A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors

Maxim Prokchorchik; Sera Choi; Eui Hwan Chung; Kyungho Won; Jeffery L. Dangl; Kee Hoon Sohn

doi:10.1111/nph.16218

A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors

Maxim Prokchorchik, Sera Choi, Eui Hwan Chung, Kyungho Won, Jeffery L. Dangl, Kee Hoon Sohn

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

39 Citations (Scopus)

Abstract

Some virulence effectors secreted from pathogens target host proteins and induce biochemical modifications that are monitored by nucleotide-binding and leucine-rich repeat (NLR) immune receptors. Arabidopsis RIN4 protein (AtRIN4: RPM1-interacting protein 4) homologs are present in diverse plant species and targeted by several bacterial type III effector proteins including the cysteine protease AvrRpt2. RIN4 is ‘guarded’ by several independently evolved NLRs from various plant species, including Arabidopsis RPS2. Recently, it was shown that the MR5 NLR from a wild apple relative can recognize the AvrRpt2 effector from Erwinia amylovora, but the details of this recognition remained unclear. The present contribution reports the mechanism of AvrRpt2 recognition by independently evolved NLRs, MR5 from apple and RPS2, both of which require proteolytically processed RIN4 for activation. It shows that the C-terminal cleaved product of apple RIN4 (MdRIN4) but not AtRIN4 is necessary and sufficient for MR5 activation. Additionally, two polymorphic residues in AtRIN4 and MdRIN4 are identified that are crucial in the regulation of and physical association with NLRs. It is proposed that polymorphisms in RIN4 from distantly related plant species allow it to remain an effector target while maintaining compatibility with multiple NLRs.

Original language	English
Pages (from-to)	1327-1342
Number of pages	16
Journal	New Phytologist
Volume	225
Issue number	3
DOIs	https://doi.org/10.1111/nph.16218
Publication status	Published - 2020 Feb 1
Externally published	Yes

Bibliographical note

Funding Information:
We thank Jay Jayaraman, Toby Newman, Sarah Grant and David Mackey for critical reading of our manuscript. We also thank Vincent Bus and Mary Horner for providing EaAvrRpt2 source material. This work was carried out with the support of National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A5A1023599, SRC) and Next‐Generation BioGreen 21 Program (SSAC) of Rural Development Administration (PJ013269). MP is the recipient of a PhD scholarship from Massey University – Plant & Food Research Joint Graduate School of Horticulture and Food Enterprise, New Zealand. SC was supported by the BK21 PLUS Research Fellowship from the Ministry of Education, Science and Technology, Republic of Korea. JLD was supported by grant IOS‐1758400 from the United States National Science Foundation and by the HHMI. JLD is an Investigator of the Howard Hughes Medical Institute. The authors declare no competing interests.

Funding Information:
We thank Jay Jayaraman, Toby Newman, Sarah Grant and David Mackey for critical reading of our manuscript. We also thank Vincent Bus and Mary Horner for providing EaAvrRpt2 source material. This work was carried out with the support of National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A5A1023599, SRC) and Next-Generation BioGreen 21 Program (SSAC) of Rural Development Administration (PJ013269). MP is the recipient of a PhD scholarship from Massey University – Plant & Food Research Joint Graduate School of Horticulture and Food Enterprise, New Zealand. SC was supported by the BK21 PLUS Research Fellowship from the Ministry of Education, Science and Technology, Republic of Korea. JLD was supported by grant IOS-1758400 from the United States National Science Foundation and by the HHMI. JLD is an Investigator of the Howard Hughes Medical Institute. The authors declare no competing interests.

Publisher Copyright:
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust

Keywords

NLR
Nicotiana benthamiana
RIN4
convergent evolution
effector recognition
plant immune receptors

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/nph.16218

Cite this

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title = "A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors",

abstract = "Some virulence effectors secreted from pathogens target host proteins and induce biochemical modifications that are monitored by nucleotide-binding and leucine-rich repeat (NLR) immune receptors. Arabidopsis RIN4 protein (AtRIN4: RPM1-interacting protein 4) homologs are present in diverse plant species and targeted by several bacterial type III effector proteins including the cysteine protease AvrRpt2. RIN4 is {\textquoteleft}guarded{\textquoteright} by several independently evolved NLRs from various plant species, including Arabidopsis RPS2. Recently, it was shown that the MR5 NLR from a wild apple relative can recognize the AvrRpt2 effector from Erwinia amylovora, but the details of this recognition remained unclear. The present contribution reports the mechanism of AvrRpt2 recognition by independently evolved NLRs, MR5 from apple and RPS2, both of which require proteolytically processed RIN4 for activation. It shows that the C-terminal cleaved product of apple RIN4 (MdRIN4) but not AtRIN4 is necessary and sufficient for MR5 activation. Additionally, two polymorphic residues in AtRIN4 and MdRIN4 are identified that are crucial in the regulation of and physical association with NLRs. It is proposed that polymorphisms in RIN4 from distantly related plant species allow it to remain an effector target while maintaining compatibility with multiple NLRs.",

