Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat

Nature Genetics volume 51, pages 1099–1105 (2019)Cite this article

Subjects

Abstract

Fusarium head blight (FHB), which is mainly caused by Fusarium graminearum, is a destructive wheat disease that threatens global wheat production. Fhb1, a quantitative trait locus discovered in Chinese germplasm, provides the most stable and the largest effect on FHB resistance in wheat. Here we show that TaHRC, a gene that encodes a putative histidine-rich calcium-binding protein, is the key determinant of Fhb1-mediated resistance to FHB. We demonstrate that TaHRC encodes a nuclear protein conferring FHB susceptibility and that a deletion spanning the start codon of this gene results in FHB resistance. Identical sequences of the TaHRC-R allele in diverse accessions indicate that Fhb1 had a single origin, and phylogenetic and haplotype analyses suggest that the TaHRC-R allele most likely originated from a line carrying the Dahongpao haplotype. This discovery opens a new avenue to improve FHB resistance in wheat, and possibly in other cereal crops, by manipulating TaHRC sequence through bioengineering approaches.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Fine mapping and cloning of Fhb1.
Fig. 2: Determination of TaHRC as a candidate for Fhb1.
Fig. 3: Haplotype and association analyses in natural populations identify the deletion in TaHRC as the likely causal mutation for Fhb1.
Fig. 4: Characterization of TaHRC.

Data availability

RNA-seq data are available from the NCBI Sequence Read Archive under accession PRJNA515933. Additional data generated or analyzed during this study are included in this article and its supplementary information files.

References

  1. Buerstmayr, H., Ban, T. & Anderson, J. A. QTL mapping and marker‐assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed. 128, 1–26 (2009).

    Article  CAS  Google Scholar 

  2. Bai, G. & Shaner, G. Management and resistance in wheat and barley to Fusarium head blight. Annu. Rev. Phytopathol. 42, 135–161 (2004).

    Article  CAS  Google Scholar 

  3. Xu, X. & Nicholson, P. Community ecology of fungal pathogens causing wheat head blight. Annu. Rev. Phytopathol. 47, 83–103 (2009).

    Article  CAS  Google Scholar 

  4. Dean, R. et al. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13, 414–430 (2012).

    Article  Google Scholar 

  5. Pestka, J. J. & Smolinski, A. T. Deoxynivalenol: toxicology and potential effects on humans. J. Toxicol. Environ. Health B Crit. Rev. 8, 39–69 (2005).

    Article  CAS  Google Scholar 

  6. van Egmond, H. P., Schothorst, R. C. & Jonker, M. A. Regulations relating to mycotoxins in food. Anal. Bioanal. Chem. 389, 147–157 (2007).

    Article  CAS  Google Scholar 

  7. Pestka, J. J. Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 84, 663–679 (2010).

    Article  CAS  Google Scholar 

  8. McMullen, M. et al. A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Dis. 96, 1712–1728 (2012).

    Article  Google Scholar 

  9. Chakraborty, S. & Newton, A. C. Climate change, plant diseases and food security: an overview. Plant Pathol. 60, 2–14 (2011).

    Article  Google Scholar 

  10. Del Ponte, E. M., Fernandes, J., Pavan, W. & Baethgen, W. E. A model‐based assessment of the impacts of climate variability on Fusarium head blight seasonal risk in southern Brazil. J. Phytopath. 157, 675–681 (2009).

    Article  Google Scholar 

  11. Zhang, X. et al. Climate change increases risk of Fusarium ear blight on wheat in central China. Ann. Appl. Biol. 164, 384–395 (2014).

    Article  Google Scholar 

  12. Cuthbert, P. A., Somers, D. J., Thomas, J., Cloutier, S. & Brulé-Babel, A. Fine mapping Fhb1, a major gene controlling Fusarium head blight resistance in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 112, 1465–1472 (2006).

    Article  CAS  Google Scholar 

  13. Yang, Z. P. et al. Marker assisted selection of Fusarium head blight resistance genes in two doubled haploid populations of wheat. Mol. Breed. 12, 309–317 (2003).

    Article  CAS  Google Scholar 

  14. Zhou, W., Kolb, F. L., Bai, G., Shaner, G. & Domier, L. L. Genetic analysis of scab resistance QTL in wheat with microsatellite and AFLP markers. Genome 45, 719–727 (2002).

    Article  CAS  Google Scholar 

  15. Anderson, J. A. et al. DNA markers for Fusarium head blight resistance QTLs in two wheat populations. Theor. Appl. Genet. 102, 1164–1168 (2001).

