A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae

Barbara Franco-Orozco, Adokiye Berepiki, Olaya Ruiz, Louise Gamble, Lucie L. Griffe, Shumei Wang, Paul R. J. Birch, Kostya Kanyuka, Anna Avrova (Lead / Corresponding author)

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Pathogen-associated molecular patterns (PAMPs) are detected by plant pattern recognition receptors (PRRs), which gives rise to PAMP-triggered immunity (PTI). We characterized a novel fungal PAMP, Cell Death Inducing 1 (RcCDI1), identified in the Rhynchosporium commune transcriptome sampled at an early stage of barley (Hordeum vulgare) infection. The ability of RcCDI1 and its homologues from different fungal species to induce cell death in Nicotiana benthamiana was tested following agroinfiltration or infiltration of recombinant proteins produced by Pichia pastoris. Virus-induced gene silencing (VIGS) and transient expression of Phytophthora infestans effectors PiAVR3a and PexRD2 were used to assess the involvement of known components of PTI in N. benthamiana responses to RcCDI1. RcCDI1 was highly upregulated early during barley colonization with R. commune. RcCDI1 and its homologues from different fungal species, including Zymoseptoria tritici, Magnaporthe oryzae and Neurospora crassa, exhibited PAMP activity, inducing cell death in Solanaceae but not in other families of dicots or monocots. RcCDI1-triggered cell death was shown to require N. benthamiana Brassinosteroid insensitive 1-Associated Kinase 1 (NbBAK1), N. benthamiana suppressor of BIR1-1 (NbSOBIR1) and N. benthamiana SGT1 (NbSGT1), but was not suppressed by PiAVR3a or PexRD2. We report the identification of a novel Ascomycete PAMP, RcCDI1, recognized by Solanaceae but not by monocots, which activates cell death through a pathway that is distinct from that triggered by the oomycete PAMP INF1.

Original languageEnglish
Pages (from-to)1657-1672
Number of pages16
JournalNew Phytologist
Volume214
Issue number4
Early online date7 Apr 2017
DOIs
Publication statusPublished - Jun 2017

Fingerprint

Solanaceae
Ascomycota
Nicotiana benthamiana
cell death
Fungi
Cell Death
fungi
pathogens
Hordeum
Liliopsida
Rhynchosporium
immunity
barley
agroinfiltration
Immunity
Mycosphaerella graminicola
Brassinosteroids
Phytophthora infestans
Magnaporthe oryzae
Magnaporthe

Keywords

  • Journal article
  • Ascomycete
  • Cell death
  • Elicitor
  • Fungal
  • Pathogen
  • Pathogen-associated molecular pattern (PAMP)
  • Rhynchosporium commune
  • Solanaceae

Cite this

Franco-Orozco, B., Berepiki, A., Ruiz, O., Gamble, L., Griffe, L. L., Wang, S., ... Avrova, A. (2017). A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. New Phytologist, 214(4), 1657-1672. https://doi.org/10.1111/nph.14542
Franco-Orozco, Barbara ; Berepiki, Adokiye ; Ruiz, Olaya ; Gamble, Louise ; Griffe, Lucie L. ; Wang, Shumei ; Birch, Paul R. J. ; Kanyuka, Kostya ; Avrova, Anna. / A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. In: New Phytologist. 2017 ; Vol. 214, No. 4. pp. 1657-1672.
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abstract = "Pathogen-associated molecular patterns (PAMPs) are detected by plant pattern recognition receptors (PRRs), which gives rise to PAMP-triggered immunity (PTI). We characterized a novel fungal PAMP, Cell Death Inducing 1 (RcCDI1), identified in the Rhynchosporium commune transcriptome sampled at an early stage of barley (Hordeum vulgare) infection. The ability of RcCDI1 and its homologues from different fungal species to induce cell death in Nicotiana benthamiana was tested following agroinfiltration or infiltration of recombinant proteins produced by Pichia pastoris. Virus-induced gene silencing (VIGS) and transient expression of Phytophthora infestans effectors PiAVR3a and PexRD2 were used to assess the involvement of known components of PTI in N. benthamiana responses to RcCDI1. RcCDI1 was highly upregulated early during barley colonization with R. commune. RcCDI1 and its homologues from different fungal species, including Zymoseptoria tritici, Magnaporthe oryzae and Neurospora crassa, exhibited PAMP activity, inducing cell death in Solanaceae but not in other families of dicots or monocots. RcCDI1-triggered cell death was shown to require N. benthamiana Brassinosteroid insensitive 1-Associated Kinase 1 (NbBAK1), N. benthamiana suppressor of BIR1-1 (NbSOBIR1) and N. benthamiana SGT1 (NbSGT1), but was not suppressed by PiAVR3a or PexRD2. We report the identification of a novel Ascomycete PAMP, RcCDI1, recognized by Solanaceae but not by monocots, which activates cell death through a pathway that is distinct from that triggered by the oomycete PAMP INF1.",
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author = "Barbara Franco-Orozco and Adokiye Berepiki and Olaya Ruiz and Louise Gamble and Griffe, {Lucie L.} and Shumei Wang and Birch, {Paul R. J.} and Kostya Kanyuka and Anna Avrova",
note = "We are grateful to the Biotechnology and Biological Sciences Research Coun cil (BBSRC) Crop Improvement Research Club, UK for funding (BB/J019569/1) this work. B.F-O. was funded by Programa Doctoral Becas COLCIENCIAS, Colombia. A.A. was also supported by the Scottish Government Rural and Environment Science and Analytical Services. K.K. was also supported by the BBSRC Institute Strategic Programme Grant ‘20:20Wheat{\circledR}’ (BB/J/00426X/1).",
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Franco-Orozco, B, Berepiki, A, Ruiz, O, Gamble, L, Griffe, LL, Wang, S, Birch, PRJ, Kanyuka, K & Avrova, A 2017, 'A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae', New Phytologist, vol. 214, no. 4, pp. 1657-1672. https://doi.org/10.1111/nph.14542

