CoChat
Sign Up
Cited by 38Wheat and Barley Genetics and PathologyPlant-Microbe Interactions and ImmunityPlant Disease Resistance and Genetics

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

A pathogen-induced putative NAC transcription factor mediates leaf rust resistance in barley

Open access
Chen, Chunhong, Jost, Matthias, Outram, Megan A., Friendship, Dorian, Chen, Jian, Wang, Aihua, Periyannan, Sambasivam, Bartoš, Jan, Holušová, Kateřina, Doležel, Jaroslav, Zhang, Peng, Bhatt, Dhara, Singh, Davinder, Lagudah, Evans, Park, Robert F., Dracatos, Peter M.·2023·Nature Communications
DOI 10.1038/s41467-023-41021-2PMC PMC10482968

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Leaf rust, caused by Puccinia hordei , is one of the most widespread and damaging foliar diseases affecting barley. The barley leaf rust resistance locus Rph7 has been shown to have unusually high sequence and haplotype divergence. In this study, we isolate the Rph7 gene using a fine mapping and RNA-Seq approach that is confirmed by mutational analysis and transgenic complementation. Rph7 is a pathogen-induced, non-canonical resistance gene encoding a protein that is distinct from other known plant disease resistance proteins in the Triticeae. Structural analysis using an AlphaFold2 protein model suggests that Rph7 encodes a putative NAC transcription factor with a zinc-finger BED domain with structural similarity to the N-terminal DNA-binding domain of the NAC transcription factor (ANAC019) from Arabidopsis . A global gene expression analysis suggests Rph7 mediates the activation and strength of the basal defence response. The isolation of Rph7 highlights the diversification of resistance mechanisms available for engineering disease control in crops.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-023-41021-2

