Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi

Abstract

Global food security depends on cereal crops with durable disease resistance. Most cereals are colonized by rust fungi, which are pathogens of major significance for global agriculture1. Cereal rusts display a high degree of host specificity and one rust species or forma specialis generally colonizes only one cereal host2. Exploiting the non-host status and transferring non-host resistance genes between cereal crop species has been proposed as a strategy for durable rust resistance breeding. The molecular determinants that define the host status to rusts, however, are largely unknown. Here, we show that orthologous genes at the Rphq2 locus for quantitative leaf rust resistance from cultivated barley3 and Rph22 from wild bulbous barley4 affect the host status to leaf rusts. Both genes encode lectin receptor-like kinases. We transformed Rphq2 and Rph22 into an experimental barley line that has been bred for susceptibility to non-adapted leaf rusts, which allowed us to quantify resistance responses against various leaf rust species. Rphq2 conferred a much stronger resistance to the leaf rust of wild bulbous barley than to the leaf rust adapted to cultivated barley, while for Rph22 the reverse was observed. We hypothesize that adapted leaf rust species mitigate perception by cognate host receptors by lowering ligand recognition. Our results provide an example of orthologous genes that connect the quantitative host with non-host resistance to cereal rusts. Such genes provide a basis to exploit non-host resistance in molecular breeding.

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Fig. 1: Rphq2 and Rph22 phenotype and mapping.
Fig. 2: Resistance mediated by Hv-LecRK and Hb-LecRK is stronger against non-adapted than against adapted leaf rust species.
Fig. 3: Molecular characterization of Hv-LecRK and Hb-LecRK proteins.

Data availability

All data are available in the main text or the Supplementary Information. GenBank accession numbers: MK512576MK512578, MK530949, MK530950, MK569504 and MN128516MN128521.

References

  1. 1.

    Savary, S. et al. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3, 430–439 (2019).

  2. 2.

    Dracatos, P. M., Haghdoust, R., Singh, D. & Park, R. F. Exploring and exploiting the boundaries of host specificity using the cereal rust and mildew models. New Phytol. 218, 453–462 (2018).

  3. 3.

    Yeo, F. K. et al. Haplotype divergence and multiple candidate genes at Rphq2, a partial resistance QTL of barley to Puccinia hordei. Theor. Appl. Genet. 129, 289–304 (2016).

  4. 4.

    Johnston, P. A., Niks, R. E., Meiyalaghan, V., Blanchet, E. & Pickering, R. Rph22: mapping of a novel leaf rust resistance gene introgressed from the non-host Hordeum bulbosum L. into cultivated barley (Hordeum vulgare L.). Theor. Appl. Genet. 126, 1613–1625 (2013).

  5. 5.

    Jones, J. D., Vance, R. E. & Dangl, J. L. Intracellular innate immune surveillance devices in plants and animals. Science 354, aaf6395 (2016).

  6. 6.

    Dardick, C. & Ronald, P. Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog. 2, e2 (2006).

  7. 7.

    Mogensen, T. H. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 22, 240–273 (2009).

  8. 8.

    Lee, H. A. et al. Current understandings of plant nonhost resistance. Mol. Plant Microbe Interact. 30, 5–15 (2017).

  9. 9.

    Fonseca, J. P. & Mysore, K. S. Genes involved in nonhost disease resistance as a key to engineer durable resistance in crops. Plant Sci. 279, 108–116 (2019).

  10. 10.

    Schulze-Lefert, P. & Panstruga, R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16, 117–125 (2011).

  11. 11.

    Niks, R. E. & Marcel, T. C. Nonhost and basal resistance: how to explain specificity? New Phytol. 182, 817–828 (2009).

  12. 12.

    Cevik, V. et al. Transgressive segregation reveals mechanisms of Arabidopsis immunity to Brassica-infecting races of white rust (Albugo candida). Proc. Natl Acad. Sci. USA 116, 2767–2773 (2019).

  13. 13.

    Anikster, Y. Host specificity versus plurivority in barley leaf rusts and their microcyclic relatives. Mycol. Res. 93, 175–181 (1989).

  14. 14.

    Blattner, F. R. Multiple intercontinental dispersals shaped the distribution area of Hordeum (Poaceae). New Phytol. 169, 603–614 (2006).

  15. 15.

    Bettgenhaeuser, J. et al. The genetic architecture of colonization resistance in Brachypodium distachyon to non-adapted stripe rust (Puccinia striiformis) isolates. PLoS Genet. 14, e1007637 (2018).

  16. 16.

    Atienza, S. G., Jafary, H. & Niks, R. E. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta 220, 71–79 (2004).

  17. 17.

    Jafary, H., Albertazzi, G., Marcel, T. C. & Niks, R. E. High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics 178, 2327–2339 (2008).

  18. 18.

    Gilbert, B. et al. Components of Brachypodium distachyon resistance to nonadapted wheat stripe rust pathogens are simply inherited. PLoS Genet. 14, e1007636 (2018).

  19. 19.

    Qi, X., Niks, R. E., Stam, P. & Lindhout, P. Identification of QTLs for partial resistance to leaf rust (Puccinia hordei) in barley. Theor. Appl. Genet. 96, 1205–1215 (1998).

  20. 20.

    Marcel, T. C., Aghnoum, R., Durand, J., Varshney, R. K. & Niks, R. E. Dissection of the barley 2L1.0 region carrying the ‘Laevigatum’ quantitative resistance gene to leaf rust using near-isogenic lines (NIL) and subNIL. Mol. Plant Microbe Interact. 20, 1604–1615 (2007).

  21. 21.

    Yeo, F. K. et al. Golden SusPtrit: a genetically well transformable barley line for studies on the resistance to rust fungi. Theor. Appl. Genet. 127, 325–337 (2014).

  22. 22.

    Hurni, S. et al. The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proc. Natl Acad. Sci. USA 112, 8780–8785 (2015).

  23. 23.

    Wang, Y. et al. Arabidopsis lectin receptor kinases LecRK-IX.1 and LecRK-IX.2 are functional analogs in regulating Phytophthora resistance and plant cell death. Mol. Plant Microbe Interact. 28, 1032–1048 (2015).

  24. 24.

    Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343, 290–294 (2014).

  25. 25.

    Kutschera, A. et al. Bacterial medium-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364, 178–181 (2019).

  26. 26.

    Bouwmeester, K. et al. The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog. 7, e1001327 (2011).

  27. 27.

    Wang, Y. & Bouwmeester, K. L-type lectin receptor kinases: new forces in plant immunity. PloS Pathog. 13, e1006433 (2017).

  28. 28.

    Wulff, B. B. & Moscou, M. J. Strategies for transferring resistance into wheat: from wide crosses to GM cassettes. Front. Plant Sci. 5, 692 (2014).

  29. 29.

    Inoue, Y. et al. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357, 80–83 (2017).

  30. 30.

    Parlevliet, J. E. Evaluation of the concept of horizontal resistance in the barley/Puccinia hordei host– pathogen relationship. Phytopathology 66, 494–497 (1976).

  31. 31.

    Martinez, F., Niks, R. E., Moral, A., Urbano, J. M. & Rubiales, D. Search for partial resistance to leaf rust in a collection of ancient Spanish wheats. Hereditas 135, 193–197 (2001).

  32. 32.

    Niks, R.E., Parlevliet, J.E., Lindhout, P. & Bai, Y. Breeding Crops with resistance to diseases and pests (Wageningen Academic, 2011).

  33. 33.

    Parlevliet, J. E. Partial resistance of barley to leafrust, Puccinia hordei. I. Effect of cultivar and development stage on latent period. Euphytica 24, 21–27 (1975).

  34. 34.

    Barnes, C. W. & Szabo, L. J. Detection and identification of four common rust pathogens of cereals and grasses using real-time polymerase chain reaction. Phytopathology 97, 717–727 (2007).

  35. 35.

    Zheng, Z. et al. Loss of function in Mlo orthologs reduces susceptibility of pepper and tomato to powdery mildew disease caused by Leveillula taurica. PLoS ONE 8, e70723 (2013).

  36. 36.

    Mascher, M. et al. A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427–433 (2017).

  37. 37.

    Ochman, H., Gerber, A. S. & Hartl, D. L. Genetic applications of an inverse polymerase chain reaction. Genetics 120, 621–623 (1988).

  38. 38.

    Nakagawa, T. et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41 (2007).

  39. 39.

    Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S. & Mullineaux, P. M. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819–832 (2000).

  40. 40.

    Hensel, G., Kastner, C., Oleszczuk, S., Riechen, J. & Kumlehn, J. Agrobacterium-mediated gene transfer to cereal crop plants: current protocols for barley, wheat, Triticale, and maize. Int. J. Plant Genomics 2009, 835608 (2009).

  41. 41.

    Larkin, M. A. et al. Clustal W and Clustal X v.2.0. Bioinformatics 23, 2947–2948 (2007).

  42. 42.

    Felsenstein, J. PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 5, 164–166 (1989).

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Acknowledgements

We thank J. Bucher (Wageningen University & Research) for producing the time-lapse video, Y. Jiang (King Abdullah University of Science and Technology) for advising on the Rphq2/Rph22 functional analyses, and J. Rajaraman (IPK Gatersleben) for providing the plasma membrane marker plasmid. This publication is based on work supported by the King Abdullah University of Science and Technology Office of Sponsored Research under Award No. OSR-CRG2018-3768 (to Y.W. and S.G.K.), the New Zealand Institute for Plant & Food Research Limited Strategic Science Investment Fund (to P.A.J.), National Natural Science Foundation of China grant no. 31471756 (to X.Q.), and NWO-ALW (file number 849.13.002) as part of the ERA-CAPS project DURESTrit 13.006 (to Y.W.).

Author information

Y.W., X.Q., R.E.N. and S.G.K. designed research. Y.W., S.S., H.d.V., P.D. and P.A.J. performed molecular experiments. Y.W., S.S., H.d.V., P.D., A.V. and R.E.N. performed rust inoculations and phenotypic scorings. G.H. and J.K. stably transformed the barley line Golden SusPtrit. Y.W. and I.B. performed subcellular localization. Y.W., R.E.N. and S.G.K. wrote the paper. All authors have read and approved the manuscript.

Correspondence to Rients E. Niks or Simon G. Krattinger.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Peter Dracatos, Kirankumar Mysore and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–12, Supplementary Tables 1 and 2, and legend for the Supplementary Video.

Reporting Summary

Supplementary Video

Time-lapse video showing P. hordei development on barley plants expressing Rphq2 and Rph22.

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Wang, Y., Subedi, S., de Vries, H. et al. Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi. Nat. Plants 5, 1129–1135 (2019). https://doi.org/10.1038/s41477-019-0545-2

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