Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis

Simon C. Groen, Noah K Whiteman, Adam K. Bahrami, Amity M. Wilczek, Jianping Cui, Jacob A. Russell, Angelica Cibrian-Jaramillo, Ian A. Butler, Jignasha D. Rana, Guo Hua Huang, Jenifer Bush, Frederick M. Ausubel, Naomi E. Pierce

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Multicellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites.We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemicinduced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.

Original languageEnglish (US)
Pages (from-to)4755-4766
Number of pages12
JournalPlant Cell
Volume25
Issue number11
DOIs
StatePublished - Nov 2013

Fingerprint

Herbivory
Arabidopsis
Trichoplusia ni
Isoleucine
ethylene
herbivores
isoleucine
jasmonic acid
Pseudomonas syringae
Salicylic Acid
pathogens
salicylic acid
Parasites
parasites
Moths
Brassica
Infection
defense mechanisms
plant pathogens
infection

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Groen, S. C., Whiteman, N. K., Bahrami, A. K., Wilczek, A. M., Cui, J., Russell, J. A., ... Pierce, N. E. (2013). Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis. Plant Cell, 25(11), 4755-4766. https://doi.org/10.1105/tpc.113.113415

Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis. / Groen, Simon C.; Whiteman, Noah K; Bahrami, Adam K.; Wilczek, Amity M.; Cui, Jianping; Russell, Jacob A.; Cibrian-Jaramillo, Angelica; Butler, Ian A.; Rana, Jignasha D.; Huang, Guo Hua; Bush, Jenifer; Ausubel, Frederick M.; Pierce, Naomi E.

In: Plant Cell, Vol. 25, No. 11, 11.2013, p. 4755-4766.

Research output: Contribution to journalArticle

Groen, SC, Whiteman, NK, Bahrami, AK, Wilczek, AM, Cui, J, Russell, JA, Cibrian-Jaramillo, A, Butler, IA, Rana, JD, Huang, GH, Bush, J, Ausubel, FM & Pierce, NE 2013, 'Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis', Plant Cell, vol. 25, no. 11, pp. 4755-4766. https://doi.org/10.1105/tpc.113.113415
Groen, Simon C. ; Whiteman, Noah K ; Bahrami, Adam K. ; Wilczek, Amity M. ; Cui, Jianping ; Russell, Jacob A. ; Cibrian-Jaramillo, Angelica ; Butler, Ian A. ; Rana, Jignasha D. ; Huang, Guo Hua ; Bush, Jenifer ; Ausubel, Frederick M. ; Pierce, Naomi E. / Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis. In: Plant Cell. 2013 ; Vol. 25, No. 11. pp. 4755-4766.
@article{97bbee5fb44f4321b8377490ce0964e5,
title = "Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis",
abstract = "Multicellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites.We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemicinduced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.",
author = "Groen, {Simon C.} and Whiteman, {Noah K} and Bahrami, {Adam K.} and Wilczek, {Amity M.} and Jianping Cui and Russell, {Jacob A.} and Angelica Cibrian-Jaramillo and Butler, {Ian A.} and Rana, {Jignasha D.} and Huang, {Guo Hua} and Jenifer Bush and Ausubel, {Frederick M.} and Pierce, {Naomi E.}",
year = "2013",
month = "11",
doi = "10.1105/tpc.113.113415",
language = "English (US)",
volume = "25",
pages = "4755--4766",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "11",

}

TY - JOUR

T1 - Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis

AU - Groen, Simon C.

AU - Whiteman, Noah K

AU - Bahrami, Adam K.

AU - Wilczek, Amity M.

AU - Cui, Jianping

AU - Russell, Jacob A.

AU - Cibrian-Jaramillo, Angelica

AU - Butler, Ian A.

AU - Rana, Jignasha D.

AU - Huang, Guo Hua

AU - Bush, Jenifer

AU - Ausubel, Frederick M.

AU - Pierce, Naomi E.

PY - 2013/11

Y1 - 2013/11

N2 - Multicellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites.We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemicinduced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.

AB - Multicellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites.We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemicinduced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.

UR - http://www.scopus.com/inward/record.url?scp=84891519640&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84891519640&partnerID=8YFLogxK

U2 - 10.1105/tpc.113.113415

DO - 10.1105/tpc.113.113415

M3 - Article

VL - 25

SP - 4755

EP - 4766

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 11

ER -