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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 (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, 116(28):14339-14348.

Abstract

The establishment of nitrogen-fixing root nodules in legume–rhizobia 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<jats:italic>Lotus japonicus.</jats:italic>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<jats:italic>Nicotiana benthamiana</jats:italic>, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level,<jats:italic>Nick4</jats:italic>is coexpressed with<jats:italic>Nfr5</jats:italic>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.

Abstract

The establishment of nitrogen-fixing root nodules in legume–rhizobia 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<jats:italic>Lotus japonicus.</jats:italic>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<jats:italic>Nicotiana benthamiana</jats:italic>, and directly binds and phosphorylates the cytoplasmic domains of NFR5 and NFR1 in vitro. At the cellular level,<jats:italic>Nick4</jats:italic>is coexpressed with<jats:italic>Nfr5</jats:italic>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.

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Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Zurich-Basel Plant Science Center
Dewey Decimal Classification:580 Plants (Botany)
Scopus Subject Areas:Health Sciences > Multidisciplinary
Uncontrolled Keywords:Multidisciplinary
Language:English
Date:9 July 2019
Deposited On:31 Jul 2019 13:39
Last Modified:29 Jul 2020 11:02
Publisher:National Academy of Sciences
ISSN:0027-8424
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1073/pnas.1815425116

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