The integrated LIM-peptidase domain of the CSA1-CHS3/DAR4 paired immune receptor detects changes in DA1 peptidase inhibitors in Arabidopsis

Benguo Gu; Toby Parkes; Fernando Rabanal; Caroline Smith; Fu Hao Lu; Neil McKenzie; Hui Dong; Detlef Weigel; Jonathan D.G. Jones; Volkan Cevik; Michael W. Bevan

doi:10.1016/j.chom.2023.04.009

The integrated LIM-peptidase domain of the CSA1-CHS3/DAR4 paired immune receptor detects changes in DA1 peptidase inhibitors in Arabidopsis

Benguo Gu, Toby Parkes, Fernando Rabanal, Caroline Smith, Fu Hao Lu, Neil McKenzie, Hui Dong, Detlef Weigel, Jonathan D.G. Jones, Volkan Cevik, Michael W. Bevan

Research output: Contribution to journal › Article › peer-review

4 Citations (SciVal)

Abstract

White blister rust, caused by the oomycete Albugo candida, is a widespread disease of Brassica crops. The Brassica relative Arabidopsis thaliana uses the paired immune receptor complex CSA1-CHS3/DAR4 to resist Albugo infection. The CHS3/DAR4 sensor NLR, which functions together with its partner, the helper NLR CSA1, carries an integrated domain (ID) with homology to DA1 peptidases. Using domain swaps with several DA1 homologs, we show that the LIM-peptidase domain of the family member CHS3/DAR4 functions as an integrated decoy for the family member DAR3, which interacts with and inhibits the peptidase activities of the three closely related peptidases DA1, DAR1, and DAR2. Albugo infection rapidly lowers DAR3 levels and activates DA1 peptidase activity, thereby promoting endoreduplication of host tissues to support pathogen growth. We propose that the paired immune receptor CSA1-CHS3/DAR4 detects the actions of a putative Albugo effector that reduces DAR3 levels, resulting in defense activation.

Original language	English
Pages (from-to)	949-961.e5
Journal	Cell Host and Microbe
Volume	31
Issue number	6
Early online date	10 May 2023
DOIs	https://doi.org/10.1016/j.chom.2023.04.009
Publication status	Published - 14 Jun 2023

Bibliographical note

Funding Information:
We thank Dr. Yan Ma for advice on N. tabacum infiltration, and Drs. Catherine Gardener, Dae Sung Kim, Xiaokun Liu, and Pingtao Ding for advice on pathogen growth tests. This work was funded by the Biological and Biotechnological Sciences Research Council (BBSRC) Newton Fund to B.G. and M.W.B., BBSRC grant BB/K017225 to M.W.B., and Institute Strategic Grant GEN ( BB/P013511/1 ) to M.W.B. Work in the J.D.G.J. lab was supported by a Gatsby Charitable Foundation grant to TSL Norwich, by BBSRC BB/M003809/1 (supported V.C.) and ERC grant 233376 “Albugon” (supported VK). Work in the V.C. lab was supported by the University of Bath University Research Studentship Account (URSA), University of Bath start-up fund , and Royal Society International Collaboration Awards ( ICA∖R1∖201511 ). We thank the 1001 Genomes Plus (1001G+) project, funded by ERA-CAPS through BBSRC , DFG , and FWF to Paul Kersey, Detlef Weigel, and Magnus Nordborg, for access to newly assembled Arabidopsis genomes.

Data and code availability
Sequences of CSA1, CHS3/DAR4, DA1 and DAR3 are publicly available from Genbank. Accession numbers are listed in the key resources table. All data generated in this study are in Tables S1–S16.
No original code was used in this study.
Any additional information required to re-analyze the data reported in this paper is available from the lead contact upon request.

