The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice

Kana Miyata, Toshinori Kozaki, Yusuke Kouzai, Kenjirou Ozawa, Kazuo Ishii, Erika Asamizu, Yoshihiro Okabe, Yosuke Umehara, Ayano Miyamoto, Yoshihiro Kobae, Kohki Akiyama, Hanae Kaku, Yoko Nishizawa, Naoto Shibuya, Tomomi Nakagawa

Research output: Contribution to journalArticle

95 Citations (Scopus)

Abstract

Plants are constantly exposed to threats from pathogenic microbes and thus developed an innate immune system to protect themselves. On the other hand, many plants also have the ability to establish endosymbiosis with beneficial microbes such as arbuscular mycorrhizal (AM) fungi or rhizobial bacteria, which improves the growth of host plants. How plants evolved these systems managing such opposite plant-microbe interactions is unclear. We show here that knockout (KO) mutants of OsCERK1, a rice receptor kinase essential for chitin signaling, were impaired not only for chitin-triggered defense responses but also for AM symbiosis, indicating the bifunctionality of OsCERK1 in defense and symbiosis. On the other hand, a KO mutant of OsCEBiP, which forms a receptor complex with OsCERK1 and is essential for chitin-triggered immunity, established mycorrhizal symbiosis normally. Therefore, OsCERK1 but not chitin-triggered immunity is required for AM symbiosis. Furthermore, experiments with chimeric receptors showed that the kinase domains of OsCERK1 and homologs from non-leguminous, mycorrhizal plants could trigger nodulation signaling in legume-rhizobium interactions as the kinase domain of Nod factor receptor1 (NFR1), which is essential for triggering the nodulation program in leguminous plants, did. Because leguminous plants are believed to have developed the rhizobial symbiosis on the basis of AM symbiosis, our results suggest that the symbiotic function of ancestral CERK1 in AM symbiosis enabled the molecular evolution to leguminous NFR1 and resulted in the establishment of legume-rhizobia symbiosis. These results also suggest that OsCERK1 and homologs serve as a molecular switch that activates defense or symbiotic responses depending on the infecting microbes.

Original languageEnglish
Pages (from-to)1864-1872
Number of pages9
JournalPlant and Cell Physiology
Volume55
Issue number11
DOIs
Publication statusPublished - Jun 27 2014
Externally publishedYes

Fingerprint

Chitin
Symbiosis
chitin
symbiosis
Immunity
immunity
rice
receptors
phosphotransferases (kinases)
Rhizobium
knockout mutants
Phosphotransferases
nodulation
microorganisms
Fabaceae
legumes
Oryza
beneficial microorganisms
Molecular Evolution
mycorrhizal fungi

Keywords

  • Arbuscular mycorrhizal fungi
  • Defense
  • Lotus japonicus
  • Rhizobia
  • Rice
  • Symbiosis

ASJC Scopus subject areas

  • Plant Science
  • Physiology
  • Cell Biology
  • Medicine(all)

Cite this

The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. / Miyata, Kana; Kozaki, Toshinori; Kouzai, Yusuke; Ozawa, Kenjirou; Ishii, Kazuo; Asamizu, Erika; Okabe, Yoshihiro; Umehara, Yosuke; Miyamoto, Ayano; Kobae, Yoshihiro; Akiyama, Kohki; Kaku, Hanae; Nishizawa, Yoko; Shibuya, Naoto; Nakagawa, Tomomi.

In: Plant and Cell Physiology, Vol. 55, No. 11, 27.06.2014, p. 1864-1872.

Research output: Contribution to journalArticle

Miyata, K, Kozaki, T, Kouzai, Y, Ozawa, K, Ishii, K, Asamizu, E, Okabe, Y, Umehara, Y, Miyamoto, A, Kobae, Y, Akiyama, K, Kaku, H, Nishizawa, Y, Shibuya, N & Nakagawa, T 2014, 'The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice', Plant and Cell Physiology, vol. 55, no. 11, pp. 1864-1872. https://doi.org/10.1093/pcp/pcu129
Miyata, Kana ; Kozaki, Toshinori ; Kouzai, Yusuke ; Ozawa, Kenjirou ; Ishii, Kazuo ; Asamizu, Erika ; Okabe, Yoshihiro ; Umehara, Yosuke ; Miyamoto, Ayano ; Kobae, Yoshihiro ; Akiyama, Kohki ; Kaku, Hanae ; Nishizawa, Yoko ; Shibuya, Naoto ; Nakagawa, Tomomi. / The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. In: Plant and Cell Physiology. 2014 ; Vol. 55, No. 11. pp. 1864-1872.
@article{e9ce5f1c2eb54aeeaeee0af5f1751910,
title = "The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice",
abstract = "Plants are constantly exposed to threats from pathogenic microbes and thus developed an innate immune system to protect themselves. On the other hand, many plants also have the ability to establish endosymbiosis with beneficial microbes such as arbuscular mycorrhizal (AM) fungi or rhizobial bacteria, which improves the growth of host plants. How plants evolved these systems managing such opposite plant-microbe interactions is unclear. We show here that knockout (KO) mutants of OsCERK1, a rice receptor kinase essential for chitin signaling, were impaired not only for chitin-triggered defense responses but also for AM symbiosis, indicating the bifunctionality of OsCERK1 in defense and symbiosis. On the other hand, a KO mutant of OsCEBiP, which forms a receptor complex with OsCERK1 and is essential for chitin-triggered immunity, established mycorrhizal symbiosis normally. Therefore, OsCERK1 but not chitin-triggered immunity is required for AM symbiosis. Furthermore, experiments with chimeric receptors showed that the kinase domains of OsCERK1 and homologs from non-leguminous, mycorrhizal plants could trigger nodulation signaling in legume-rhizobium interactions as the kinase domain of Nod factor receptor1 (NFR1), which is essential for triggering the nodulation program in leguminous plants, did. Because leguminous plants are believed to have developed the rhizobial symbiosis on the basis of AM symbiosis, our results suggest that the symbiotic function of ancestral CERK1 in AM symbiosis enabled the molecular evolution to leguminous NFR1 and resulted in the establishment of legume-rhizobia symbiosis. These results also suggest that OsCERK1 and homologs serve as a molecular switch that activates defense or symbiotic responses depending on the infecting microbes.",
keywords = "Arbuscular mycorrhizal fungi, Defense, Lotus japonicus, Rhizobia, Rice, Symbiosis",
author = "Kana Miyata and Toshinori Kozaki and Yusuke Kouzai and Kenjirou Ozawa and Kazuo Ishii and Erika Asamizu and Yoshihiro Okabe and Yosuke Umehara and Ayano Miyamoto and Yoshihiro Kobae and Kohki Akiyama and Hanae Kaku and Yoko Nishizawa and Naoto Shibuya and Tomomi Nakagawa",
year = "2014",
month = "6",
day = "27",
doi = "10.1093/pcp/pcu129",
language = "English",
volume = "55",
pages = "1864--1872",
journal = "Plant and Cell Physiology",
issn = "0032-0781",
publisher = "Oxford University Press",
number = "11",

