Genome editing of an African elite rice variety confers resistance against endemic and emerging Xanthomonas oryzae pv. oryzae strains

  1. Van Schepler-Luu
  2. Coline Sciallano
  3. Melissa Stiebner
  4. Chonghui Ji
  5. Gabriel Boulard
  6. Amadou Diallo
  7. Florence Auguy
  8. Si Nian Char
  9. Yugander Arra
  10. Kyrylo Schenstnyi
  11. Marcel Buchholzer
  12. Eliza PI Loo
  13. Atugonza L Bilaro
  14. David Lihepanyama
  15. Mohammed Mkuya
  16. Rosemary Murori
  17. Ricardo Oliva
  18. Sebastien Cunnac
  19. Bing Yang
  20. Boris Szurek  Is a corresponding author
  21. Wolf B Frommer  Is a corresponding author
  1. Heinrich Heine University Düsseldorf, Germany
  2. Université Montpellier, France
  3. University of Missouri, United States
  4. Tanzania Agricultural Research Institute (TARI)-Uyole Centre, United Republic of Tanzania
  5. International Rice Research Institute, Kenya
  6. World Vegetable Center, Taiwan

Abstract

Bacterial leaf blight (BB) of rice, caused by Xanthomonas oryzae pv. oryzae (Xoo), threatens global food security and the livelihood of small-scale rice producers. Analyses of Xoo collections from Asia, Africa and the Americas demonstrated complete continental segregation, despite robust global rice trade. Here, we report unprecedented BB outbreaks in Tanzania. The causative strains, unlike endemic African Xoo, carry Asian-type TAL effectors targeting the sucrose transporter SWEET11a and iTALes suppressing Xa1. Phylogenomics clustered these strains with Xoo from Southern-China. African rice varieties do not carry effective resistance. To protect African rice production against this emerging threat, we developed a hybrid CRISPR-Cas9/Cpf1 system to edit all known TALe-binding elements in three SWEET promoters of the East African elite variety Komboka. The edited lines show broad-spectrum resistance against Asian and African strains of Xoo, including strains recently discovered in Tanzania. The strategy could help to protect global rice crops from BB pandemics.

Data availability

All data supporting the results are available in the main text or supplementary materials. All data that support the findings of this study were included in the manuscript; raw data are available at Dryad (https://doi.org/10.5061/dryad.xpnvx0kk3; Summary of raw data files deposited at dryad is provided in Source_data_overview deposited raw data @dryad). Sequencing data for strains from this study have been deposited in the NCBI Sequence Read Archive (SRA) database (Accession codes for iTz strains are provided in Supplementary File 2 - Tabs 1 and 2). Source data have deposited at Dryad. Materials will be made available under MTA.

The following data sets were generated

Article and author information

Author details

  1. Van Schepler-Luu

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
  2. Coline Sciallano

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8988-7733
  3. Melissa Stiebner

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8626-0951
  4. Chonghui Ji

    Division of Plant Science and Technology, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  5. Gabriel Boulard

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    Competing interests
    No competing interests declared.
  6. Amadou Diallo

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    Competing interests
    No competing interests declared.
  7. Florence Auguy

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    Competing interests
    No competing interests declared.
  8. Si Nian Char

    Division of Plant Science and Technology, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5759-0764
  9. Yugander Arra

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6778-4258
  10. Kyrylo Schenstnyi

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1595-6382
  11. Marcel Buchholzer

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7485-6918
  12. Eliza PI Loo

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    No competing interests declared.
  13. Atugonza L Bilaro

    Tanzania Agricultural Research Institute (TARI)-Uyole Centre, Mbeya, United Republic of Tanzania
    Competing interests
    No competing interests declared.
  14. David Lihepanyama

    Tanzania Agricultural Research Institute (TARI)-Uyole Centre, Mbeya, United Republic of Tanzania
    Competing interests
    No competing interests declared.
  15. Mohammed Mkuya

    Eastern and Southern Africa Region, International Rice Research Institute, Nairobi, Kenya
    Competing interests
    No competing interests declared.
  16. Rosemary Murori