Keywords

Albugo
Arabidopsis
Brassicaceae
DA1 peptidase
endoreduplication
growth control
integrated domain
NLR
resistance genes

ASJC Scopus subject areas

Parasitology
Microbiology
Virology

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10.1016/j.chom.2023.04.009Licence: CC BY

Cite this

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title = "The integrated LIM-peptidase domain of the CSA1-CHS3/DAR4 paired immune receptor detects changes in DA1 peptidase inhibitors in Arabidopsis",

abstract = "White blister rust, caused by the oomycete Albugo candida, is a widespread disease of Brassica crops. The Brassica relative Arabidopsis thaliana uses the paired immune receptor complex CSA1-CHS3/DAR4 to resist Albugo infection. The CHS3/DAR4 sensor NLR, which functions together with its partner, the helper NLR CSA1, carries an integrated domain (ID) with homology to DA1 peptidases. Using domain swaps with several DA1 homologs, we show that the LIM-peptidase domain of the family member CHS3/DAR4 functions as an integrated decoy for the family member DAR3, which interacts with and inhibits the peptidase activities of the three closely related peptidases DA1, DAR1, and DAR2. Albugo infection rapidly lowers DAR3 levels and activates DA1 peptidase activity, thereby promoting endoreduplication of host tissues to support pathogen growth. We propose that the paired immune receptor CSA1-CHS3/DAR4 detects the actions of a putative Albugo effector that reduces DAR3 levels, resulting in defense activation.",

keywords = "Albugo, Arabidopsis, Brassicaceae, DA1 peptidase, endoreduplication, growth control, integrated domain, NLR, resistance genes",

author = "Benguo Gu and Toby Parkes and Fernando Rabanal and Caroline Smith and Lu, {Fu Hao} and Neil McKenzie and Hui Dong and Detlef Weigel and Jones, {Jonathan D.G.} and Volkan Cevik and Bevan, {Michael W.}",

note = "Funding Information: We thank Dr. Yan Ma for advice on N. tabacum infiltration, and Drs. Catherine Gardener, Dae Sung Kim, Xiaokun Liu, and Pingtao Ding for advice on pathogen growth tests. This work was funded by the Biological and Biotechnological Sciences Research Council (BBSRC) Newton Fund to B.G. and M.W.B., BBSRC grant BB/K017225 to M.W.B., and Institute Strategic Grant GEN ( BB/P013511/1 ) to M.W.B. Work in the J.D.G.J. lab was supported by a Gatsby Charitable Foundation grant to TSL Norwich, by BBSRC BB/M003809/1 (supported V.C.) and ERC grant 233376 “Albugon” (supported VK). Work in the V.C. lab was supported by the University of Bath University Research Studentship Account (URSA), University of Bath start-up fund , and Royal Society International Collaboration Awards ( ICA∖R1∖201511 ). We thank the 1001 Genomes Plus (1001G+) project, funded by ERA-CAPS through BBSRC , DFG , and FWF to Paul Kersey, Detlef Weigel, and Magnus Nordborg, for access to newly assembled Arabidopsis genomes. Data and code availability Sequences of CSA1, CHS3/DAR4, DA1 and DAR3 are publicly available from Genbank. Accession numbers are listed in the key resources table. All data generated in this study are in Tables S1–S16. No original code was used in this study. Any additional information required to re-analyze the data reported in this paper is available from the lead contact upon request.",

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doi = "10.1016/j.chom.2023.04.009",

language = "English",

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pages = "949--961.e5",

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T1 - The integrated LIM-peptidase domain of the CSA1-CHS3/DAR4 paired immune receptor detects changes in DA1 peptidase inhibitors in Arabidopsis

AU - Gu, Benguo

AU - Parkes, Toby

AU - Rabanal, Fernando

AU - Smith, Caroline

AU - Lu, Fu Hao

AU - McKenzie, Neil

AU - Dong, Hui

AU - Weigel, Detlef

AU - Jones, Jonathan D.G.

AU - Cevik, Volkan

AU - Bevan, Michael W.