    Article  CAS  Google Scholar 

  16. Waldron, B., Moreno-Sevilla, B., Anderson, J., Stack, R. & Frohberg, R. RFLP mapping of QTL for Fusarium head blight resistance in wheat. Crop Sci. 39, 805–811 (1999).

    Article  CAS  Google Scholar 

  17. Bai, G., Kolb, F. L., Shaner, G. & Domier, L. L. Amplified fragment length polymorphism markers linked to a major quantitative trait locus controlling scab resistance in wheat. Phytopathology 89, 343–348 (1999).

    Article  CAS  Google Scholar 

  18. Pumphrey, M. O., Bernardo, R. & Anderson, J. A. Validating the QTL for Fusarium head blight resistance in near-isogenic wheat lines developed from breeding populations. Crop Sci. 47, 200–206 (2007).

    Article  CAS  Google Scholar 

  19. Bernardo, A. N., Ma, H., Zhang, D. & Bai, G. Single nucleotide polymorphism in wheat chromosome region harboring Fhb1 for Fusarium head blight resistance. Mol. Breed. 29, 477–488 (2012).

    Article  Google Scholar 

  20. Jin, F. et al. Fusarium head blight resistance in US winter wheat cultivars and elite breeding lines. Crop Sci. 53, 2006–2013 (2013).

    Article  Google Scholar 

  21. Schweiger, W. et al. Suppressed recombination and unique candidate genes in the divergent haplotype encoding Fhb1, a major Fusarium head blight resistance locus in wheat. Theor. Appl. Genet. 129, 1607–1623 (2016).

    Article  CAS  Google Scholar 

  22. Rawat, N. et al. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat. Genet. 48, 1576–1580 (2016).

    Article  CAS  Google Scholar 

  23. Yang, J., Bai, G. & Shaner, G. E. Novel quantitative trait loci (QTL) for Fusarium head blight resistance in wheat cultivar Chokwang. Theor. Appl. Genet. 111, 1571–1579 (2005).

    Article  CAS  Google Scholar 

  24. Paux, E. et al. A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322, 101–104 (2008).

    Article  CAS  Google Scholar 

  25. Choulet, F. et al. Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22, 1686–1701 (2010).

    Article  CAS  Google Scholar 

  26. Hofstad, A. N. et al. Examining the transcriptional response in wheat near-isogenic lines to infection and deoxynivalenol treatment. Plant Genome 9, 1 (2016).

    Article  CAS  Google Scholar 

  27. Jia, H., Cho, S. & Muehlbauer, G. J. Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and -susceptible alleles. Mol. Plant-Microbe Inter. 22, 1366–1378 (2009).

    Article  CAS  Google Scholar 

  28. Wu, L. et al. Stripe rust resistance gene Yr18 and its suppressor gene in Chinese wheat landraces. Plant Breed. 134, 634–640 (2015).

    Article  CAS  Google Scholar 

  29. Lin, F. et al. Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419 × Wangshuibai population. I: Type II resistance. Theor. Appl. Genet. 109, 1504–1511 (2004).

    Article  CAS  Google Scholar 

  30. White, P. J. & Broadley, M. R. Calcium in plants. Annu. Bot. 92, 487–511 (2003).

    Article  CAS  Google Scholar 

  31. Wang, Y. et al. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat. Biotechnol. 32, 947–951 (2014).

    Article  CAS  Google Scholar 

  32. Fukuoka, S. et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325, 998–1001 (2009).

    Article  CAS  Google Scholar 

  33. Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl Acad. Sci. USA 107, 13544–13549 (2010).

    Article  CAS  Google Scholar 

  34. Shi, G. et al. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 2, e1600822 (2016).

    Article  Google Scholar 

  35. van Schie, C. C. & Takken, F. L. Susceptibility genes 101: how to be a good host. Annu. Rev. Phytopathol. 52, 551–581 (2014).

    Article  Google Scholar 

  36. Kugler, K. G. et al. Quantitative trait loci-dependent analysis of a gene co-expression network associated with Fusarium head blight resistance in bread wheat (Triticum aestivum L.). BMC Genomics 14, 1 (2013).

    Article  Google Scholar 

  37. Kang, J. et al. Exotic scab resistance quantitative trait loci effects on soft red winter wheat. Crop Sci. 51, 924–933 (2011).

    Article  Google Scholar 

  38. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    Article  CAS  Google Scholar 

  39. Bai, G. H., Shaner, G. & Ohm, H. Inheritance of resistance to Fusarium graminearum in wheat. Theor. Appl. Genet. 100, 1–8 (2000).

    Article  Google Scholar 

  40. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).

