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The protein interactome of the citrus Huanglongbing pathogen Candidatus Liberibacter asiaticus

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  • Erica W. Carter

    (University of Florida
    University of Florida)

  • Orlene Guerra Peraza

    (University of Florida)

  • Nian Wang

    (University of Florida
    University of Florida)

Abstract

The bacterium Candidatus Liberibacter asiaticus (CLas) causes citrus Huanglongbing disease. Our understanding of the pathogenicity and biology of this microorganism remains limited because CLas has not yet been cultivated in artificial media. Its genome is relatively small and encodes approximately 1136 proteins, of which 415 have unknown functions. Here, we use a high-throughput yeast-two-hybrid (Y2H) screen to identify interactions between CLas proteins, thus providing insights into their potential functions. We identify 4245 interactions between 542 proteins, after screening 916 bait and 936 prey proteins. The false positive rate of the Y2H assay is estimated to be 2.9%. Pull-down assays for nine protein-protein interactions (PPIs) likely involved in flagellar function support the robustness of the Y2H results. The average number of PPIs per node in the CLas interactome is 15.6, which is higher than the numbers previously reported for interactomes of free-living bacteria, suggesting that CLas genome reduction has been accompanied by increased protein multi-functionality. We propose potential functions for 171 uncharacterized proteins, based on the PPI results, guilt-by-association analyses, and comparison with data from other bacterial species. We identify 40 hub-node proteins, including quinone oxidoreductase and LysR, which are known to protect other bacteria against oxidative stress and might be important for CLas survival in the phloem. We expect our PPI database to facilitate research on CLas biology and pathogenicity mechanisms.

Suggested Citation

  • Erica W. Carter & Orlene Guerra Peraza & Nian Wang, 2023. "The protein interactome of the citrus Huanglongbing pathogen Candidatus Liberibacter asiaticus," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43648-7
    DOI: 10.1038/s41467-023-43648-7
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    1. Soon Gang Choi & Julien Olivet & Patricia Cassonnet & Pierre-Olivier Vidalain & Katja Luck & Luke Lambourne & Kerstin Spirohn & Irma Lemmens & Mélanie Dos Santos & Caroline Demeret & Louis Jones & Sud, 2019. "Maximizing binary interactome mapping with a minimal number of assays," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Peter Uetz & Loic Giot & Gerard Cagney & Traci A. Mansfield & Richard S. Judson & James R. Knight & Daniel Lockshon & Vaibhav Narayan & Maithreyan Srinivasan & Pascale Pochart & Alia Qureshi-Emili & Y, 2000. "A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae," Nature, Nature, vol. 403(6770), pages 623-627, February.
    3. Stephen Oliver, 2000. "Guilt-by-association goes global," Nature, Nature, vol. 403(6770), pages 601-602, February.
    4. Jean-Christophe Rain & Luc Selig & Hilde De Reuse & Véronique Battaglia & Céline Reverdy & Stéphane Simon & Gerlinde Lenzen & Fabien Petel & Jérôme Wojcik & Vincent Schächter & Y. Chemama & Agnès Labi, 2001. "Erratum: The protein–protein interaction map of Helicobacter pylori," Nature, Nature, vol. 409(6821), pages 743-743, February.
    5. Jean-Christophe Rain & Luc Selig & Hilde De Reuse & Véronique Battaglia & Céline Reverdy & Stéphane Simon & Gerlinde Lenzen & Fabien Petel & Jérôme Wojcik & Vincent Schächter & Y. Chemama & Agnès Labi, 2001. "The protein–protein interaction map of Helicobacter pylori," Nature, Nature, vol. 409(6817), pages 211-215, January.
    6. H. Jeong & S. P. Mason & A.-L. Barabási & Z. N. Oltvai, 2001. "Lethality and centrality in protein networks," Nature, Nature, vol. 411(6833), pages 41-42, May.
    7. Núria Crua Asensio & Elisabet Muñoz Giner & Natalia Sánchez de Groot & Marc Torrent Burgas, 2017. "Centrality in the host–pathogen interactome is associated with pathogen fitness during infection," Nature Communications, Nature, vol. 8(1), pages 1-6, April.
    8. Wenxiu Ma & Zhiqian Pang & Xiaoen Huang & Jin Xu & Sheo Shankar Pandey & Jinyun Li & Diann S. Achor & Fernanda N. C. Vasconcelos & Connor Hendrich & Yixiao Huang & Wenting Wang & Donghwan Lee & Daniel, 2022. "Citrus Huanglongbing is a pathogen-triggered immune disease that can be mitigated with antioxidants and gibberellin," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
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