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Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional regulatory modes

Yu Yang, Nak Hyun Kim, Volkan Cevik, Pierre Jacob, Li Wan, Oliver J. Furzer, Jeffery L. Dangl
doi: https://doi.org/10.1101/2022.05.10.491418
Yu Yang
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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Nak Hyun Kim
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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Volkan Cevik
3The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, United Kingdom
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Pierre Jacob
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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Li Wan
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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Oliver J. Furzer
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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Jeffery L. Dangl
1Department of Biology; University of North Carolina at Chapel Hill; Chapel Hill, NC, United States of America
2Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
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  • For correspondence: dangl@email.unc.edu
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Abstract

Some plant NLR immune receptors are encoded in head-to-head pairs that function together. Alleles of the NLR pair CHS3/CSA1 form three clades. The clade 1 sensor CHS3 contains an integrated domain (ID) with homology to regulatory domains, which is lacking in clades 2 and 3. We defined two regulatory modes for CHS3/CSA1 pairs. One is likely mediated by effector binding to the clade 1 ID of CHS3 and the other relies on CHS3/CSA1 pairs from all clades detecting effector modification of an associated pattern recognition receptor. We suggest that an ancestral Arabidopsis CHS3/CSA1 pair gained a second recognition specificity and regulatory mechanism through ID acquisition, while retaining its original specificity as a ‘Guard’ against perturbation of pattern recognition receptor targeting by a pathogen effector. This likely comes with a cost, since both ID and non-ID alleles of the pair persist in diverse Arabidopsis populations through balancing selection.

Summary We dissect a novel case where two regulatory modes emerged across three clades of the co-evolved CHS3/CSA1 plant immune receptor pairs, which features recruitment of an integrated domain (ID) into the clade 1 CHS3 alleles. Pre- and post-ID integration alleles maintain functionality; balancing selection maintains both in the Arabidopsis pan-genome.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵a National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China.

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-NC-ND 4.0 International license.
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Posted May 11, 2022.
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Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional regulatory modes
Yu Yang, Nak Hyun Kim, Volkan Cevik, Pierre Jacob, Li Wan, Oliver J. Furzer, Jeffery L. Dangl
bioRxiv 2022.05.10.491418; doi: https://doi.org/10.1101/2022.05.10.491418
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Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional regulatory modes
Yu Yang, Nak Hyun Kim, Volkan Cevik, Pierre Jacob, Li Wan, Oliver J. Furzer, Jeffery L. Dangl
bioRxiv 2022.05.10.491418; doi: https://doi.org/10.1101/2022.05.10.491418

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