    Article  Google Scholar 

  41. Pearson, W. R., Wood, T., Zhang, Z. & Miller, W. Comparison of DNA sequences with protein sequences. Genomics 46, 24–36 (1997).

    Article  CAS  Google Scholar 

  42. Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859–1875 (2005).

    Article  CAS  Google Scholar 

  43. International Wheat Genome Sequencing Consortium (IWGSC). A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345, 1251788 (2014).

    Article  Google Scholar 

  44. Trapnell, C. et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).

    Article  CAS  Google Scholar 

  45. Miki, D. & Shimamoto, K. Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 45, 490–495 (2004).

    Article  CAS  Google Scholar 

  46. Cruz, L. F., Rupp, J. L. S., Trick, H. N. & Fellers, J. P. Stable resistance to wheat streak mosaic virus in wheat mediated by RNAi. In Vitro Cell. Dev. Biol. Plant 50, 665–672 (2014).

    Article  CAS  Google Scholar 

  47. Christensen, A. H. & Quail, P. H. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Trans. Res. 5, 213–218 (1996).

    Article  CAS  Google Scholar 

  48. Anand, A., Trick, H. N., Gill, B. S. & Muthukrishnan, S. Stable transgene expression and random gene silencing in wheat. Plant Biotechnol. J. 1, 241–251 (2003).

    Article  CAS  Google Scholar 

  49. Zhai, Z., Sooksa-nguan, T. & Vatamaniuk, O. K. Establishing RNA interference as a reverse-genetic approach for gene functional analysis in protoplasts. Plant Physiol. 149, 642–652 (2009).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by US Department of Agriculture US Wheat and Barley Scab Initiative and National Research Initiative competitive grants 2017-67007-25939 and 2017-67007-25929 from the USDA National Institute of Food and Agriculture. We thank W. Wang for excellent technical support. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer. This is contribution number 16-129-J from the Kansas Agricultural Experiment Station.

Author information

Authors and Affiliations

  1. Department of Agronomy, Kansas State University, Manhattan, KS, USA

    Zhenqi Su, Hui Chen, Shan Wang, Hongxiang Ma, Shibin Cai, Dongtao Liu, Dadong Zhang, Tao Li & Guihua Bai

  2. Institute of Cereal and Oil Crops, Hebei Academy of Agricultural and Forestry Sciences, Shijiazhuang, China

    Zhenqi Su

  3. Department of Plant Pathology, Kansas State University, Manhattan, KS, USA

    Amy Bernardo, Bin Tian & Harold Trick

  4. Institute of Food Crops, Jiangsu Academy of Agricultural Science, Nanjing, China

    Hongxiang Ma & Shibin Cai

  5. Agriculture College, Yangzhou University, Yangzhou, China

    Tao Li

  6. USDA–ARS, Hard Winter Wheat Genetics Research Unit, Manhattan, KS, USA

    Paul St. Amand & Guihua Bai

  7. Department of Agronomy, Iowa State University, Ames, IA, USA

    Jianming Yu

  8. Crop Instutute, Chinese Academy of Agricultural Science, Beijing, China

    Zengyan Zhang

Authors
  1. Zhenqi Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy Bernardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongxiang Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shibin Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dongtao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dadong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Harold Trick
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Paul St. Amand
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jianming Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Zengyan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Guihua Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.B. designed the research. Z.S., A.B., B.T., H.M., H.C., S.C., D.Z. and T.L. performed the research with support from G.B., H.T. and P.S.A. D.L., J.Y., Z.Z. and S.W. analyzed data. G.B. and H.T. contributed new reagents and analytic tools. G.B. and Z.S. wrote the paper. All authors contributed to revision of the manuscript.

Corresponding author

Correspondence to Guihua Bai.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–11

Reporting Summary

Supplementary Table 1

Primers used for fine mapping, gene cloning, association mapping, diagnostic marker development and gene transformation

Supplementary Table 2

A list of genes in the Fhb1 region based on the reference sequence of Chinese Spring and CM82036

Supplementary Table 3

Differentially expressed genes between Fhb1 NILs that were identified by RNA-seq and mapped on chromosome 3B

Supplementary Table 4

List of names, identification numbers (IDs), sources of wheat accessions and sequence polymorphisms in TaHRC

Supplementary Table 5

Haplotype distribution of the three candidate genes across 1,632 wheat accessions from 73 countries worldwide

Supplementary Table 6

Comparison of FHB resistance among haplotypes Hap_Ning, Hap_DHP and Hap_ND

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, Z., Bernardo, A., Tian, B. et al. A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nat Genet 51, 1099–1105 (2019). https://doi.org/10.1038/s41588-019-0425-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41588-019-0425-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing