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A novel BLUF photoreceptor modulates the Xanthomonas citri subsp. citri–host plant interaction

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Abstract

Plant–pathogen interaction is influenced by multiple environmental factors, including temperature and light. Recent works have shown that light modulates not only the defense response of plants but also the pathogens virulence. Xanthomonas citri subsp. citri (Xcc) is the bacterium responsible for citrus canker, an important plant disease worldwide. The Xcc genome presents four genes encoding putative photoreceptors: one bacteriophytochrome and three blue light photoreceptors, one LOV and two BLUFs (bluf1: XAC2120 and bluf2: XAC3278). The presence of two BLUFs proteins is an outstanding feature of Xcc. In this work we show that the bluf2 gene is functional. The mutant strain, XccΔbluf2, was constructed demonstrating that BLUF2 regulates swimming-type motility, adhesion to leaves, exopolysaccharide production and biofilm formation, features involved in the Xcc virulence processes. An important aspect during the plant–pathogen interaction is the oxidative response of the host and the consequent reaction of the pathogen. We observed that ROS detoxification is regulated by Xcc bluf2 gene. The phenotypes of disease in orange plants produced by WT and XccΔbluf2 strains were evaluated, observing different phenotypes. Altogether, these results show that BLUF2 negatively regulates virulence during citrus canker. This work constitutes the first report on BLUF-like receptors in plant pathogenic bacteria.

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The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files. Source data are provided with this paper.

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Acknowledgements

We would like to thank the staff from the English Department of the Facultad de Ciencias Bioquímicas y Farmacéuticas (UNR) for the language correction of the manuscript. We also thank Rodrigo Vena for assistance with the microscopy facility. This work was supported by grants from the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) (PICT2017-2242 to EGO) and Universidad Nacional de Rosario (UNR), (Grant N° 1BIO432) to EGO. AC and JT are fellows of Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina), MBR is fellow of ANPCyT; SP and EGO are staff member of Consejo de Investigaciones UNR (CIUNR).

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Author notes

  1. Analía Carrau and Josefina Tano have contributed equally to this work.

Authors and Affiliations

  1. Instituto de Biología Molecular y Celular de Rosario, Consejo Nacional de Investigaciones Científicas y Técnicas, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Suipacha 531, S2002LRK, Rosario, Argentina

    Analía Carrau, Josefina Tano, María Belén Ripa & Elena Graciela Orellano

  2. Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Biodiversidad y Biología Experimental, Buenos Aires, Argentina

    Laura Moyano

  3. Instituto de Biodiversidad y Biología Experimental y Aplicada, Consejo Nacional de Investigaciones Científicas y Técnicas-Universidad de Buenos Aires (IBBEA, CONICET-UBA), Buenos Aires, Argentina

    Laura Moyano

  4. Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Suipacha 531, S2002LRK, Rosario, Argentina

    Silvana Petrocelli

  5. Área Estadística y Procesamiento de Datos, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina

    Laura Piskulic

  6. Programa de Pós-Graduação em Biotecnologia, Núcleo de Pesquisas em Ciências Biológicas, Universidade Federal de Ouro Preto, Ouro Preto, MG, Brazil

    Leandro Marcio Moreira

  7. Departamento de Ciências Biológicas, Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Ouro Preto, MG, Brazil

    Leandro Marcio Moreira

  8. Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil

    José Salvatore Leister Patané

  9. Laboratório de Ciclo Celular, Instituto Butantan, São Paulo, SP, Brazil

    João Carlos Setubal

Authors
  1. Analía Carrau
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  2. Josefina Tano
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  10. Elena Graciela Orellano
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Corresponding author

Correspondence to Elena Graciela Orellano.

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Additional information

This publication is dedicated to Prof. Silvia E. Braslavsky, a pioneer in photobiology and photobiophysics, on the occasion of her 80th birthday.

Supplementary Information

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Supplementary file1 (DOCX 14 KB)

Supplementary file2 (DOCX 17 KB)

43630_2023_420_MOESM3_ESM.tif

Supplementary file3Figure S1. Construction of X. citri pv. citri XccΔbluf2 strain. Steps for the generation of XccΔbluf2 mutant strain using the suicide plasmid pKMobGII to replace the Xcc bluf2 gene with a Sm/Sp-resistance cassette (TIF 1926 KB)

43630_2023_420_MOESM4_ESM.png

Supplementary file4Figure S2. Bacterial growth curves in liquid SB medium. Saturated cultures of Xcc WT, XccΔbluf2 and cXccΔbluf2 strains were subcultured into fresh SB medium at 2% (v/v) inocula. Bacterial growth curves at 28 ºC were obtained taking aliquots of cells suspension at different times growing under different light conditions. We measured the OD600 in (A) White light, (B) Blue light and in (C) Darkness, and the CFU/mL in (D) White light, (E) Blue light and in (F) Darkness, as a function of time. Data are represented as the mean ± standard error of two independent biological samples (PNG 94 KB)

43630_2023_420_MOESM5_ESM.png

Supplementary file5Figure S3. Expression levels of Xcc bluf2 gene in the plant-mimicking XVM2 medium growth under different light conditions. (A) Amplified products of the bluf2 gene by semiquantitative RT-PCR using RNA preparations from Xcc WT (1), XccΔbluf2 (2) and cXccΔbluf2 (3) cultures grown in XVM2 under white light, blue light and dark conditions for 6 hours. As a control for constitutive bacterial expression a fragment of rpoB gene was simultaneously amplified. (B) Expression profiles obtained by densitometric quantification of bluf2 band intensities normalized with rpoB band intensities. Integrated optical density (IOD), arbitrary units (A.U) (PNG 413 KB)

43630_2023_420_MOESM6_ESM.png

Supplementary file6Figure S4. Flagella analysis. Flagella of Xcc WT and XccΔbluf2 were observed by TEM. Bacteria were obtained from the border of swarming plates incubated under white light, blue light or darkness. Arrows indicate bacterial flagella. The results are representative of three independent experiments (PNG 737 KB)

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Carrau, A., Tano, J., Moyano, L. et al. A novel BLUF photoreceptor modulates the Xanthomonas citri subsp. citri–host plant interaction. Photochem Photobiol Sci 22, 1901–1918 (2023). https://doi.org/10.1007/s43630-023-00420-6

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