A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis

Simon Boje Hansen; Thi Bich Luu; Kira Gysel; Damiano Lironi; Christina Krönauer; Henriette Rübsam; Ingeborg Bitsch Jensen; Magdalini Tsitsikli; Thea Gramkov Birkefeldt; Alen Trgovcevic; Jens Stougaard; Simona Radutoiu; Kasper Røjkjær Andersen

doi:10.1073/pnas.2405671121

A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis

Simon Boje Hansen, Thi Bich Luu, Kira Gysel, Damiano Lironi, Christina Krönauer, Henriette Rübsam, Ingeborg Bitsch Jensen, Magdalini Tsitsikli, Thea Gramkov Birkefeldt, Alen Trgovcevic, Jens Stougaard, Simona Radutoiu, Kasper Røjkjær Andersen

Department of Molecular Biology and Genetics - Plant Molecular Biology

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this "juxtamembrane motif" promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.

Original language	English
Article number	e2405671121
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	121
Issue	46
Pages (from-to)	e2405671121
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.2405671121
Publication status	Published - Nov 2024

Keywords

kinases and pseudokinases
Nod factor receptors
plant–microbe interactions
receptor signaling
root nodule symbiosis

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10.1073/pnas.2405671121

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Hansen, S. B., Luu, T. B., Gysel, K., Lironi, D., Krönauer, C., Rübsam, H., Jensen, I. B., Tsitsikli, M., Birkefeldt, T. G., Trgovcevic, A., Stougaard, J., Radutoiu, S., & Andersen, K. R. (2024). A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 121(46), e2405671121. Article e2405671121. https://doi.org/10.1073/pnas.2405671121

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title = "A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis",

abstract = "Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this {"}juxtamembrane motif{"} promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.",

keywords = "kinases and pseudokinases, Nod factor receptors, plant–microbe interactions, receptor signaling, root nodule symbiosis",

author = "Hansen, {Simon Boje} and Luu, {Thi Bich} and Kira Gysel and Damiano Lironi and Christina Kr{\"o}nauer and Henriette R{\"u}bsam and Jensen, {Ingeborg Bitsch} and Magdalini Tsitsikli and Birkefeldt, {Thea Gramkov} and Alen Trgovcevic and Jens Stougaard and Simona Radutoiu and Andersen, {Kasper R{\o}jkj{\ae}r}",

year = "2024",

month = nov,

doi = "10.1073/pnas.2405671121",

language = "English",

volume = "121",

pages = "e2405671121",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

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Hansen, SB, Luu, TB , Gysel, K, Lironi, D, Krönauer, C, Rübsam, H, Jensen, IB, Tsitsikli, M, Birkefeldt, TG, Trgovcevic, A , Stougaard, J , Radutoiu, S & Andersen, KR 2024, 'A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis', Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 46, e2405671121, pp. e2405671121. https://doi.org/10.1073/pnas.2405671121

A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis. / Hansen, Simon Boje; Luu, Thi Bich ; Gysel, Kira et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 121, No. 46, e2405671121, 11.2024, p. e2405671121.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis

AU - Hansen, Simon Boje

AU - Luu, Thi Bich

AU - Gysel, Kira

AU - Lironi, Damiano

AU - Krönauer, Christina

AU - Rübsam, Henriette

AU - Jensen, Ingeborg Bitsch

AU - Tsitsikli, Magdalini

AU - Birkefeldt, Thea Gramkov

AU - Trgovcevic, Alen

AU - Stougaard, Jens

AU - Radutoiu, Simona

AU - Andersen, Kasper Røjkjær

PY - 2024/11

Y1 - 2024/11

N2 - Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this "juxtamembrane motif" promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.

AB - Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this "juxtamembrane motif" promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.

KW - kinases and pseudokinases

KW - Nod factor receptors

KW - plant–microbe interactions

KW - receptor signaling

KW - root nodule symbiosis

UR - http://www.scopus.com/inward/record.url?scp=85208517046&partnerID=8YFLogxK

U2 - 10.1073/pnas.2405671121

DO - 10.1073/pnas.2405671121

M3 - Journal article

C2 - 39495923

AN - SCOPUS:85208517046

SN - 0027-8424

VL - 121

SP - e2405671121

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

IS - 46

M1 - e2405671121

ER -

A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis

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