The oomycete microbe-associated molecular pattern Pep-13 triggers SERK3/BAK1-independent plant immunity

Haixia Wang, Huan He, Yetong Qi, Hazel McLellan, Zhejuan Tian, Paul R. J. Birch, Zhendong Tian (Lead / Corresponding author)

Research output: Contribution to journalArticle

Abstract

To prevent disease, pattern recognition receptors (PRRs) are responsible for detecting microbe-associated molecular patterns (MAMPs) to switch on plant innate immunity. SOMATIC EMBROYOGENESIS KINASE 3 (SERK3)/BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) is a well-characterized receptor-like kinase (RLK) that serves as a pivotal co-receptor with PRRs to activate immunity following recognition of MAMPs including flg22, EF-Tu, INF1 and XEG1. However, the requirement for SERK3/BAK1 in many pattern-triggered immune (PTI) signaling pathways is not yet known. Pep-13 is an oomycete MAMP that consists of a highly conserved motif (an oligopeptide of 13 amino acids) shared in Phytophthora transglutaminases. Quantitative RT-PCR analysis reveals that the transcripts of three PTI marker genes (WRKY7, WRKY8 and ACRE31) rapidly accumulate in response to three different MAMPs: flg22, chitin and Pep-13. Whereas silencing of SERK3/BAK1 in Nicotiana benthamiana or potato compromised transcript accumulation in response to flg22, it did not attenuate WRKY7, WRKY8 and ACRE31 up-regulation in response to chitin or Pep-13. This indicates that Pep-13 triggers immunity in a SERK3/BAK1-independent manner, similar to chitin. Surprisingly, silencing of SERK3/BAK1 led to significantly increased accumulation of PTI marker gene transcripts following Pep-13 or chitin treatment, compared to controls. This was accompanied by reduced expression of brassinosteroid (BR) marker genes StSTDH, StEXP8 and StCAB50 and StCHL1, which is a negative regulator of PTI, supporting previous reports that SERK3/BAK1-dependent BR signaling attenuates plant immunity. We provide Pep-13 as an alternative to chitin as a trigger of SERK3/BAK1-independent immunity.

Original languageEnglish
Pages (from-to)173-182
Number of pages10
JournalPlant Cell Reports
Volume38
Issue number2
Early online date28 Nov 2018
DOIs
Publication statusPublished - Feb 2019

Fingerprint

brassinosteroids
Oomycetes
phosphotransferases (kinases)
immunity
microorganisms
chitin
receptors
genetic markers
oligopeptides
Nicotiana benthamiana
protein-glutamine gamma-glutamyltransferase
Phytophthora

Keywords

  • Disease resistance
  • Flagellin
  • Late blight
  • MAMP
  • Transcriptome
  • Plant Immunity/drug effects
  • Gene Expression Regulation, Plant/drug effects
  • RNA, Messenger/genetics
  • Brassinosteroids/pharmacology
  • Flagellin/pharmacology
  • RNA Interference
  • Alarmins/metabolism
  • Plant Proteins/genetics
  • Plants, Genetically Modified
  • Tobacco/genetics
  • Peptides/pharmacology
  • Chitin/pharmacology
  • Transcription, Genetic/drug effects
  • Solanum tuberosum/genetics
  • Phytophthora infestans/drug effects

