Natural variation of immune epitopes reveals intrabacterial antagonism

Proc Natl Acad Sci U S A. 2024 Jun 4;121(23):e2319499121. doi: 10.1073/pnas.2319499121. Epub 2024 May 30.

Abstract

Plants and animals detect biomolecules termed microbe-associated molecular patterns (MAMPs) and induce immunity. Agricultural production is severely impacted by pathogens which can be controlled by transferring immune receptors. However, most studies use a single MAMP epitope and the impact of diverse multicopy MAMPs on immune induction is unknown. Here, we characterized the epitope landscape from five proteinaceous MAMPs across 4,228 plant-associated bacterial genomes. Despite the diversity sampled, natural variation was constrained and experimentally testable. Immune perception in both Arabidopsis and tomato depended on both epitope sequence and copy number variation. For example, Elongation Factor Tu is predominantly single copy, and 92% of its epitopes are immunogenic. Conversely, 99.9% of bacterial genomes contain multiple cold shock proteins, and 46% carry a nonimmunogenic form. We uncovered a mechanism for immune evasion, intrabacterial antagonism, where a nonimmunogenic cold shock protein blocks perception of immunogenic forms encoded in the same genome. These data will lay the foundation for immune receptor deployment and engineering based on natural variation.

Keywords: microbe-associated molecular patterns; natural variation; pattern recognition receptor; plant innate immunity.

MeSH terms

  • Arabidopsis* / genetics
  • Arabidopsis* / immunology
  • Bacteria / genetics
  • Bacteria / immunology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / immunology
  • Cold Shock Proteins and Peptides / genetics
  • Cold Shock Proteins and Peptides / immunology
  • Cold Shock Proteins and Peptides / metabolism
  • Epitopes* / immunology
  • Genome, Bacterial
  • Pathogen-Associated Molecular Pattern Molecules / immunology
  • Pathogen-Associated Molecular Pattern Molecules / metabolism
  • Peptide Elongation Factor Tu / genetics
  • Peptide Elongation Factor Tu / immunology
  • Plant Immunity / genetics
  • Plant Immunity / immunology
  • Solanum lycopersicum* / genetics
  • Solanum lycopersicum* / immunology
  • Solanum lycopersicum* / microbiology

Substances

  • Epitopes
  • Pathogen-Associated Molecular Pattern Molecules
  • Peptide Elongation Factor Tu
  • Bacterial Proteins
  • Cold Shock Proteins and Peptides