Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences

Wei Lin Wan, Lisha Zhang, Rory Pruitt, Maricris Zaidem, Rik Brugman, Xiyu Ma, Elzbieta Krol, Artemis Perraki, Joachim Kilian, Guido Grossmann, Mark Stahl, Libo Shan, Cyril Zipfel, Jan A.L. van Kan, Rainer Hedrich, Detlef Weigel, Andrea A. Gust*, Thorsten Nürnberger

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

Pattern recognition receptors (PRRs) sense microbial patterns and activate innate immunity against attempted microbial invasions. The leucine-rich repeat receptor kinases (LRR-RK) FLS2 and EFR, and the LRR receptor protein (LRR-RP) receptors RLP23 and RLP42, respectively, represent prototypical members of these two prominent and closely related PRR families. We conducted a survey of Arabidopsis thaliana immune signaling mediated by these receptors to address the question of commonalities and differences between LRR-RK and LRR-RP signaling. Quantitative differences in timing and amplitude were observed for several early immune responses, with RP-mediated responses typically being slower and more prolonged than those mediated by RKs. Activation of RLP23, but not FLS2, induced the production of camalexin. Transcriptomic analysis revealed that RLP23-regulated genes represent only a fraction of those genes differentially expressed upon FLS2 activation. Several positive and negative regulators of FLS2-signaling play similar roles in RLP23 signaling. Intriguingly, the cytoplasmic receptor kinase BIK1, a positive regulator of RK signaling, acts as a negative regulator of RP-type immune receptors in a manner dependent on BIK1 kinase activity. Our study unveiled unexpected differences in two closely related receptor systems and reports a new negative role of BIK1 in plant immunity.

Original languageEnglish
Pages (from-to)2080-2095
JournalNew Phytologist
Volume221
Issue number4
Early online date25 Sep 2018
DOIs
Publication statusPublished - Mar 2019

Fingerprint

Arabidopsis
Protein Kinases
phosphotransferases (kinases)
Phosphotransferases
Pattern Recognition Receptors
receptors
Leucine
proteins
Plant Immunity
Cytoplasmic and Nuclear Receptors
Innate Immunity
Genes
Proteins
leucine
transcriptomics
genes
Arabidopsis thaliana
immunity
immune response

Keywords

  • Arabidopsis
  • immune receptor
  • immune signaling comparison
  • plant immunity
  • receptor kinase
  • receptor protein

Cite this

Wan, W. L., Zhang, L., Pruitt, R., Zaidem, M., Brugman, R., Ma, X., ... Nürnberger, T. (2019). Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences. New Phytologist, 221(4), 2080-2095. https://doi.org/10.1111/nph.15497
Wan, Wei Lin ; Zhang, Lisha ; Pruitt, Rory ; Zaidem, Maricris ; Brugman, Rik ; Ma, Xiyu ; Krol, Elzbieta ; Perraki, Artemis ; Kilian, Joachim ; Grossmann, Guido ; Stahl, Mark ; Shan, Libo ; Zipfel, Cyril ; van Kan, Jan A.L. ; Hedrich, Rainer ; Weigel, Detlef ; Gust, Andrea A. ; Nürnberger, Thorsten. / Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences. In: New Phytologist. 2019 ; Vol. 221, No. 4. pp. 2080-2095.
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abstract = "Pattern recognition receptors (PRRs) sense microbial patterns and activate innate immunity against attempted microbial invasions. The leucine-rich repeat receptor kinases (LRR-RK) FLS2 and EFR, and the LRR receptor protein (LRR-RP) receptors RLP23 and RLP42, respectively, represent prototypical members of these two prominent and closely related PRR families. We conducted a survey of Arabidopsis thaliana immune signaling mediated by these receptors to address the question of commonalities and differences between LRR-RK and LRR-RP signaling. Quantitative differences in timing and amplitude were observed for several early immune responses, with RP-mediated responses typically being slower and more prolonged than those mediated by RKs. Activation of RLP23, but not FLS2, induced the production of camalexin. Transcriptomic analysis revealed that RLP23-regulated genes represent only a fraction of those genes differentially expressed upon FLS2 activation. Several positive and negative regulators of FLS2-signaling play similar roles in RLP23 signaling. Intriguingly, the cytoplasmic receptor kinase BIK1, a positive regulator of RK signaling, acts as a negative regulator of RP-type immune receptors in a manner dependent on BIK1 kinase activity. Our study unveiled unexpected differences in two closely related receptor systems and reports a new negative role of BIK1 in plant immunity.",
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Wan, WL, Zhang, L, Pruitt, R, Zaidem, M, Brugman, R, Ma, X, Krol, E, Perraki, A, Kilian, J, Grossmann, G, Stahl, M, Shan, L, Zipfel, C, van Kan, JAL, Hedrich, R, Weigel, D, Gust, AA & Nürnberger, T 2019, 'Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences', New Phytologist, vol. 221, no. 4, pp. 2080-2095. https://doi.org/10.1111/nph.15497

Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences. / Wan, Wei Lin; Zhang, Lisha; Pruitt, Rory; Zaidem, Maricris; Brugman, Rik; Ma, Xiyu; Krol, Elzbieta; Perraki, Artemis; Kilian, Joachim; Grossmann, Guido; Stahl, Mark; Shan, Libo; Zipfel, Cyril; van Kan, Jan A.L.; Hedrich, Rainer; Weigel, Detlef; Gust, Andrea A.; Nürnberger, Thorsten.

In: New Phytologist, Vol. 221, No. 4, 03.2019, p. 2080-2095.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Comparing Arabidopsis receptor kinase and receptor protein-mediated immune signaling reveals BIK1-dependent differences

AU - Wan, Wei Lin

AU - Zhang, Lisha

AU - Pruitt, Rory

AU - Zaidem, Maricris

AU - Brugman, Rik

AU - Ma, Xiyu

AU - Krol, Elzbieta

AU - Perraki, Artemis

AU - Kilian, Joachim

AU - Grossmann, Guido

AU - Stahl, Mark

AU - Shan, Libo

AU - Zipfel, Cyril

AU - van Kan, Jan A.L.

AU - Hedrich, Rainer

AU - Weigel, Detlef

AU - Gust, Andrea A.

AU - Nürnberger, Thorsten

PY - 2019/3

Y1 - 2019/3

N2 - Pattern recognition receptors (PRRs) sense microbial patterns and activate innate immunity against attempted microbial invasions. The leucine-rich repeat receptor kinases (LRR-RK) FLS2 and EFR, and the LRR receptor protein (LRR-RP) receptors RLP23 and RLP42, respectively, represent prototypical members of these two prominent and closely related PRR families. We conducted a survey of Arabidopsis thaliana immune signaling mediated by these receptors to address the question of commonalities and differences between LRR-RK and LRR-RP signaling. Quantitative differences in timing and amplitude were observed for several early immune responses, with RP-mediated responses typically being slower and more prolonged than those mediated by RKs. Activation of RLP23, but not FLS2, induced the production of camalexin. Transcriptomic analysis revealed that RLP23-regulated genes represent only a fraction of those genes differentially expressed upon FLS2 activation. Several positive and negative regulators of FLS2-signaling play similar roles in RLP23 signaling. Intriguingly, the cytoplasmic receptor kinase BIK1, a positive regulator of RK signaling, acts as a negative regulator of RP-type immune receptors in a manner dependent on BIK1 kinase activity. Our study unveiled unexpected differences in two closely related receptor systems and reports a new negative role of BIK1 in plant immunity.

AB - Pattern recognition receptors (PRRs) sense microbial patterns and activate innate immunity against attempted microbial invasions. The leucine-rich repeat receptor kinases (LRR-RK) FLS2 and EFR, and the LRR receptor protein (LRR-RP) receptors RLP23 and RLP42, respectively, represent prototypical members of these two prominent and closely related PRR families. We conducted a survey of Arabidopsis thaliana immune signaling mediated by these receptors to address the question of commonalities and differences between LRR-RK and LRR-RP signaling. Quantitative differences in timing and amplitude were observed for several early immune responses, with RP-mediated responses typically being slower and more prolonged than those mediated by RKs. Activation of RLP23, but not FLS2, induced the production of camalexin. Transcriptomic analysis revealed that RLP23-regulated genes represent only a fraction of those genes differentially expressed upon FLS2 activation. Several positive and negative regulators of FLS2-signaling play similar roles in RLP23 signaling. Intriguingly, the cytoplasmic receptor kinase BIK1, a positive regulator of RK signaling, acts as a negative regulator of RP-type immune receptors in a manner dependent on BIK1 kinase activity. Our study unveiled unexpected differences in two closely related receptor systems and reports a new negative role of BIK1 in plant immunity.

KW - Arabidopsis

KW - immune receptor

KW - immune signaling comparison

KW - plant immunity

KW - receptor kinase

KW - receptor protein

U2 - 10.1111/nph.15497

DO - 10.1111/nph.15497

M3 - Article

VL - 221

SP - 2080

EP - 2095

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 4

ER -