Cite this

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title = "The oomycete microbe-associated molecular pattern Pep-13 triggers SERK3/BAK1-independent plant immunity",
abstract = "To prevent disease, pattern recognition receptors (PRRs) are responsible for detecting microbe-associated molecular patterns (MAMPs) to switch on plant innate immunity. SOMATIC EMBROYOGENESIS KINASE 3 (SERK3)/BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) is a well-characterized receptor-like kinase (RLK) that serves as a pivotal co-receptor with PRRs to activate immunity following recognition of MAMPs including flg22, EF-Tu, INF1 and XEG1. However, the requirement for SERK3/BAK1 in many pattern-triggered immune (PTI) signaling pathways is not yet known. Pep-13 is an oomycete MAMP that consists of a highly conserved motif (an oligopeptide of 13 amino acids) shared in Phytophthora transglutaminases. Quantitative RT-PCR analysis reveals that the transcripts of three PTI marker genes (WRKY7, WRKY8 and ACRE31) rapidly accumulate in response to three different MAMPs: flg22, chitin and Pep-13. Whereas silencing of SERK3/BAK1 in Nicotiana benthamiana or potato compromised transcript accumulation in response to flg22, it did not attenuate WRKY7, WRKY8 and ACRE31 up-regulation in response to chitin or Pep-13. This indicates that Pep-13 triggers immunity in a SERK3/BAK1-independent manner, similar to chitin. Surprisingly, silencing of SERK3/BAK1 led to significantly increased accumulation of PTI marker gene transcripts following Pep-13 or chitin treatment, compared to controls. This was accompanied by reduced expression of brassinosteroid (BR) marker genes StSTDH, StEXP8 and StCAB50 and StCHL1, which is a negative regulator of PTI, supporting previous reports that SERK3/BAK1-dependent BR signaling attenuates plant immunity. We provide Pep-13 as an alternative to chitin as a trigger of SERK3/BAK1-independent immunity.",
keywords = "Disease resistance, Flagellin, Late blight, MAMP, Transcriptome, Plant Immunity/drug effects, Gene Expression Regulation, Plant/drug effects, RNA, Messenger/genetics, Brassinosteroids/pharmacology, Flagellin/pharmacology, RNA Interference, Alarmins/metabolism, Plant Proteins/genetics, Plants, Genetically Modified, Tobacco/genetics, Peptides/pharmacology, Chitin/pharmacology, Transcription, Genetic/drug effects, Solanum tuberosum/genetics, Phytophthora infestans/drug effects",
author = "Haixia Wang and Huan He and Yetong Qi and Hazel McLellan and Zhejuan Tian and Birch, {Paul R. J.} and Zhendong Tian",
note = "Funding for this research was provided by: National Natural Science Foundation of China (31761143007, 31171603) Biotechnology and Biological Sciences Research Council (BB/L026880/1) Fundamental Research Funds for the Central Universities (CN) (2662017PY069)",
year = "2019",
month = "2",
doi = "10.1007/s00299-018-2359-5",
language = "English",
volume = "38",
pages = "173--182",
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issn = "0721-7714",
publisher = "Springer Verlag",
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The oomycete microbe-associated molecular pattern Pep-13 triggers SERK3/BAK1-independent plant immunity. / Wang, Haixia; He, Huan; Qi, Yetong; McLellan, Hazel; Tian, Zhejuan; Birch, Paul R. J.; Tian, Zhendong (Lead / Corresponding author).

In: Plant Cell Reports, Vol. 38, No. 2, 02.2019, p. 173-182.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The oomycete microbe-associated molecular pattern Pep-13 triggers SERK3/BAK1-independent plant immunity

AU - Wang, Haixia

AU - He, Huan

AU - Qi, Yetong

AU - McLellan, Hazel

AU - Tian, Zhejuan

AU - Birch, Paul R. J.

AU - Tian, Zhendong

N1 - Funding for this research was provided by: National Natural Science Foundation of China (31761143007, 31171603) Biotechnology and Biological Sciences Research Council (BB/L026880/1) Fundamental Research Funds for the Central Universities (CN) (2662017PY069)

