A Giant NLR Gene Confers Broad-spectrum Resistance to Phytophthora Sojae in Soybean

Overview

Journal Nat Commun

Specialty Biology

Date 2021 Nov 6

PMID 34741017

Citations 36

Authors

Weidong Wang

Liyang Chen

Kevin Fengler

Joy Bolar

Victor Llaca

Xutong Wang

Chancelor B Clark

Tomara J Fleury

Jon Myrvold

David ONeal

Maria Magdalena van Dyk

Ashley Hudson

Jesse Munkvold

Andy Baumgarten

Jeff Thompson

Guohong Cai

Oswald Crasta

Rajat Aggarwal

Jianxin Ma

Affiliations

Soon will be listed here.

Abstract

Phytophthora root and stem rot caused by P. sojae is a destructive soybean soil-borne disease found worldwide. Discovery of genes conferring broad-spectrum resistance to the pathogen is a need to prevent the outbreak of the disease. Here, we show that soybean Rps11 is a 27.7-kb nucleotide-binding site-leucine-rich repeat (NBS-LRR or NLR) gene conferring broad-spectrum resistance to the pathogen. Rps11 is located in a genomic region harboring a cluster of large NLR genes of a single origin in soybean, and is derived from rounds of unequal recombination. Such events result in promoter fusion and LRR expansion that may contribute to the broad resistance spectrum. The NLR gene cluster exhibits drastic structural diversification among phylogenetically representative varieties, including gene copy number variation ranging from five to 23 copies, and absence of allelic copies of Rps11 in any of the non-Rps11-donor varieties examined, exemplifying innovative evolution of NLR genes and NLR gene clusters.

Citing Articles

Fine mapping of the unique Ur-11 gene conferring broad resistance to the rust pathogen of common bean.

Valentini G, Hurtado-Gonzales O, Xavier L, He R, Gill U, Song Q Theor Appl Genet. 2025; 138(3):64.

PMID: 40035870 DOI: 10.1007/s00122-025-04856-5.

The genomic landscape of gene-level structural variations in Japanese and global soybean Glycine max cultivars.

Yano R, Li F, Hiraga S, Takeshima R, Kobayashi M, Toda K Nat Genet. 2025; .

PMID: 40033060 DOI: 10.1038/s41588-025-02113-5.

Transcriptome Comparison between Resistant and Susceptible Soybean Cultivars in Response to Inoculation of Phytophthora sojae.

Shim S, Kang I, You H, Kim H, Lee S Plant Pathol J. 2024; 40(6):641-655.

PMID: 39639668 PMC: 11626037. DOI: 10.5423/PPJ.OA.09.2024.0154.

Soybean genomics research community strategic plan: A vision for 2024-2028.

Stupar R, Locke A, Allen D, Stacey M, Ma J, Weiss J Plant Genome. 2024; 17(4):e20516.

PMID: 39572930 PMC: 11628913. DOI: 10.1002/tpg2.20516.

Chromosome-specific barcode system with centromeric repeat in cultivated soybean and wild progenitor.

Tek A, Nagaki K, Yildiz Akkamis H, Tanaka K, Kobayashi H Life Sci Alliance. 2024; 7(12).

PMID: 39353738 PMC: 11447526. DOI: 10.26508/lsa.202402802.

References

Nagy E, Bennetzen J . Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res. 2008; 18(12):1918-23. PMC: 2593579. DOI: 10.1101/gr.078766.108. View

Hufford M, Seetharam A, Woodhouse M, Chougule K, Ou S, Liu J . De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science. 2021; 373(6555):655-662. PMC: 8733867. DOI: 10.1126/science.abg5289. View

Schmutz J, Cannon S, Schlueter J, Ma J, Mitros T, Nelson W . Genome sequence of the palaeopolyploid soybean. Nature. 2010; 463(7278):178-83. DOI: 10.1038/nature08670. View

Abney T, Melgar J, Richards T, Scott D, Grogan J, Young J . New Races of Phytophthora sojae with Rps1-d Virulence. Plant Dis. 2019; 81(6):653-655. DOI: 10.1094/PDIS.1997.81.6.653. View

