A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity

Noriyuki Hatsugai; Daisuke Igarashi; Keisuke Mase; You Lu; Yayoi Tsuda; Suma Chakravarthy; Hai Lei Wei; Joseph W. Foley; Alan Collmer; Jane Glazebrook; Fumiaki Katagiri

doi:10.15252/embj.201796529

A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity

Noriyuki Hatsugai, Daisuke Igarashi, Keisuke Mase, You Lu, Yayoi Tsuda, Suma Chakravarthy, Hai Lei Wei, Joseph W. Foley, Alan Collmer, Jane Glazebrook, Fumiaki Katagiri

Plant and Microbial Biology

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

45 Scopus citations

Abstract

Since signaling machineries for two modes of plant-induced immunity, pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta. These observations led us to discovery of a network-buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI-Mediating and PTI-Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.

Original language	English (US)
Pages (from-to)	2758-2769
Number of pages	12
Journal	EMBO Journal
Volume	36
Issue number	18
DOIs	https://doi.org/10.15252/embj.201796529
State	Published - Sep 15 2017

Bibliographical note

Funding Information:
We are grateful to Narayana Upadhyaya and Peter Dodds of CSIRO for providing the AvrRpm1sp-Cya (pNR527) plasmid. We thank Amanda Thao for technical assistance in RNA-Seq library construction, the University of Minnesota Genomics Center (www.genomics.umn.edu) for sequencing of the RNA-Seq libraries, and the Minnesota Supercomputing Institute (www.msi.umn.edu) for a high performance computing environment. This work was supported by grants from National Science Foundation, IOS-1121425 and MCB-1518058 to F.K., IOS-1025642 to A.C. and IOS-1353854 to J.G., and a grant from Ajinomoto Co. to F.K.

Publisher Copyright:
© 2017 The Authors

Keywords

deep perturbation
fitness cost of immunity
network resilience
plant immune signaling network

Publisher link

10.15252/embj.201796529

Find It

Find It at U of M Libraries

Cite this

@article{e2397f357379494cb9f7a7154fe54ace,

title = "A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity",

abstract = "Since signaling machineries for two modes of plant-induced immunity, pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta. These observations led us to discovery of a network-buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI-Mediating and PTI-Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.",

keywords = "deep perturbation, fitness cost of immunity, network resilience, plant immune signaling network",

author = "Noriyuki Hatsugai and Daisuke Igarashi and Keisuke Mase and You Lu and Yayoi Tsuda and Suma Chakravarthy and Wei, {Hai Lei} and Foley, {Joseph W.} and Alan Collmer and Jane Glazebrook and Fumiaki Katagiri",

note = "Funding Information: We are grateful to Narayana Upadhyaya and Peter Dodds of CSIRO for providing the AvrRpm1sp-Cya (pNR527) plasmid. We thank Amanda Thao for technical assistance in RNA-Seq library construction, the University of Minnesota Genomics Center (www.genomics.umn.edu) for sequencing of the RNA-Seq libraries, and the Minnesota Supercomputing Institute (www.msi.umn.edu) for a high performance computing environment. This work was supported by grants from National Science Foundation, IOS-1121425 and MCB-1518058 to F.K., IOS-1025642 to A.C. and IOS-1353854 to J.G., and a grant from Ajinomoto Co. to F.K. Publisher Copyright: {\textcopyright} 2017 The Authors",

year = "2017",

month = sep,

day = "15",

doi = "10.15252/embj.201796529",

language = "English (US)",

volume = "36",

pages = "2758--2769",

journal = "EMBO Journal",

issn = "0261-4189",

publisher = "Nature Publishing Group",

number = "18",

}

TY - JOUR

T1 - A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity

AU - Hatsugai, Noriyuki

AU - Igarashi, Daisuke

AU - Mase, Keisuke

AU - Lu, You

AU - Tsuda, Yayoi

AU - Chakravarthy, Suma

AU - Wei, Hai Lei

AU - Foley, Joseph W.

AU - Collmer, Alan

AU - Glazebrook, Jane

AU - Katagiri, Fumiaki

N1 - Funding Information: We are grateful to Narayana Upadhyaya and Peter Dodds of CSIRO for providing the AvrRpm1sp-Cya (pNR527) plasmid. We thank Amanda Thao for technical assistance in RNA-Seq library construction, the University of Minnesota Genomics Center (www.genomics.umn.edu) for sequencing of the RNA-Seq libraries, and the Minnesota Supercomputing Institute (www.msi.umn.edu) for a high performance computing environment. This work was supported by grants from National Science Foundation, IOS-1121425 and MCB-1518058 to F.K., IOS-1025642 to A.C. and IOS-1353854 to J.G., and a grant from Ajinomoto Co. to F.K. Publisher Copyright: © 2017 The Authors

PY - 2017/9/15

Y1 - 2017/9/15

N2 - Since signaling machineries for two modes of plant-induced immunity, pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta. These observations led us to discovery of a network-buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI-Mediating and PTI-Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.

AB - Since signaling machineries for two modes of plant-induced immunity, pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), extensively overlap, PTI and ETI signaling likely interact. In an Arabidopsis quadruple mutant, in which four major sectors of the signaling network, jasmonate, ethylene, PAD4, and salicylate, are disabled, the hypersensitive response (HR) typical of ETI is abolished when the Pseudomonas syringae effector AvrRpt2 is bacterially delivered but is intact when AvrRpt2 is directly expressed in planta. These observations led us to discovery of a network-buffered signaling mechanism that mediates HR signaling and is strongly inhibited by PTI signaling. We named this mechanism the ETI-Mediating and PTI-Inhibited Sector (EMPIS). The signaling kinetics of EMPIS explain apparently different plant genetic requirements for ETI triggered by different effectors without postulating different signaling machineries. The properties of EMPIS suggest that information about efficacy of the early immune response is fed back to the immune signaling network, modulating its activity and limiting the fitness cost of unnecessary immune responses.

KW - deep perturbation

KW - fitness cost of immunity

KW - network resilience

KW - plant immune signaling network

UR - http://www.scopus.com/inward/record.url?scp=85029409180&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85029409180&partnerID=8YFLogxK

U2 - 10.15252/embj.201796529

DO - 10.15252/embj.201796529

M3 - Article

C2 - 28811287

AN - SCOPUS:85029409180

SN - 0261-4189

VL - 36

SP - 2758

EP - 2769

JO - EMBO Journal

JF - EMBO Journal

IS - 18

ER -

A plant effector-triggered immunity signaling sector is inhibited by pattern-triggered immunity

Abstract

Bibliographical note

Keywords

Publisher link

Find It

Other files and links

Fingerprint

Cite this