A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation

Jaslyn E.M.M. Wong, Marcin Nadzieja, Lene H. Madsen, Christoph A. Bücherl, Svend Dam, Niels N. Sandal, Daniel Couto, Paul Derbyshire, Mette Uldum-Berentsen, Sina Schroeder, Veit Schwämmle, Fábio C.S. Nogueira, Mette H. Asmussen, Søren Thirup, Simona Radutoiu, Mickaël Blaise, Kasper R. Andersen, Frank L.H. Menke, Cyril Zipfel, Jens Stougaard*

*Kontaktforfatter for dette arbejde

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

The establishment of nitrogen-fixing root nodules in legume–rhi-zobia symbiosis requires an intricate communication between the host plant and its symbiont. We are, however, limited in our understanding of the symbiosis signaling process. In particular, how membrane-localized receptors of legumes activate signal transduction following perception of rhizobial signaling molecules has mostly remained elusive. To address this, we performed a coimmunoprecipitation-based proteomics screen to identify proteins associated with Nod factor receptor 5 (NFR5) in Lotus japonicus. Out of 51 NFR5-associated proteins, we focused on a receptor-like cytoplasmic kinase (RLCK), which we named NFR5-interacting cytoplasmic kinase 4 (NiCK4). NiCK4 associates with heterologously expressed NFR5 in Nicotiana benthamiana, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level, Nick4 is coexpressed with Nfr5 in root hairs and nodule cells, and the NiCK4 protein relocates to the nucleus in an NFR5/NFR1-dependent manner upon Nod factor treatment. Phenotyping of retrotransposon insertion mutants revealed that NiCK4 promotes nodule organogenesis. Together, these results suggest that the identified RLCK, NiCK4, acts as a component of the Nod factor signaling pathway downstream of NFR5.

OriginalsprogEngelsk
TidsskriftProceedings of the National Academy of Sciences of the United States of America
Vol/bind116
Udgave nummer28
Sider (fra-til)14339-14348
Antal sider10
ISSN0027-8424
DOI
StatusUdgivet - 25. jun. 2019

Fingeraftryk

Cytoplasmic and Nuclear Receptors
Fabaceae
Loteae
Proteins
Nitrogen
Communication
Membranes
In Vitro Techniques

Citer dette

Wong, Jaslyn E.M.M. ; Nadzieja, Marcin ; Madsen, Lene H. ; Bücherl, Christoph A. ; Dam, Svend ; Sandal, Niels N. ; Couto, Daniel ; Derbyshire, Paul ; Uldum-Berentsen, Mette ; Schroeder, Sina ; Schwämmle, Veit ; Nogueira, Fábio C.S. ; Asmussen, Mette H. ; Thirup, Søren ; Radutoiu, Simona ; Blaise, Mickaël ; Andersen, Kasper R. ; Menke, Frank L.H. ; Zipfel, Cyril ; Stougaard, Jens. / A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation. I: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Bind 116, Nr. 28. s. 14339-14348.
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title = "A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation",
abstract = "The establishment of nitrogen-fixing root nodules in legume–rhi-zobia symbiosis requires an intricate communication between the host plant and its symbiont. We are, however, limited in our understanding of the symbiosis signaling process. In particular, how membrane-localized receptors of legumes activate signal transduction following perception of rhizobial signaling molecules has mostly remained elusive. To address this, we performed a coimmunoprecipitation-based proteomics screen to identify proteins associated with Nod factor receptor 5 (NFR5) in Lotus japonicus. Out of 51 NFR5-associated proteins, we focused on a receptor-like cytoplasmic kinase (RLCK), which we named NFR5-interacting cytoplasmic kinase 4 (NiCK4). NiCK4 associates with heterologously expressed NFR5 in Nicotiana benthamiana, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level, Nick4 is coexpressed with Nfr5 in root hairs and nodule cells, and the NiCK4 protein relocates to the nucleus in an NFR5/NFR1-dependent manner upon Nod factor treatment. Phenotyping of retrotransposon insertion mutants revealed that NiCK4 promotes nodule organogenesis. Together, these results suggest that the identified RLCK, NiCK4, acts as a component of the Nod factor signaling pathway downstream of NFR5.",
keywords = "Lotus, NFR5, NiCK4, Nodulation, RLCK",
author = "Wong, {Jaslyn E.M.M.} and Marcin Nadzieja and Madsen, {Lene H.} and B{\"u}cherl, {Christoph A.} and Svend Dam and Sandal, {Niels N.} and Daniel Couto and Paul Derbyshire and Mette Uldum-Berentsen and Sina Schroeder and Veit Schw{\"a}mmle and Nogueira, {F{\'a}bio C.S.} and Asmussen, {Mette H.} and S{\o}ren Thirup and Simona Radutoiu and Micka{\"e}l Blaise and Andersen, {Kasper R.} and Menke, {Frank L.H.} and Cyril Zipfel and Jens Stougaard",
year = "2019",
month = "6",
day = "25",
doi = "10.1073/pnas.1815425116",
language = "English",
volume = "116",
pages = "14339--14348",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "28",

