature and structurally conserved across kingdoms. The enzyme is responsible for interconversion of serine and glycine and is essential for cellular one-carbon metabolism. Alleles of Rhg4 conferring resistance or susceptibility differ by two genetic polymorphisms that alter a key regulatory property of the enzyme.

Our discovery reveals an unprecedented plant resistance mechanism against a pathogen. The mechanistic knowledge of the resistance gene can be readily exploited to improve nematode resistance of soybean, an increasingly important global crop. & Wrather, J.

Suppression of soybean yield potential in the continental United States from plant diseases estimated from 2006 to 2009. Plant Health Prog. Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. 52, 635–636 (1960).

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A decade of QTL mapping for cyst nematode resistance in soybean. 44, 1121–1131 (2004). 5.

‘Forrest’ resistance to the soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. 103, 710–717 (2001). 6. Histological responses of resistant and susceptible soybean varieties, and backcross progeny to entry development of Heterodera glycines. Phytopathology 55, 375–381 (1965).

7. & Opperman, C. Genetic analysis of parasitism in soybean cyst nematode Heterodera glycines. Genetics 146, 1311–1318 (1997). 8. L., Colgrove, A.

L., Colgrove, K. Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Prog. A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biol. 10, 104 (2010).

10. Soybean cyst nematode resistance in soybean is independent of the Rhg4 locus LRR-RLK gene.

11, 539–549 (2011). 11. TILLING to detect induced mutations in soybean. BMC Plant Biol. 8, 9 (2008). 12.

TILLING: A reverse genetics and a functional genomics tool in soybean. In The handbook of Plant Functional Genomics: Concepts and Protocols (eds Kahl, G. & Meksem, K.) 251–265 (Wiley, 2008). 13. Impacts of genetic bottlenecks on soybean genome diversity. USA 103, 1 (2007).

14. Q., Bradshaw, J. D., Whitham, S. The development of an efficient multipurpose Bean pod mottle virus viral vector set for foreign gene expression and RNA silencing. Plant Physiol. 153, 52–65 (2010). 15.

The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol. 155, 1960–1975 (2011). Forza motorsport 6 download.

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The biological significance of substrate inhibition: A mechanism with diverse functions. Bioessays 32, 422–429 (2010). 18. Polymorphisms in the thymidylate synthase and serine hydroxymethyltransferase genes and risk of adult acute lymphocytic leukemia.

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A high-throughput automated technique for counting females of Heterodera glycines using a fluorescence-based imaging system. 42, 201–206 (2010). 33. High density integrated linkage map based on SSR markers in soybean.

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Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. 187, 1003–1017 (2010). 36. Kumar, P., Henikoff, S. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature Protocols 4, 1073–1081 (2009). 37.

Analysis of the cDNAs of hypothetical genes on Arabidopsis chromosome 2 reveals numerous transcript variants. Plant Physiol. 139, 1323–1337 (2005).

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Construction and expression of hybrid plasmids containing the Escherichia coli glyA gene. Gene 14, 63–72 (1981). Yang for technical assistance with soybean hairy root propagation and M. Kroll for proofreading the manuscript. Gresshoff, A. Bendahmane, D. McClure for critical reading of the manuscript.

Sharma and S. Puthur for use of the HPLC facility and technical help. This work was supported by the Illinois-Missouri Biotechnology Alliance (project 2005-3 to M.G.M. And K.M.), United Soybean Board (project 0253 to K.M., S.C.

And M.G.M.; project 3253 to K.M. And S.C.; project 2268 to K.M. And M.G.M; project 1251 to J.H. And S.A.W.), USDA-NIFA (grant 2006-5 to K.M.), the National Science Foundation Plant Genome Research Program (grant 0820642 to S.A.W., J.H., M.G.M. And T.J.B.), the National Science Foundation CAREER Program (DBI-0845196 to D.K.), Missouri Soybean Merchandising Council (project 258 to M.G.M.), Illinois Soybean Association, North Central Soybean Research Program, Iowa Soybean Association, and a Department of Education Graduate Assistance in Areas of National Need (GAANN) Fellowship (to S.D.W.).

Author notes. Shiming Liu.

& Pramod K. Kandoth These authors contributed equally to this work. Affiliations. Department of Plant, Soil and Agricultural Systems, Southern Illinois University, Carbondale, Illinois 62901, USA. Shiming Liu., Aziz Jamai., Tarik El-Mellouki.

& Khalid Meksem. Division of Plant Sciences, Christopher S.

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Bond Life Sciences Center and Interdisciplinary Plant Group, University of Missouri, Columbia, Missouri 65211, USA. Pramod K. Kandoth., Greg Yeckel., Robert Heinz., John Alden. & Melissa G. Mitchum. Department of Computer Science, Christopher S. Bond Life Sciences Center and Informatics Institute, University of Missouri, Columbia, Missouri 65211, USA.

Samantha D. Warren. & Dmitry Korkin. Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011, USA. Chunling Yang., Parijat S. Juvale., John Hill., Thomas J.

Baum. & Steven A. Whitham.

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Contributed equally as first authors. Contributed equally as senior authors. Carried out mapping and haplotyping studies. Developed the TILLING population used in this study.

Developed two of the RIL populations used in this study. Identified the TILLING mutants and conducted the haplotyping analysis. Carried out SCN phenotyping of all RILs, TILLING mutants, and soybean lines. Collected leaf tissues for RIL and TILLING studies. Collected leaf tissues haplotyping analyses.

Confirmed the mutations, cloned the genes, and conducted sequence analyses. P.K.K., C.Y., R.H.

Developed and carried out VIGS assays. Conducted RNAi experiments. Carried out the promoter analysis. Carried out the complementation analysis. Performed the computational analysis. Performed the biochemical studies. Provided materials and advice for VIGS analysis.

Designed the research, and together with S.L., P.K.K. Wrote the manuscript. All authors reviewed and commented on the manuscript.

Competing interests The authors declare no competing financial interests. Corresponding authors Correspondence to.