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Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain

View ORCID ProfileAleksandra Białas, View ORCID ProfileThorsten Langner, View ORCID ProfileAdeline Harant, View ORCID ProfileMauricio P Contreras, View ORCID ProfileClare EM Stevenson, View ORCID ProfileDavid M Lawson, View ORCID ProfileJan Sklenar, View ORCID ProfileRonny Kellner, View ORCID ProfileMatthew J Moscou, View ORCID ProfileRyohei Terauchi, View ORCID ProfileMark J Banfield, View ORCID ProfileSophien Kamoun
doi: https://doi.org/10.1101/2021.01.26.428286
Aleksandra Białas
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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  • ORCID record for Aleksandra Białas
Thorsten Langner
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Adeline Harant
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Mauricio P Contreras
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Clare EM Stevenson
2Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK
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  • ORCID record for Clare EM Stevenson
David M Lawson
2Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK
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Jan Sklenar
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Ronny Kellner
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Matthew J Moscou
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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Ryohei Terauchi
3Division of Genomics and Breeding, Iwate Biotechnology Research Centre, Iwate, Japan
4Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
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Mark J Banfield
2Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK
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Sophien Kamoun
1The Sainsbury Laboratory, University of East Anglia, Norwich Research Park, Norwich, NR4 7UH, UK
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  • For correspondence: sophien.kamoun@tsl.ac.uk
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ABSTRACT

A subset of plant NLR immune receptors carry unconventional integrated domains in addition to their canonical domain architecture. One example is rice Pik-1 that comprises an integrated heavy metal–associated (HMA) domain. Here, we reconstructed the evolutionary history of Pik-1 and its NLR partner, Pik-2, and tested hypotheses about adaptive evolution of the HMA domain. Phylogenetic analyses revealed that the HMA domain integrated into Pik-1 before Oryzinae speciation over 15 million years ago and has been under diversifying selection. Ancestral sequence reconstruction coupled with functional studies showed that two Pik-1 allelic variants independently evolved from a weakly binding ancestral state to high-affinity binding of the blast fungus effector AVR-PikD. We conclude that for most of its evolutionary history the Pik-1 HMA domain did not sense AVR-PikD, and that different Pik-1 receptors have recently evolved through distinct biochemical paths to produce similar phenotypic outcomes. These findings highlight the dynamic nature of the evolutionary mechanisms underpinning NLR adaptation to plant pathogens.

Competing Interest Statement

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

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 January 27, 2021.
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Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain
Aleksandra Białas, Thorsten Langner, Adeline Harant, Mauricio P Contreras, Clare EM Stevenson, David M Lawson, Jan Sklenar, Ronny Kellner, Matthew J Moscou, Ryohei Terauchi, Mark J Banfield, Sophien Kamoun
bioRxiv 2021.01.26.428286; doi: https://doi.org/10.1101/2021.01.26.428286
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Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain
Aleksandra Białas, Thorsten Langner, Adeline Harant, Mauricio P Contreras, Clare EM Stevenson, David M Lawson, Jan Sklenar, Ronny Kellner, Matthew J Moscou, Ryohei Terauchi, Mark J Banfield, Sophien Kamoun
bioRxiv 2021.01.26.428286; doi: https://doi.org/10.1101/2021.01.26.428286

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