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Wong, JEMM, Nadzieja, M, Madsen, LH, Bücherl, CA, Dam, S, Sandal, NN, Couto, D, Derbyshire, P, Uldum-Berentsen, M, Schroeder, S, Schwämmle, V, Nogueira, FCS, Asmussen, MH, Thirup, S, Radutoiu, S, Blaise, M, Andersen, KR, Menke, FLH, Zipfel, C & Stougaard, J 2019, 'A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation', Proceedings of the National Academy of Sciences of the United States of America, bind 116, nr. 28, s. 14339-14348. https://doi.org/10.1073/pnas.1815425116

A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation. / Wong, Jaslyn E.M.M.; Nadzieja, Marcin; Madsen, Lene H.; Bücherl, Christoph A.; Dam, Svend; Sandal, Niels N.; Couto, Daniel; Derbyshire, Paul; Uldum-Berentsen, Mette; Schroeder, Sina; Schwämmle, Veit; Nogueira, Fábio C.S.; Asmussen, Mette H.; Thirup, Søren; Radutoiu, Simona; Blaise, Mickaël; Andersen, Kasper R.; Menke, Frank L.H.; Zipfel, Cyril; Stougaard, Jens.

I: Proceedings of the National Academy of Sciences of the United States of America, Bind 116, Nr. 28, 25.06.2019, s. 14339-14348.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - A Lotus japonicus cytoplasmic kinase connects Nod factor perception by the NFR5 LysM receptor to nodulation

AU - Wong, Jaslyn E.M.M.

AU - Nadzieja, Marcin

AU - Madsen, Lene H.

AU - Bücherl, Christoph A.

AU - Dam, Svend

AU - Sandal, Niels N.

AU - Couto, Daniel

AU - Derbyshire, Paul

AU - Uldum-Berentsen, Mette

AU - Schroeder, Sina

AU - Schwämmle, Veit

AU - Nogueira, Fábio C.S.

AU - Asmussen, Mette H.

AU - Thirup, Søren

AU - Radutoiu, Simona

AU - Blaise, Mickaël

AU - Andersen, Kasper R.

AU - Menke, Frank L.H.

AU - Zipfel, Cyril

AU - Stougaard, Jens

PY - 2019/6/25

Y1 - 2019/6/25

N2 - The establishment of nitrogen-fixing root nodules in legume–rhi-zobia symbiosis requires an intricate communication between the host plant and its symbiont. We are, however, limited in our understanding of the symbiosis signaling process. In particular, how membrane-localized receptors of legumes activate signal transduction following perception of rhizobial signaling molecules has mostly remained elusive. To address this, we performed a coimmunoprecipitation-based proteomics screen to identify proteins associated with Nod factor receptor 5 (NFR5) in Lotus japonicus. Out of 51 NFR5-associated proteins, we focused on a receptor-like cytoplasmic kinase (RLCK), which we named NFR5-interacting cytoplasmic kinase 4 (NiCK4). NiCK4 associates with heterologously expressed NFR5 in Nicotiana benthamiana, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level, Nick4 is coexpressed with Nfr5 in root hairs and nodule cells, and the NiCK4 protein relocates to the nucleus in an NFR5/NFR1-dependent manner upon Nod factor treatment. Phenotyping of retrotransposon insertion mutants revealed that NiCK4 promotes nodule organogenesis. Together, these results suggest that the identified RLCK, NiCK4, acts as a component of the Nod factor signaling pathway downstream of NFR5.

AB - The establishment of nitrogen-fixing root nodules in legume–rhi-zobia symbiosis requires an intricate communication between the host plant and its symbiont. We are, however, limited in our understanding of the symbiosis signaling process. In particular, how membrane-localized receptors of legumes activate signal transduction following perception of rhizobial signaling molecules has mostly remained elusive. To address this, we performed a coimmunoprecipitation-based proteomics screen to identify proteins associated with Nod factor receptor 5 (NFR5) in Lotus japonicus. Out of 51 NFR5-associated proteins, we focused on a receptor-like cytoplasmic kinase (RLCK), which we named NFR5-interacting cytoplasmic kinase 4 (NiCK4). NiCK4 associates with heterologously expressed NFR5 in Nicotiana benthamiana, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level, Nick4 is coexpressed with Nfr5 in root hairs and nodule cells, and the NiCK4 protein relocates to the nucleus in an NFR5/NFR1-dependent manner upon Nod factor treatment. Phenotyping of retrotransposon insertion mutants revealed that NiCK4 promotes nodule organogenesis. Together, these results suggest that the identified RLCK, NiCK4, acts as a component of the Nod factor signaling pathway downstream of NFR5.

KW - Lotus

KW - NFR5

KW - NiCK4

KW - Nodulation

KW - RLCK

U2 - 10.1073/pnas.1815425116

DO - 10.1073/pnas.1815425116

M3 - Journal article

VL - 116

SP - 14339

EP - 14348

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 28

ER -