}

TY - JOUR

T1 - The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice

AU - Miyata, Kana

AU - Kozaki, Toshinori

AU - Kouzai, Yusuke

AU - Ozawa, Kenjirou

AU - Ishii, Kazuo

AU - Asamizu, Erika

AU - Okabe, Yoshihiro

AU - Umehara, Yosuke

AU - Miyamoto, Ayano

AU - Kobae, Yoshihiro

AU - Akiyama, Kohki

AU - Kaku, Hanae

AU - Nishizawa, Yoko

AU - Shibuya, Naoto

AU - Nakagawa, Tomomi

PY - 2014/6/27

Y1 - 2014/6/27

N2 - Plants are constantly exposed to threats from pathogenic microbes and thus developed an innate immune system to protect themselves. On the other hand, many plants also have the ability to establish endosymbiosis with beneficial microbes such as arbuscular mycorrhizal (AM) fungi or rhizobial bacteria, which improves the growth of host plants. How plants evolved these systems managing such opposite plant-microbe interactions is unclear. We show here that knockout (KO) mutants of OsCERK1, a rice receptor kinase essential for chitin signaling, were impaired not only for chitin-triggered defense responses but also for AM symbiosis, indicating the bifunctionality of OsCERK1 in defense and symbiosis. On the other hand, a KO mutant of OsCEBiP, which forms a receptor complex with OsCERK1 and is essential for chitin-triggered immunity, established mycorrhizal symbiosis normally. Therefore, OsCERK1 but not chitin-triggered immunity is required for AM symbiosis. Furthermore, experiments with chimeric receptors showed that the kinase domains of OsCERK1 and homologs from non-leguminous, mycorrhizal plants could trigger nodulation signaling in legume-rhizobium interactions as the kinase domain of Nod factor receptor1 (NFR1), which is essential for triggering the nodulation program in leguminous plants, did. Because leguminous plants are believed to have developed the rhizobial symbiosis on the basis of AM symbiosis, our results suggest that the symbiotic function of ancestral CERK1 in AM symbiosis enabled the molecular evolution to leguminous NFR1 and resulted in the establishment of legume-rhizobia symbiosis. These results also suggest that OsCERK1 and homologs serve as a molecular switch that activates defense or symbiotic responses depending on the infecting microbes.

AB - Plants are constantly exposed to threats from pathogenic microbes and thus developed an innate immune system to protect themselves. On the other hand, many plants also have the ability to establish endosymbiosis with beneficial microbes such as arbuscular mycorrhizal (AM) fungi or rhizobial bacteria, which improves the growth of host plants. How plants evolved these systems managing such opposite plant-microbe interactions is unclear. We show here that knockout (KO) mutants of OsCERK1, a rice receptor kinase essential for chitin signaling, were impaired not only for chitin-triggered defense responses but also for AM symbiosis, indicating the bifunctionality of OsCERK1 in defense and symbiosis. On the other hand, a KO mutant of OsCEBiP, which forms a receptor complex with OsCERK1 and is essential for chitin-triggered immunity, established mycorrhizal symbiosis normally. Therefore, OsCERK1 but not chitin-triggered immunity is required for AM symbiosis. Furthermore, experiments with chimeric receptors showed that the kinase domains of OsCERK1 and homologs from non-leguminous, mycorrhizal plants could trigger nodulation signaling in legume-rhizobium interactions as the kinase domain of Nod factor receptor1 (NFR1), which is essential for triggering the nodulation program in leguminous plants, did. Because leguminous plants are believed to have developed the rhizobial symbiosis on the basis of AM symbiosis, our results suggest that the symbiotic function of ancestral CERK1 in AM symbiosis enabled the molecular evolution to leguminous NFR1 and resulted in the establishment of legume-rhizobia symbiosis. These results also suggest that OsCERK1 and homologs serve as a molecular switch that activates defense or symbiotic responses depending on the infecting microbes.

KW - Arbuscular mycorrhizal fungi

KW - Defense

KW - Lotus japonicus

KW - Rhizobia

KW - Rice

KW - Symbiosis

UR - http://www.scopus.com/inward/record.url?scp=84911964533&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84911964533&partnerID=8YFLogxK

U2 - 10.1093/pcp/pcu129

DO - 10.1093/pcp/pcu129

M3 - Article

C2 - 25231970

AN - SCOPUS:84911964533

VL - 55

SP - 1864

EP - 1872

JO - Plant and Cell Physiology

JF - Plant and Cell Physiology

SN - 0032-0781

IS - 11

ER -