A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. / Franco-Orozco, Barbara; Berepiki, Adokiye; Ruiz, Olaya; Gamble, Louise; Griffe, Lucie L.; Wang, Shumei; Birch, Paul R. J.; Kanyuka, Kostya; Avrova, Anna (Lead / Corresponding author).

In: New Phytologist, Vol. 214, No. 4, 06.2017, p. 1657-1672.

Research output: Contribution to journalArticle

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T1 - A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae

AU - Franco-Orozco, Barbara

AU - Berepiki, Adokiye

AU - Ruiz, Olaya

AU - Gamble, Louise

AU - Griffe, Lucie L.

AU - Wang, Shumei

AU - Birch, Paul R. J.

AU - Kanyuka, Kostya

AU - Avrova, Anna

N1 - We are grateful to the Biotechnology and Biological Sciences Research Coun cil (BBSRC) Crop Improvement Research Club, UK for funding (BB/J019569/1) this work. B.F-O. was funded by Programa Doctoral Becas COLCIENCIAS, Colombia. A.A. was also supported by the Scottish Government Rural and Environment Science and Analytical Services. K.K. was also supported by the BBSRC Institute Strategic Programme Grant ‘20:20Wheat®’ (BB/J/00426X/1).

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N2 - Pathogen-associated molecular patterns (PAMPs) are detected by plant pattern recognition receptors (PRRs), which gives rise to PAMP-triggered immunity (PTI). We characterized a novel fungal PAMP, Cell Death Inducing 1 (RcCDI1), identified in the Rhynchosporium commune transcriptome sampled at an early stage of barley (Hordeum vulgare) infection. The ability of RcCDI1 and its homologues from different fungal species to induce cell death in Nicotiana benthamiana was tested following agroinfiltration or infiltration of recombinant proteins produced by Pichia pastoris. Virus-induced gene silencing (VIGS) and transient expression of Phytophthora infestans effectors PiAVR3a and PexRD2 were used to assess the involvement of known components of PTI in N. benthamiana responses to RcCDI1. RcCDI1 was highly upregulated early during barley colonization with R. commune. RcCDI1 and its homologues from different fungal species, including Zymoseptoria tritici, Magnaporthe oryzae and Neurospora crassa, exhibited PAMP activity, inducing cell death in Solanaceae but not in other families of dicots or monocots. RcCDI1-triggered cell death was shown to require N. benthamiana Brassinosteroid insensitive 1-Associated Kinase 1 (NbBAK1), N. benthamiana suppressor of BIR1-1 (NbSOBIR1) and N. benthamiana SGT1 (NbSGT1), but was not suppressed by PiAVR3a or PexRD2. We report the identification of a novel Ascomycete PAMP, RcCDI1, recognized by Solanaceae but not by monocots, which activates cell death through a pathway that is distinct from that triggered by the oomycete PAMP INF1.

AB - Pathogen-associated molecular patterns (PAMPs) are detected by plant pattern recognition receptors (PRRs), which gives rise to PAMP-triggered immunity (PTI). We characterized a novel fungal PAMP, Cell Death Inducing 1 (RcCDI1), identified in the Rhynchosporium commune transcriptome sampled at an early stage of barley (Hordeum vulgare) infection. The ability of RcCDI1 and its homologues from different fungal species to induce cell death in Nicotiana benthamiana was tested following agroinfiltration or infiltration of recombinant proteins produced by Pichia pastoris. Virus-induced gene silencing (VIGS) and transient expression of Phytophthora infestans effectors PiAVR3a and PexRD2 were used to assess the involvement of known components of PTI in N. benthamiana responses to RcCDI1. RcCDI1 was highly upregulated early during barley colonization with R. commune. RcCDI1 and its homologues from different fungal species, including Zymoseptoria tritici, Magnaporthe oryzae and Neurospora crassa, exhibited PAMP activity, inducing cell death in Solanaceae but not in other families of dicots or monocots. RcCDI1-triggered cell death was shown to require N. benthamiana Brassinosteroid insensitive 1-Associated Kinase 1 (NbBAK1), N. benthamiana suppressor of BIR1-1 (NbSOBIR1) and N. benthamiana SGT1 (NbSGT1), but was not suppressed by PiAVR3a or PexRD2. We report the identification of a novel Ascomycete PAMP, RcCDI1, recognized by Solanaceae but not by monocots, which activates cell death through a pathway that is distinct from that triggered by the oomycete PAMP INF1.

KW - Journal article

KW - Ascomycete

KW - Cell death

KW - Elicitor

KW - Fungal

KW - Pathogen

KW - Pathogen-associated molecular pattern (PAMP)

KW - Rhynchosporium commune

KW - Solanaceae

U2 - 10.1111/nph.14542

DO - 10.1111/nph.14542

M3 - Article

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JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

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