DeYoung B, Innes R . Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol. 2006; 7(12):1243-9. PMC: 1973153. DOI: 10.1038/ni1410. View

Van de Weyer A, Monteiro F, Furzer O, Nishimura M, Cevik V, Witek K . A Species-Wide Inventory of NLR Genes and Alleles in Arabidopsis thaliana. Cell. 2019; 178(5):1260-1272.e14. PMC: 6709784. DOI: 10.1016/j.cell.2019.07.038. View

Jones J, Vance R, Dangl J . Intracellular innate immune surveillance devices in plants and animals. Science. 2016; 354(6316). DOI: 10.1126/science.aaf6395. View

Dorrance A, Schmitthenner A . New Sources of Resistance to Phytophthora sojae in the Soybean Plant Introductions. Plant Dis. 2019; 84(12):1303-1308. DOI: 10.1094/PDIS.2000.84.12.1303. View

Ou S, Liu J, Chougule K, Fungtammasan A, Seetharam A, Stein J . Effect of sequence depth and length in long-read assembly of the maize inbred NC358. Nat Commun. 2020; 11(1):2288. PMC: 7211024. DOI: 10.1038/s41467-020-16037-7. View

10.

Gao H, Bhattacharyya M . The soybean-Phytophthora resistance locus Rps1-k encompasses coiled coil-nucleotide binding-leucine rich repeat-like genes and repetitive sequences. BMC Plant Biol. 2008; 8:29. PMC: 2330051. DOI: 10.1186/1471-2229-8-29. View

11.

Koren S, Walenz B, Berlin K, Miller J, Bergman N, Phillippy A . Canu: scalable and accurate long-read assembly via adaptive -mer weighting and repeat separation. Genome Res. 2017; 27(5):722-736. PMC: 5411767. DOI: 10.1101/gr.215087.116. View

12.

Chu J, Peng B, Tang K, Yi X, Zhou H, Wang H . Eight soybean reference genome resources from varying latitudes and agronomic traits. Sci Data. 2021; 8(1):164. PMC: 8249447. DOI: 10.1038/s41597-021-00947-2. View

13.

Ping J, Liu Y, Sun L, Zhao M, Li Y, She M . Dt2 is a gain-of-function MADS-domain factor gene that specifies semideterminacy in soybean. Plant Cell. 2014; 26(7):2831-42. PMC: 4145117. DOI: 10.1105/tpc.114.126938. View

14.

Dobin A, Davis C, Schlesinger F, Drenkow J, Zaleski C, Jha S . STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2012; 29(1):15-21. PMC: 3530905. DOI: 10.1093/bioinformatics/bts635. View

15.

Walker B, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S . Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014; 9(11):e112963. PMC: 4237348. DOI: 10.1371/journal.pone.0112963. View

16.

Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S . Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell. 1999; 11(7):1365-76. PMC: 144280. DOI: 10.1105/tpc.11.7.1365. View

17.

Steuernagel B, Witek K, Krattinger S, Ramirez-Gonzalez R, Schoonbeek H, Yu G . The NLR-Annotator Tool Enables Annotation of the Intracellular Immune Receptor Repertoire. Plant Physiol. 2020; 183(2):468-482. PMC: 7271791. DOI: 10.1104/pp.19.01273. View

18.

Sun Q, Collins N, Ayliffe M, Smith S, Drake J, Pryor T . Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics. 2001; 158(1):423-38. PMC: 1461629. DOI: 10.1093/genetics/158.1.423. View

19.

Ping J, Fitzgerald J, Zhang C, Lin F, Bai Y, Wang D . Identification and molecular mapping of Rps11, a novel gene conferring resistance to Phytophthora sojae in soybean. Theor Appl Genet. 2015; 129(2):445-51. DOI: 10.1007/s00122-015-2638-2. View

20.

McHale L, Tan X, Koehl P, Michelmore R . Plant NBS-LRR proteins: adaptable guards. Genome Biol. 2006; 7(4):212. PMC: 1557992. DOI: 10.1186/gb-2006-7-4-212. View