Transcriptional profiling reveals conserved and species-specific plant defense responses during the interaction of Physcomitrium patens with Botrytis cinerea

Abstract

Key message

Evolutionary conserved defense mechanisms present in extant bryophytes and angiosperms, as well as moss-specific defenses are part of the immune response of Physcomitrium patens.

Abstract

Bryophytes and tracheophytes are descendants of early land plants that evolved adaptation mechanisms to cope with different kinds of terrestrial stresses, including drought, variations in temperature and UV radiation, as well as defense mechanisms against microorganisms present in the air and soil. Although great advances have been made on pathogen perception and subsequent defense activation in angiosperms, limited information is available in bryophytes. In this study, a transcriptomic approach uncovered the molecular mechanisms underlying the defense response of the bryophyte Physcomitrium patens (previously Physcomitrella patens) against the important plant pathogen Botrytis cinerea. A total of 3.072 differentially expressed genes were significantly affected during B. cinerea infection, including genes encoding proteins with known functions in angiosperm immunity and involved in pathogen perception, signaling, transcription, hormonal signaling, metabolic pathways such as shikimate and phenylpropanoid, and proteins with diverse role in defense against biotic stress. Similarly as in other plants, B. cinerea infection leads to downregulation of genes involved in photosynthesis and cell cycle progression. These results highlight the existence of evolutionary conserved defense responses to pathogens throughout the green plant lineage, suggesting that they were probably present in the common ancestors of land plants. Moreover, several genes acquired by horizontal transfer from prokaryotes and fungi, and a high number of P. patens-specific orphan genes were differentially expressed during B. cinerea infection, suggesting that they are important players in the moss immune response.

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Data availability

The sequencing raw data from the RNA-Seq libraries were deposited on the Sequence Read Archive from NCBI under SRA accession: PRJNA647932. Data are available through https://www.ncbi.nlm.nih.gov/bioproject/647932. In addition, data sets supporting the results of this article are included in Additional files.

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Acknowledgements

This work was supported by “Fondo Conjunto” Uruguay-México (AUCI-AMEXCID), “Agencia Nacional de Investigación e Innovación (ANII) (graduate fellowships)” Uruguay, “Programa de Desarrollo de las Ciencias Básicas (PEDECIBA)” Uruguay, and “Programa para Grupo de I+D Comisión Sectorial de Investigación Científica, Universidad de la República”, Uruguay. The authors thank Héctor Romero and Andrea Zimmers for bioinformatics advice.

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GR performed the experiments; GR, AA and IPDL analyzed and interpreted the data and participated in discussions; GR and AA helped to write the article; LV participated in the interpretation of the data, artwork, discussions and drafting of the work; RM participated in the drafting of this work; all the authors revised and contributed to the final version of the manuscript; IPDL wrote the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Inés Ponce De León.

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Reboledo, G., Agorio, A.d., Vignale, L. et al. Transcriptional profiling reveals conserved and species-specific plant defense responses during the interaction of Physcomitrium patens with Botrytis cinerea. Plant Mol Biol (2021). https://doi.org/10.1007/s11103-021-01116-0

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Keywords

  • Physcomitrium patens
  • Botrytis cinerea
  • Transcriptome
  • Defense genes
  • Orphan genes