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 54

  1. Dracatos, P. M., Lu, J., Sánchez-Martín, J. & Wulff, B. B. H. Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley. Plant Biotechnol. J. https://doi.org/10.1111/pbi.14106 (2023). · DOI
  2. Cotterill, P., Rees, R., Platz, G. & Dill-Macky, R. Effects of leaf rust on selected Australian barleys. Aust. J. Exp. Agric. 32, 747–751 (1992). · DOI
  3. Park, R. F. et al. Leaf rust of cultivated barley: pathology and control. Annu. Rev. Phytopathol. 53, 565–589 (2015). · DOI
  4. 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). · DOI
  5. Dracatos, P. M., Singh, D., Bansal, U. & Park, R. F. Identification of new sources of adult plant resistance to Puccinia hordei in international barley (Hordeum vulgare L.) germplasm. Eur. J. Plant Pathol. 141, 463–476 (2015). · DOI
  6. Elmansour, H., Singh, D., Dracatos, P. M. & Park, R. F. Identification and characterization of seedling and adult plant resistance to Puccinia hordei in selected African barley germplasm. Euphytica 213, 119 (2017). · DOI
  7. Singh, D., Dracatos, P. M., Loughman, R. & Park, R. F. Genetic mapping of resistance to Puccinia hordei in three barley doubled-haploid populations. Euphytica 213, 16 (2016).
  8. Singh, D. et al. Genome-wide association studies provide insights on genetic architecture of resistance to leaf rust in a worldwide barley collection. Mol. Breed. 38, 43 (2018). · DOI
  9. Rothwell, C. T., Singh, D., Dracatos, P. M. & Park, R. F. Inheritance and dharacterization of Rph27: A third race-specific resistance gene in the barley cultivar Quinn. Phytopathology 110, 1067–1073 (2020). · DOI
  10. Jost, M., Singh, D., Lagudah, E., Park, R. F. & Dracatos, P. Fine mapping of leaf rust resistance gene Rph13 from wild barley. Theor. Appl. Genet. 133, 1887–1895 (2020). · DOI
  11. Mehnaz, M. et al. A novel locus conferring resistance to Puccinia hordei maps to the genomic region corresponding to Rph14 on barley chromosome 2HS. Front. Plant Sci. 13, 980870 (2022). · DOI
  12. Mehnaz, M. et al. Discovery and fine mapping of Rph28: a new gene conferring resistance to Puccinia hordei from wild barley. Theor. Appl. Genet. 134, 2167–2179 (2021). · DOI
  13. Dracatos, P. M. et al. The coiled-coil NLR Rph1, confers leaf rust resistance in barley cultivar Sudan. Plant Physiol. 179, 1362–1372 (2019). · DOI
  14. Wang, Y. et al. Orthologous receptor kinases quantitatively affect the host status of barley to leaf rust fungi. Nat. Plants 5, 1129–1135 (2019). · DOI
  15. Chen, Y. et al. A collinearity-incorporating homology inference dtrategy for vonnecting emerging assemblies in the triticeae tribe as a pilot practice in the plant pangenomic era. Mol. Plant 13, 1694–1708 (2020). · DOI
  16. Dinh, H. X. et al. The barley leaf rust resistance gene Rph3 encodes a predicted membrane protein and is induced upon infection by avirulent pathotypes of Puccinia hordei. Nat. Commun. 13, 2386 (2022).
  17. Dinh, H. X., Singh, D., Periyannan, S., Park, R. F. & Pourkheirandish, M. Molecular genetics of leaf rust resistance in wheat and barley. Theor. Appl. Genet. 133, 2035–2050 (2020). · DOI
  18. Zhou, J.-M. & Zhang, Y. Plant immunity: danger perception and signaling. Cell 181, 978–989 (2020). · DOI
  19. Zhang, J., Zhang, P., Dodds, P. & Lagudah, E. How target-sequence enrichment and sequencing (TEnSeq) pipelines have catalyzed resistance gene cloning in the wheat-eust pathosystem. Front. Plant Sci. 11, 678 (2020). · DOI
  20. Sánchez-Martín, J. & Keller, B. NLR immune receptors and diverse types of non-NLR proteins control race-specific resistance in Triticeae. Curr. Opin. Plant Biol. 62, 102053 (2021). · DOI
  21. Kolodziej, M. C. et al. A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat. Nat. Commun. 12, 956 (2021). · DOI
  22. Roane, C. & Starling, T. Inheritance of reaction to Puccinia hordei in barley. III. Genes in the cultivars Cebada Capa and Franger. Phytopathology 57, 66–68 (1970).
  23. Shtaya, M. J. Y., Sillero, J. C. & Rubiales, D. Identification of a new pathotype of Puccinia hordei with virulence for the resistance gene Rph7. Eur. J. Plant Pathol. 116, 103–106 (2006). · DOI
  24. Golan, T., Anikster, Y., Moseman, J. G. & Wahl, I. A new virulent strain of Puccinia hordei. Euphytica 27, 185–189 (1978). · DOI
  25. Steffenson, B. J. et al. Pathotypes of Puccinia hordei with virulence for the barley leaf rustresistance gene Rph7 in the United-States. Plant Dis. 77, 867–869 (1993). · DOI
  26. Tuleen, N. & McDaniel, M. Location of genes Pa and Pa5. Barley Newsl. 15, 106–107 (1971).
  27. Graner, A. et al. Molecular mapping of the leaf rust resistance gene Rph7 in barley. Plant Breed. 119, 389–392 (2000). · DOI
  28. Brunner, S., Keller, B. & Feuillet, C. A large rearrangement involving genes and low-copy DNA interrupts the microcollinearity between rice and barley at the Rph7 locus. Genetics 164, 673–683 (2003). · DOI
  29. Scherrer, B. et al. Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17, 361–374 (2005). · DOI
  30. Walkowiak, S. et al. Multiple wheat genomes reveal global variation in modern breeding. Nature 588, 277–283 (2020). · DOI
  31. Sánchez-Martín, J. et al. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. Genome Biol. 17, 221 (2016). · DOI
  32. Jayakodi, M. et al. The barley pan-genome reveals the hidden legacy of mutation breeding. Nature 588, 284–289 (2020). · DOI · Paper page
  33. Holm, L. Dali server: structural unification of protein families. Nucleic Acids Res. 50, W210–W215 (2022). · DOI
  34. Welner, D. H. et al. DNA binding by the plant-specific NAC transcription factors in crystal and solution: a firm link to WRKY and GCM transcription factors. Biochem. J. 444, 395–404 (2012). · DOI
  35. Gilmour, J. Octal notation for designating physiologic races of plant pathogens. Nature 242, 620–620 (1973). · DOI
  36. Park, R. F. & Karakousis, A. Characterization and mapping of gene Rph19 conferring resistance to Puccinia hordei in the cultivar ‘Reka 1’ and several Australian barleys. Plant Breed. 121, 232–236 (2002). · DOI
  37. Chandler, P. M. & Harding, C. A. ‘Overgrowth’ mutants in barley and wheat: new alleles and phenotypes of the ‘Green Revolution’ DELLA gene. J. Exp. Bot. 64, 1603–1613 (2013). · DOI
  38. Chen, C. et al. BED domain-containing NLR from wild barley confers resistance to leaf rust. Plant Biotechnol. J. 19, 1206–1215 (2021). · DOI
  39. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). · DOI · Paper page
  40. Monat, C. et al. TRITEX: chromosome-scale sequence assembly of Triticeae genomes with open-source tools. Genome Biol. 20, 284 (2019). · DOI · Paper page
  41. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
  42. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). · DOI · Paper page
  43. Danecek, P. et al. Twelve years of SAMtools and BCFtools. GigaScience 10, giab008 (2021). · DOI
  44. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011). · DOI
  45. Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12, 323 (2011).
  46. Mascher, M. et al. Long-read sequence assembly: a technical evaluation in barley. Plant Cell 33, 1888–1906 (2021). · DOI
  47. Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019). · DOI · Paper page
  48. Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015). · DOI · Paper page
  49. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
  50. Pettersen, E. F. et al. UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021). · DOI
  51. Ortiz, D. et al. The stem rust effector protein AvrSr50 escapes Sr50 recognition by a substitution in a single surface-exposed residue. New Phytol. 234, 592–606 (2022). · DOI
  52. Upadhyaya, N. M. et al. Genomics accelerated isolation of a new stem rust avirulence gene-wheat resistance gene pair. Nat. Plants 7, 1220–1228 (2021). · DOI
  53. Saur, I. M. L. et al. A cell death assay in barley and wheat protoplasts for identification and validation of matching pathogen AVR effector and plant NLR immune receptors. Plant Methods 15, 118 (2019).
  54. Luo, M. et al. A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol. 39, 561–566 (2021). · DOI

Metadata

Authors
Chen, C., Jost, M., Outram, M. A., Friendship, D., Chen, J., Wang, A., Periyannan, S., Bartoš, J., Holušová, K., Doležel, J., Zhang, P., Bhatt, D., Singh, D., Lagudah, E., Park, R. F., & Dracatos, P. M.
Affiliations
  • Commonwealth Scientific and Industrial Research Organisation (AU)
  • The University of Sydney (AU)
  • Czech Academy of Sciences, Institute of Experimental Botany (CZ)
Corresponding author
  • Lagudah, Evans
  • Park, Robert F.
  • Dracatos, Peter M.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2023-09-06
Volume
14
Issue
1
Pages
5468-5468
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-023-41021-2
PMC
PMC10482968
OpenAlex
W4386476389
Cited by
38
References
1
Citations by year
2026: 8 · 2025: 18 · 2024: 11 · 2023: 1
FWCI
6.12
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • La Trobe University (cc-by)
Funders
Grains Research and Development Corporation (US00074)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Wheat and Barley Genetics and Pathology
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Disease Resistance and Genetics
Keywords
barley leaf rust, Puccinia hordei, NAC transcription factors, fine mapping, transgenic complementation, gene expression, disease resistance engineering, Triticeae
MeSH terms
Hordeum, Basidiomycota, Eczema, Gene Expression Regulation, Poaceae, Plant Diseases, Plant Proteins, Transcription Factors, Arabidopsis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review