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Jurassic NLR: conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1

View ORCID ProfileHiroaki Adachi, View ORCID ProfileToshiyuki Sakai, View ORCID ProfileJiorgos Kourelis, View ORCID ProfileJose L. Gonzalez Hernandez, View ORCID ProfileAbbas Maqbool, View ORCID ProfileSophien Kamoun
doi: https://doi.org/10.1101/2020.10.12.333484
Hiroaki Adachi
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, NR4 7UH, Norwich, UK
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Toshiyuki Sakai
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, NR4 7UH, Norwich, UK
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Jiorgos Kourelis
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, NR4 7UH, Norwich, UK
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Jose L. Gonzalez Hernandez
2Agronomy, Horticulture and Plant Sciences Department, South Dakota State University, Brookings, South Dakota, US
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Abbas Maqbool
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, NR4 7UH, Norwich, UK
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Sophien Kamoun
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, NR4 7UH, Norwich, UK
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  • For correspondence: sophien.kamoun@tsl.ac.uk
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ABSTRACT

In plants, NLR immune receptors generally exhibit hallmarks of rapid evolution even at the intraspecific level. We reconstructed the evolutionary history of ZAR1, an atypically conserved NLR that traces its origin to early flowering plant lineages ~220 to 150 million years ago (Jurassic period). Ortholog sequence analyses revealed highly conserved features of ZAR1, including regions for pathogen effector recognition, intramolecular interactions and cell death activation. This uncovered a new conserved surface on the ZAR1 resistosome underside that is required for cell death induction. Throughout its evolution, ZAR1 acquired novel features, such as a C-terminal integration of a thioredoxin-like domain. ZAR1 duplicated into two paralog families, which underwent distinct evolutionary paths. We conclude that ZAR1 stands out among angiosperm NLRs for having experienced relatively limited gene duplication and expansion throughout its deep evolutionary history. Nonetheless, ZAR1 did also give rise to non-canonical NLR proteins with integrated domains and degenerated molecular features.

Competing Interest Statement

S.K. receives funding from industry on NLR biology.

Footnotes

  • This version includes additional analyses, notably experiments showing that the newly discovered conserved surface on the ZAR1 resistosome underside is required for cell death induction.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 23, 2021.
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Jurassic NLR: conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1
Hiroaki Adachi, Toshiyuki Sakai, Jiorgos Kourelis, Jose L. Gonzalez Hernandez, Abbas Maqbool, Sophien Kamoun
bioRxiv 2020.10.12.333484; doi: https://doi.org/10.1101/2020.10.12.333484
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Jurassic NLR: conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1
Hiroaki Adachi, Toshiyuki Sakai, Jiorgos Kourelis, Jose L. Gonzalez Hernandez, Abbas Maqbool, Sophien Kamoun
bioRxiv 2020.10.12.333484; doi: https://doi.org/10.1101/2020.10.12.333484

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