PY - 2019/2

Y1 - 2019/2

N2 - To prevent disease, pattern recognition receptors (PRRs) are responsible for detecting microbe-associated molecular patterns (MAMPs) to switch on plant innate immunity. SOMATIC EMBROYOGENESIS KINASE 3 (SERK3)/BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) is a well-characterized receptor-like kinase (RLK) that serves as a pivotal co-receptor with PRRs to activate immunity following recognition of MAMPs including flg22, EF-Tu, INF1 and XEG1. However, the requirement for SERK3/BAK1 in many pattern-triggered immune (PTI) signaling pathways is not yet known. Pep-13 is an oomycete MAMP that consists of a highly conserved motif (an oligopeptide of 13 amino acids) shared in Phytophthora transglutaminases. Quantitative RT-PCR analysis reveals that the transcripts of three PTI marker genes (WRKY7, WRKY8 and ACRE31) rapidly accumulate in response to three different MAMPs: flg22, chitin and Pep-13. Whereas silencing of SERK3/BAK1 in Nicotiana benthamiana or potato compromised transcript accumulation in response to flg22, it did not attenuate WRKY7, WRKY8 and ACRE31 up-regulation in response to chitin or Pep-13. This indicates that Pep-13 triggers immunity in a SERK3/BAK1-independent manner, similar to chitin. Surprisingly, silencing of SERK3/BAK1 led to significantly increased accumulation of PTI marker gene transcripts following Pep-13 or chitin treatment, compared to controls. This was accompanied by reduced expression of brassinosteroid (BR) marker genes StSTDH, StEXP8 and StCAB50 and StCHL1, which is a negative regulator of PTI, supporting previous reports that SERK3/BAK1-dependent BR signaling attenuates plant immunity. We provide Pep-13 as an alternative to chitin as a trigger of SERK3/BAK1-independent immunity.

AB - To prevent disease, pattern recognition receptors (PRRs) are responsible for detecting microbe-associated molecular patterns (MAMPs) to switch on plant innate immunity. SOMATIC EMBROYOGENESIS KINASE 3 (SERK3)/BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) is a well-characterized receptor-like kinase (RLK) that serves as a pivotal co-receptor with PRRs to activate immunity following recognition of MAMPs including flg22, EF-Tu, INF1 and XEG1. However, the requirement for SERK3/BAK1 in many pattern-triggered immune (PTI) signaling pathways is not yet known. Pep-13 is an oomycete MAMP that consists of a highly conserved motif (an oligopeptide of 13 amino acids) shared in Phytophthora transglutaminases. Quantitative RT-PCR analysis reveals that the transcripts of three PTI marker genes (WRKY7, WRKY8 and ACRE31) rapidly accumulate in response to three different MAMPs: flg22, chitin and Pep-13. Whereas silencing of SERK3/BAK1 in Nicotiana benthamiana or potato compromised transcript accumulation in response to flg22, it did not attenuate WRKY7, WRKY8 and ACRE31 up-regulation in response to chitin or Pep-13. This indicates that Pep-13 triggers immunity in a SERK3/BAK1-independent manner, similar to chitin. Surprisingly, silencing of SERK3/BAK1 led to significantly increased accumulation of PTI marker gene transcripts following Pep-13 or chitin treatment, compared to controls. This was accompanied by reduced expression of brassinosteroid (BR) marker genes StSTDH, StEXP8 and StCAB50 and StCHL1, which is a negative regulator of PTI, supporting previous reports that SERK3/BAK1-dependent BR signaling attenuates plant immunity. We provide Pep-13 as an alternative to chitin as a trigger of SERK3/BAK1-independent immunity.

KW - Disease resistance

KW - Flagellin

KW - Late blight

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KW - Transcriptome

KW - Plant Immunity/drug effects

KW - Gene Expression Regulation, Plant/drug effects

KW - RNA, Messenger/genetics

KW - Brassinosteroids/pharmacology

KW - Flagellin/pharmacology

KW - RNA Interference

KW - Alarmins/metabolism

KW - Plant Proteins/genetics

KW - Plants, Genetically Modified

KW - Tobacco/genetics

KW - Peptides/pharmacology

KW - Chitin/pharmacology

KW - Transcription, Genetic/drug effects

KW - Solanum tuberosum/genetics

KW - Phytophthora infestans/drug effects

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