Skip to main content
Log in

The Hessian fly resistance gene HvRHF1 is localized in an NBS-LRR gene cluster in barley

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Hessian fly (Mayetiola destructor Say) is a significant pest in cereal crops, causing substantial yield losses worldwide. While host resistance is the most efficient method for pest control, research on genetic characterization of Hessian fly resistance in barley (Hordeum vulgare L.) has been limited, and the underlying resistance mechanism remains largely unknown. In this study, we conducted fine mapping of a crucial Hessian fly resistance locus, known as HvRHF1, using a biparental population. Assisted with genetic markers and robust phenotyping assay, we pinpointed the HvRHF1 gene to an ~ 82 kb region on chromosome 4H. Gene prediction and annotation revealed that the HvRHF1 locus comprises three complete NBS-LRR genes, which are characteristic of disease resistance genes. As a result, our study not only provides valuable resources for resistance in barley and genetic tools for breeding, but also identifies candidate genes that lay the foundation for cloning HvRHF1. This endeavor will significantly contribute to our understanding of the molecular mechanisms underlying cereal resistance to Hessian fly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bayer MM, Rapazote-Flores P, Ganal M, Hedley PE, Macaulay M, Plieske J, Ramsay L, Russell J, Shaw PD, Thomas W, Waugh R (2017) Development and evaluation of a barley 50k iSelect SNP array. Front Plant Sci 8:1792

    Article  PubMed  PubMed Central  Google Scholar 

  • Buntin DG, Raymer PL (1989) Hessian fly (Diptera: Cecidomyiidae) damage and forage production of winter wheat. J Econ Entomol 82:301–306

    Article  Google Scholar 

  • Buntin GD, Ott SL, Johnson JW (1992) Integration of plant resistance, insecticides, and planting date for management of the Hessian fly (Diptera: Cecidomyiidae) in winter wheat. J Econ Entomol 85:530–538

    Article  Google Scholar 

  • Chen M-S, Echegaray E, Jeffrey Whitworth R, Wang H, Sloderbeck PE, Knutson A, Giles KL, Royer TA (2009) Virulence analysis of Hessian fly populations from Texas, Oklahoma, and Kansas. J Econ Entomol 102:774–780

    Article  PubMed  Google Scholar 

  • Curtin SJ, Tiffin P, Guhlin J, Trujillo DI, Burghart LT, Atkins P, Baltes NJ, Denny R, Voytas DF, Stupar RM, Young ND (2017) Validating genome-wide association candidates controlling quantitative variation in nodulation. Plant Physiol 173:921–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci U S A 106:22163–22168

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Gagne RJ, Hatchett JH, Lhaloui S, Elbouhssini M (1991) Hessian fly and barley stem gall midge, 2 different species of Mayetiola (Diptera, Cecidomyiidae) in Morocco. Ann Entomol Soc Am 84:436–443

    Article  Google Scholar 

  • Garcés-Carrera S, Knutson A, Wang H, Giles KL, Huang F, Whitworth RJ, Smith CM, Chen M-S (2014) Virulence and biotype analyses of Hessian fly (Diptera: Cecidomyiidae) populations from Texas, Louisiana, and Oklahoma. J Econ Entomol 107:417–423

    Article  PubMed  Google Scholar 

  • Gupta PK, Kulwal PL, Jaiswal V (2019) Chapter Two - Association mapping in plants in the post-GWAS genomics era. In: Kumar D (ed) Advances in genetics. Academic Press, pp 75–154

    Google Scholar 

  • He C, Holme J, Anthony J (2014) SNP genotyping: the KASP assay. Methods Mol Biol 1145:75–86

    Article  CAS  PubMed  Google Scholar 

  • Hill CC, Cartwright WB, Wiebe GA (1952) Barley varieties resistant to the Hessian fly. Agron J 44:4–5

    Article  Google Scholar 

  • Jayakodi M, Padmarasu S, Haberer G, Bonthala VS, Gundlach H, Monat C, Lux T, Kamal N, Lang D, Himmelbach A, Ens J, Zhang XQ, Angessa TT, Zhou G, Tan C, Hill C, Wang P, Schreiber M, Boston LB, Plott C, Jenkins J, Guo Y, Fiebig A, Budak H, Xu D, Zhang J, Wang C, Grimwood J, Schmutz J, Guo G, Zhang G, Mochida K, Hirayama T, Sato K, Chalmers KJ, Langridge P, Waugh R, Pozniak CJ, Scholz U, Mayer KFX, Spannagl M, Li C, Mascher M, Stein N (2020) The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 588:284–289

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Ji H, Kim SR, Kim YH, Suh JP, Park HM, Sreenivasulu N, Misra G, Kim SM, Hechanova SL, Kim H, Lee GS, Yoon UH, Kim TH, Lim H, Suh SC, Yang J, An G, Jena KK (2016) Map-based cloning and characterization of the BPH18 gene from wild rice conferring resistance to brown planthopper (BPH) insect pest. Sci Rep 6:34376

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Kapos P, Devendrakumar KT, Li X (2019) Plant NLRs: from discovery to application. Plant Sci 279:3–18

    Article  CAS  PubMed  Google Scholar 

  • Karki M, Chu C, Anderson K, Nandety RS, Fiedler J, Schachterle J, Brueggeman RS, Liu Z, Yang S (2023) Genome-wide association study of host resistance to Hessian fly in barley. Phytopathology 1:aj3

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lhaloui S, Buschman L, El Bouhssini M, Starks K, Keith D, El Houssaini KAA (1992) Control of Mayetiola species (Diptera: Cecidomyiidae) with Carbofuran in bread wheat, durum wheat, and barley, with yield loss assessment and its economic analysis. Al Awamia 77:55–73

