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A head-to-head NLR gene pair from wild emmer confers stripe rust resistance in wheat

Nature Genetics volume 57, pages 1543–1552 (2025)Cite this article

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Abstract

Wheat stripe rust poses a major threat to global food security. Discovery of disease resistance genes from wild relatives enables multigene stacking that could enhance durability. Here we use map-based cloning and long-read sequencing to isolate two adjacent nucleotide-binding and leucine-rich repeat (NLR) receptors from wild emmer wheat. Using mutagenesis, gene silencing and genetic transformation, we show that the genes TdNLR1 and TdNLR2 oriented head-to-head are both required for YrTD121-mediated stripe rust resistance. TdNLR1 encodes a canonical NLR (CC-NB-ARC-LRR) protein, whereas TdNLR2 encodes an atypical one (NB-ARC-LRR). Both genes lack an integrated domain previously associated with effector perception, representing an uncommon architecture for paired NLRs in plants. The coiled coil domain of TdNLR1 triggers cell death and self-associates in planta. YrTD121 was present in wild emmer but absent in all other Triticum species examined. Our work sheds light on the function of paired NLRs in conferring disease resistance and facilitates breeding for resistance.

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Fig. 1: Map-based cloning of YrTD121.
Fig. 2: Functional validation of TdNLR1 and TdNLR2 by mutagenesis and BSMV-induced gene silencing assays.
Fig. 3: Functional validation of TdNLR1 and TdNLR2 using CRISPR–Cas9 gene editing and transgenic complementation.
Fig. 4: Phylogenetic tree based on TdNLR1, TdNLR2 and 50 cloned R proteins in cereal species.
Fig. 5: Cell death assay and self-association of the TdNLR1 CC domain.
Fig. 6: Agronomic traits of CM42 and CM42 + YrTD121.

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Data availability

Data supporting the findings of this work are available in the article and its supplementary information. The wild emmer reference genome assembly WEW_v2.1 was collected from the NCBI database under BioProject no. PRJNA310175 (ref. 52). The transcriptome raw data are available under BioProject no. PRJNA1221773. The genomic sequence of the ptg005881l contig for the YrTD121 region is available under accession no. PV110151.1. The genomic DNA sequences of TdNLR1 and TdNLR2 from TD121 are accessible under GenBank accession nos. OP948046.1 and PP874936.1. The genomic DNA sequences of other TdNLR haplotypes in this study are available under accession nos. OP948047.1–OP948060.1, accession no. OR472555.1 for TdNLR1, and accession nos. PP874937.1–PP874945.1 and PQ412542.1 for TdNLR2. Source data are provided with this paper.

Code availability

All software packages used in the study are publicly available and as described in Methods and Reporting Summary.

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Acknowledgements

We thank R. A. McIntosh (Plant Breeding Institute, University of Sydney) for the critical review of this paper; The Lady Barbara Davis Wild Cereal Gene bank, the Institute of Evolution, at the University of Haifa and Y. X. Liu for providing the seeds of wild emmer accessions TD121 (TD104059) and PI 487260, respectively; and L. L. Dong and D. D. Wu for assistance with the bioinformatics analysis. This research was supported by the National Natural Science Foundation of China (grant nos. 32272068 and 32341035 to L.H.), the National Key Research and Development Program of China (grant no. 2023YFD1200402 to Z.Y.L. and L.H.), the Key Research and Development Program of Sichuan Province (grant nos. 2021YFYZ0002 to D.C.L. and 2024YFNH0024 to L.H.), the Sichuan Provincial Agricultural Department Innovative Research Team (grant no. SCCXTD-2024-11 to D.C.L.), the State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China (grant nos. SKL-ZD202206 to L.Q.Z. and SKL-KF202322 to L.H.) and the United States-Israel Binational Agricultural Research and Development Fund (nos. IS-4628-13 and US-5515-22C to T.F.).

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Author notes

  1. These authors contributed equally: Yanling Hu, Miaomiao Li.

Authors and Affiliations

  1. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China

    Yanling Hu, Yanyan Huang, Lihua Feng, Lianquan Zhang, Bihua Wu & Lin Huang

  2. Triticeae Research Institute, Sichuan Agricultural University, Chengdu, China

    Yanling Hu, Yuqin Li, Lilin Du, Ruijie Xie, Binyang Xu, Yinghui Li, Yunfeng Jiang, Ming Hao, Bo Jiang, Shunzong Ning, Zhongwei Yuan, Dengcai Liu & Lin Huang

  3. State Key Laboratory of Seed Innovation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Miaomiao Li & Zhiyong Liu

  4. State Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Taian, China

    Fei Ni

  5. Wheat Research Institute, School of Life Sciences and Engineering, Southwest University of Science and Technology, Mianyang, China

    Chongjing Xia

  6. Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, China

    Ke Wang

  7. State Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agriculture Sciences in Weifang, Weifang, China

    Binyang Xu & Shisheng Chen

  8. Department of Evolutionary and Environmental Biology and the Institute of Evolution, University of Haifa, Mount Carmel, Israel

    Tzion Fahima

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Contributions

B.H.W., Z.Y.L., T.F., D.C.L. and L.H. conceived and designed the research. Y.L.H., L.H.F. and L.H. developed the mapping population. Y.L.H., Y.Q.L., S.Z.N., M.H. and L.Q.Z. contributed to the development of the mutant lines. Y.L.H., Y.Q.L. and R.J.X. conducted the VIGS. Y.L.H., M.M.L., L.L.D. and R.J.X. performed the gene cloning and expression analysis. K.W. performed the gene editing work. M.M.L. and Z.Y.L. performed some of the transgenic experiments. Y.L.H., M.M.L., L.H.F., B.J., Z.W.Y. and M.H. performed the field stripe rust tests and haplotype analysis of NLRs. Y.L.H., Y.Q.L. and Y.Y.H. contributed to the cell death assay and protein–protein interaction experiments. Y.L.H., M.M.L., S.S.C., B.Y.X. and C.J.X. performed the stripe rust tests in the growth chambers. F.N. and Y.F.J. performed the PacBio sequence assembly and transcriptome analysis. Y.L.H. and Y.H.L. contributed to the phylogenetic analysis. Y.L.H., L.Q.Z. and L.L.D. developed the introgression lines. Y.L.H., B.H.W., Z.Y.L., T.F., D.C.L. and L.H. wrote the paper with input from all coauthors.

Corresponding authors

Correspondence to Bihua Wu, Zhiyong Liu, Tzion Fahima, Dengcai Liu or Lin Huang.

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Competing interests

L.H., Y.L.H., D.C.L., B.H.W., L.H.F., L.Q.Z., Z.W.Y., S.Z.N. and M.H. declare using the TdNLR sequences under a China patent filing no. 202211502138.2, which are based on the results described. L.H., Y.L.H., D.C.L., B.H.W., L.Q.Z., Z.W.Y., S.Z.N. and M.H. declare competing interest in the use of the markers linked to YrTD121 under a China patent filing no. 202110932684.9. The other authors declare no competing interests.

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Hu, Y., Li, M., Li, Y. et al. A head-to-head NLR gene pair from wild emmer confers stripe rust resistance in wheat. Nat Genet 57, 1543–1552 (2025). https://doi.org/10.1038/s41588-025-02207-0

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