Natural variation of immune epitopes reveals intrabacterial antagonism

Author:

Stevens Danielle M.12,Moreno-Pérez Alba2ORCID,Weisberg Alexandra J.3ORCID,Ramsing Charis2,Fliegmann Judith4ORCID,Zhang Ning56ORCID,Madrigal Melanie2,Martin Gregory56ORCID,Steinbrenner Adam7ORCID,Felix Georg4ORCID,Coaker Gitta2ORCID

Affiliation:

1. Integrative Genetics and Genomics Graduate Group, University of California, Davis, CA 95616

2. Department of Plant Pathology, University of California, Davis, CA 95616

3. Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331

4. Center for Plant Molecular Biology, University of Tübingen, Tübingen 72074, Germany

5. Boyce Thompson Institute for Plant Research, Ithaca, NY 14853

6. Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY 14853

7. Department of Biology, University of Washington, Seattle, WA 98195

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.

Funder

HHS | National Institutes of Health

United States - Israel Binational Agricultural Research and Development Fund

USDA | National Institute of Food and Agriculture

Publisher

Proceedings of the National Academy of Sciences

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