    Google Scholar 

  • Liu XM, Brown-Guedira GL, Hatchett JH, Owuoche JO, Chen MS (2005a) Genetic characterization and molecular mapping of a Hessian fly-resistance gene transferred from T. turgidum ssp. dicoccum to common wheat. Theor Appl Genet 111:1308–1315

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Fritz AK, Reese JC, Wilde GE, Gill BS, Chen MS (2005b) H9, H10, and H11 compose a cluster of Hessian fly-resistance genes in the distal gene-rich region of wheat chromosome 1AS. Theor Appl Genet 110:1473–1480

    Article  CAS  PubMed  Google Scholar 

  • Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607

    Article  CAS  PubMed  Google Scholar 

  • Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Simkova H, Stankova H, Vrana J, Chan S, Munoz-Amatriain M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Dolezel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433

    Article  CAS  PubMed  ADS  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  PubMed Central  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizuno H, Katagiri S, Kanamori H, Mukai Y, Sasaki T, Matsumoto T, Wu J (2020) Evolutionary dynamics and impacts of chromosome regions carrying R-gene clusters in rice. Sci Rep 10:872

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Mornhinweg DW (2010) Biotic stress in barley: insect problems and solutions. Barley, pp 355–390

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noble WB, Suneson CA (1943) Differentiation of the two genetic factors for resistance to the hessian fly in Dawson wheat. J Agric Res 67:0027–0032

    Google Scholar 

  • Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant Microbe Interact 16:645–649

    Article  CAS  PubMed  Google Scholar 

  • Olembo JR, Patterson FL, Gallun RL (1966) Genetic analyses of the resistance to Mayetiola destructor (Say) in Hordeum vulgare L. Crop. Science 6:1966

    Google Scholar 

  • Perrière G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369

  • Ramirez-Gonzalez RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31:2038–2039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapazote-Flores P, Bayer M, Milne L, Mayer CD, Fuller J, Guo W, Hedley PE, Morris J, Halpin C, Kam J, McKim SM, Zwirek M, Casao MC, Barakate A, Schreiber M, Stephen G, Zhang R, Brown JWS, Waugh R, Simpson CG (2019) BaRTv1.0: an improved barley reference transcript dataset to determine accurate changes in the barley transcriptome using RNA-seq. BMC Genomics 20:968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rashed A, Tanner C (2021) Small grain pest. In: Kaur N (ed) Pacific northwest insect management handbook. Oregon State University, Corvallis, OR, pp B21-30

    Google Scholar 

  • Ratcliffe RH, Safranski GG, Patterson FL, Ohm HW, Taylor PL (1994) Biotype status of hessian fly (Diptera, Cecidomyiidae) populations from the eastern United-States and their response to 14 Hessian fly resistance genes. J Econ Entomol 87:1113–1121

    Article  Google Scholar 

  • Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci U S A 95:9750–9754

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Sadeghi R, Odubiyi S, Nikoukar A, Schroeder KL, Rashed A (2021) Mayetiola destructor (Diptera: Cecidmyiidae) host preference and survival on small grains with respect to leaf reflectance and phytohormone concentrations. Sci Rep-Uk 11

  • Shukle RH, Subramanyam S, Saltzmann KA, Williams CE (2010) Ultrastructural changes in the midguts of Hessian fly larvae feeding on resistant wheat. J Insect Physiol 56:754–760

  • Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: join map. Plant J 3:739–744

    Article  CAS  Google Scholar 

  • Stuart JJ, Chen MS, Shukle R, Harris MO (2012) Gall midges (Hessian flies) as plant pathogens. Annu Rev Phytopathol 50:339–357

    Article  CAS  PubMed  Google Scholar 

  • Tadesse W, El-Hanafi S, El-Fakhouri K, Imseg I, Rachdad FE, El-Gataa Z, El Bouhssini M (2022) Wheat breeding for Hessian fly resistance at ICARDA. Crop J 10:1528–1535

    Article  Google Scholar 

  • Tamura Y, Hattori M, Yoshioka H, Yoshioka M, Takahashi A, Wu J, Sentoku N, Yasui H (2014) Map-based cloning and characterization of a brown planthopper resistance gene BPH26 from Oryza sativa L. ssp. indica cultivar ADR52. Sci Rep 4:5872

    Article  PubMed  PubMed Central  ADS  Google Scholar 

  • You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253

    Article  Google Scholar 

  • Zhao Y, Huang J, Wang Z, Jing S, Wang Y, Ouyang Y, Cai B, Xin XF, Liu X, Zhang C, Pan Y, Ma R, Li Q, Jiang W, Zeng Y, Shangguan X, Wang H, Du B, Zhu L, Xu X, Feng YQ, He SY, Chen R, Zhang Q, He G (2016) Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proc Natl Acad Sci U S A 113:12850–12855

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

Download references

Acknowledgements

The authors thank Kirk Anderson for the help with HF infestation and phenotyping; and Megan Overlander-Chen, Xiaohong (Sherry) Jiang, and Abby d'Eustachio for technical assistance.

Funding

This work was supported by the U.S. Department of Agriculture, Agricultural Research Service through project 3060-21000-046-000D. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. The U.S. Department of Agriculture is an equal opportunity provider and employer.

Author information

Authors and Affiliations

Authors

Contributions

SY conceived and designed the experiments. MK, MGR, and SY performed the experiments. All authors analyzed the data. All authors commented on the first draft wrote by MK and SY.

Corresponding author

Correspondence to Shengming Yang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Peter Langridge.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karki, M., Robbani, M.G., Chu, C. et al. The Hessian fly resistance gene HvRHF1 is localized in an NBS-LRR gene cluster in barley. Theor Appl Genet 137, 71 (2024). https://doi.org/10.1007/s00122-024-04581-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00122-024-04581-5

Navigation