    Africa Regional Office, International Rice Research Institute, Nairobi, Kenya
    Competing interests
    No competing interests declared.
  17. Ricardo Oliva

    World Vegetable Center, Tainan, Taiwan
    Competing interests
    No competing interests declared.
  18. Sebastien Cunnac

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    Competing interests
    No competing interests declared.
  19. Bing Yang

    Division of Plant Science and Technology, University of Missouri, Columbia, United States
    Competing interests
    No competing interests declared.
  20. Boris Szurek

    Plant Health Institute of Montpellier, Université Montpellier, Montpellier, France
    For correspondence
    boris.szurek@ird.fr
    Competing interests
    No competing interests declared.
  21. Wolf B Frommer

    Institute for Molecular Physiology, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    For correspondence
    frommew@hhu.de
    Competing interests
    Wolf B Frommer, The Healthy Crops team has filed for patents (PCT/US20 12/071722: Genetically modified plants with resistance to Xanthomonas and other bacterial plant pathogens; PCT/US20 10/033535: Novel sugar transporters; US 2011/0201118 A1: Nuclease activity of TAL effector and Fok1 fusion protein; PCT/EP2020/059893: Diagnostic Kit and method for SWEET-based rice blight resistance and resistant breeding lines), but is charitable and non-profit and aims at helping small scale rice farmers in Asia and Africa by reducing yield losses caused by pathogens . The authors declare no competing interests..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6465-0115

Funding

Bill and Melinda Gates Foundation (OPP1155704)

  • Wolf B Frommer

Alexander von Humboldt-Stiftung (Professorship)

  • Wolf B Frommer

Deutsche Forschungsgemeinschaft (EXC-2048/1 - project ID 390686111)

  • Wolf B Frommer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Schepler-Luu et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,176
    views
  • 354
    downloads
  • 12
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Van Schepler-Luu
  2. Coline Sciallano
  3. Melissa Stiebner
  4. Chonghui Ji
  5. Gabriel Boulard
  6. Amadou Diallo
  7. Florence Auguy
  8. Si Nian Char
  9. Yugander Arra
  10. Kyrylo Schenstnyi
  11. Marcel Buchholzer
  12. Eliza PI Loo
  13. Atugonza L Bilaro
  14. David Lihepanyama
  15. Mohammed Mkuya
  16. Rosemary Murori
  17. Ricardo Oliva
  18. Sebastien Cunnac
  19. Bing Yang
  20. Boris Szurek
  21. Wolf B Frommer
(2023)
Genome editing of an African elite rice variety confers resistance against endemic and emerging Xanthomonas oryzae pv. oryzae strains
eLife 12:e84864.
https://doi.org/10.7554/eLife.84864

Share this article

https://doi.org/10.7554/eLife.84864

Further reading

    1. Microbiology and Infectious Disease
    Vivian C Salgueiro-Toledo, Jorge Bertol ... Rafael Prados-Rosales
    Research Article

    Pathogenic and nonpathogenic mycobacteria secrete extracellular vesicles (EVs) under various conditions. EVs produced by Mycobacterium tuberculosis (Mtb) have raised significant interest for their potential in cell communication, nutrient acquisition, and immune evasion. However, the relevance of vesicle secretion during tuberculosis infection remains unknown due to the limited understanding of mycobacterial vesicle biogenesis. We have previously shown that a transposon mutant in the LCP-related gene virR (virRmut) manifested a strong attenuated phenotype during experimental macrophage and murine infections, concomitant to enhanced vesicle release. In this study, we aimed to understand the role of VirR in the vesicle production process in Mtb. We employ genetic, transcriptional, proteomics, ultrastructural, and biochemical methods to investigate the underlying processes explaining the enhanced vesiculogenesis phenomenon observed in the virRmut. Our results establish that VirR is critical to sustain proper cell permeability via regulation of cell envelope remodeling possibly through the interaction with similar cell envelope proteins, which control the link between peptidoglycan and arabinogalactan. These findings advance our understanding of mycobacterial extracellular vesicle biogenesis and suggest that these set of proteins could be attractive targets for therapeutic intervention.