N1 - Funding Information: We thank Dr. Yan Ma for advice on N. tabacum infiltration, and Drs. Catherine Gardener, Dae Sung Kim, Xiaokun Liu, and Pingtao Ding for advice on pathogen growth tests. This work was funded by the Biological and Biotechnological Sciences Research Council (BBSRC) Newton Fund to B.G. and M.W.B., BBSRC grant BB/K017225 to M.W.B., and Institute Strategic Grant GEN ( BB/P013511/1 ) to M.W.B. Work in the J.D.G.J. lab was supported by a Gatsby Charitable Foundation grant to TSL Norwich, by BBSRC BB/M003809/1 (supported V.C.) and ERC grant 233376 “Albugon” (supported VK). Work in the V.C. lab was supported by the University of Bath University Research Studentship Account (URSA), University of Bath start-up fund , and Royal Society International Collaboration Awards ( ICA∖R1∖201511 ). We thank the 1001 Genomes Plus (1001G+) project, funded by ERA-CAPS through BBSRC , DFG , and FWF to Paul Kersey, Detlef Weigel, and Magnus Nordborg, for access to newly assembled Arabidopsis genomes. Data and code availability Sequences of CSA1, CHS3/DAR4, DA1 and DAR3 are publicly available from Genbank. Accession numbers are listed in the key resources table. All data generated in this study are in Tables S1–S16. No original code was used in this study. Any additional information required to re-analyze the data reported in this paper is available from the lead contact upon request.

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Y1 - 2023/6/14

N2 - White blister rust, caused by the oomycete Albugo candida, is a widespread disease of Brassica crops. The Brassica relative Arabidopsis thaliana uses the paired immune receptor complex CSA1-CHS3/DAR4 to resist Albugo infection. The CHS3/DAR4 sensor NLR, which functions together with its partner, the helper NLR CSA1, carries an integrated domain (ID) with homology to DA1 peptidases. Using domain swaps with several DA1 homologs, we show that the LIM-peptidase domain of the family member CHS3/DAR4 functions as an integrated decoy for the family member DAR3, which interacts with and inhibits the peptidase activities of the three closely related peptidases DA1, DAR1, and DAR2. Albugo infection rapidly lowers DAR3 levels and activates DA1 peptidase activity, thereby promoting endoreduplication of host tissues to support pathogen growth. We propose that the paired immune receptor CSA1-CHS3/DAR4 detects the actions of a putative Albugo effector that reduces DAR3 levels, resulting in defense activation.

AB - White blister rust, caused by the oomycete Albugo candida, is a widespread disease of Brassica crops. The Brassica relative Arabidopsis thaliana uses the paired immune receptor complex CSA1-CHS3/DAR4 to resist Albugo infection. The CHS3/DAR4 sensor NLR, which functions together with its partner, the helper NLR CSA1, carries an integrated domain (ID) with homology to DA1 peptidases. Using domain swaps with several DA1 homologs, we show that the LIM-peptidase domain of the family member CHS3/DAR4 functions as an integrated decoy for the family member DAR3, which interacts with and inhibits the peptidase activities of the three closely related peptidases DA1, DAR1, and DAR2. Albugo infection rapidly lowers DAR3 levels and activates DA1 peptidase activity, thereby promoting endoreduplication of host tissues to support pathogen growth. We propose that the paired immune receptor CSA1-CHS3/DAR4 detects the actions of a putative Albugo effector that reduces DAR3 levels, resulting in defense activation.

KW - Albugo

KW - Arabidopsis

KW - Brassicaceae

KW - DA1 peptidase

KW - endoreduplication

KW - growth control

KW - integrated domain

KW - NLR

KW - resistance genes

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AN - SCOPUS:85161633561

SN - 1931-3128

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JO - Cell Host and Microbe

JF - Cell Host and Microbe

IS - 6

ER -

The integrated LIM-peptidase domain of the CSA1-CHS3/DAR4 paired immune receptor detects changes in DA1 peptidase inhibitors in Arabidopsis

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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