keywords = "NLR, Nicotiana benthamiana, RIN4, convergent evolution, effector recognition, plant immune receptors",

author = "Maxim Prokchorchik and Sera Choi and Chung, {Eui Hwan} and Kyungho Won and Dangl, {Jeffery L.} and Sohn, {Kee Hoon}",

note = "Funding Information: We thank Jay Jayaraman, Toby Newman, Sarah Grant and David Mackey for critical reading of our manuscript. We also thank Vincent Bus and Mary Horner for providing EaAvrRpt2 source material. This work was carried out with the support of National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A5A1023599, SRC) and Next‐Generation BioGreen 21 Program (SSAC) of Rural Development Administration (PJ013269). MP is the recipient of a PhD scholarship from Massey University – Plant & Food Research Joint Graduate School of Horticulture and Food Enterprise, New Zealand. SC was supported by the BK21 PLUS Research Fellowship from the Ministry of Education, Science and Technology, Republic of Korea. JLD was supported by grant IOS‐1758400 from the United States National Science Foundation and by the HHMI. JLD is an Investigator of the Howard Hughes Medical Institute. The authors declare no competing interests. Funding Information: We thank Jay Jayaraman, Toby Newman, Sarah Grant and David Mackey for critical reading of our manuscript. We also thank Vincent Bus and Mary Horner for providing EaAvrRpt2 source material. This work was carried out with the support of National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2018R1A5A1023599, SRC) and Next-Generation BioGreen 21 Program (SSAC) of Rural Development Administration (PJ013269). MP is the recipient of a PhD scholarship from Massey University – Plant & Food Research Joint Graduate School of Horticulture and Food Enterprise, New Zealand. SC was supported by the BK21 PLUS Research Fellowship from the Ministry of Education, Science and Technology, Republic of Korea. JLD was supported by grant IOS-1758400 from the United States National Science Foundation and by the HHMI. JLD is an Investigator of the Howard Hughes Medical Institute. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2019 The Authors. New Phytologist {\textcopyright} 2019 New Phytologist Trust",

year = "2020",

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day = "1",

doi = "10.1111/nph.16218",

language = "English",

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T1 - A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors

AU - Prokchorchik, Maxim

AU - Choi, Sera

AU - Chung, Eui Hwan

AU - Won, Kyungho

AU - Dangl, Jeffery L.

AU - Sohn, Kee Hoon

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PY - 2020/2/1

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N2 - Some virulence effectors secreted from pathogens target host proteins and induce biochemical modifications that are monitored by nucleotide-binding and leucine-rich repeat (NLR) immune receptors. Arabidopsis RIN4 protein (AtRIN4: RPM1-interacting protein 4) homologs are present in diverse plant species and targeted by several bacterial type III effector proteins including the cysteine protease AvrRpt2. RIN4 is ‘guarded’ by several independently evolved NLRs from various plant species, including Arabidopsis RPS2. Recently, it was shown that the MR5 NLR from a wild apple relative can recognize the AvrRpt2 effector from Erwinia amylovora, but the details of this recognition remained unclear. The present contribution reports the mechanism of AvrRpt2 recognition by independently evolved NLRs, MR5 from apple and RPS2, both of which require proteolytically processed RIN4 for activation. It shows that the C-terminal cleaved product of apple RIN4 (MdRIN4) but not AtRIN4 is necessary and sufficient for MR5 activation. Additionally, two polymorphic residues in AtRIN4 and MdRIN4 are identified that are crucial in the regulation of and physical association with NLRs. It is proposed that polymorphisms in RIN4 from distantly related plant species allow it to remain an effector target while maintaining compatibility with multiple NLRs.

AB - Some virulence effectors secreted from pathogens target host proteins and induce biochemical modifications that are monitored by nucleotide-binding and leucine-rich repeat (NLR) immune receptors. Arabidopsis RIN4 protein (AtRIN4: RPM1-interacting protein 4) homologs are present in diverse plant species and targeted by several bacterial type III effector proteins including the cysteine protease AvrRpt2. RIN4 is ‘guarded’ by several independently evolved NLRs from various plant species, including Arabidopsis RPS2. Recently, it was shown that the MR5 NLR from a wild apple relative can recognize the AvrRpt2 effector from Erwinia amylovora, but the details of this recognition remained unclear. The present contribution reports the mechanism of AvrRpt2 recognition by independently evolved NLRs, MR5 from apple and RPS2, both of which require proteolytically processed RIN4 for activation. It shows that the C-terminal cleaved product of apple RIN4 (MdRIN4) but not AtRIN4 is necessary and sufficient for MR5 activation. Additionally, two polymorphic residues in AtRIN4 and MdRIN4 are identified that are crucial in the regulation of and physical association with NLRs. It is proposed that polymorphisms in RIN4 from distantly related plant species allow it to remain an effector target while maintaining compatibility with multiple NLRs.

KW - NLR

KW - Nicotiana benthamiana

KW - RIN4

KW - convergent evolution

KW - effector recognition

KW - plant immune receptors

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ER -

A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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