Phytophthora infestans effector SFI3 targets potato UBK to suppress early immune transcriptional responses

Qin He, Hazel McLellan, Richard K. Hughes, Petra C. Boevink, Miles Armstrong, Yuan Lu, Mark J. Banfield, Zhendong Tian (Lead / Corresponding author), Paul R. J. Birch (Lead / Corresponding author)

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Abstract

The potato blight agent Phytophthora infestans secretes a range of RXLR effectors to promote disease. Recent evidence indicates that some effectors suppress early pattern‐triggered immunity (PTI) following perception of Microbe‐Associated Molecular Patterns (MAMPs). Phytophthora infestans effector PiSFI3/Pi06087/PexRD16 was previously shown to suppress MAMP‐triggered pFRK1‐Luciferase reporter gene activity. How PiSFI3 suppresses immunity is unknown.

We employed yeast‐two‐hybrid (Y2H) assays, co‐immunoprecipitation, transcriptional silencing by RNA interference and virus‐induced gene silencing (VIGS), and X‐ray crystallography for structure‐guided mutagenesis, to investigate the function of PiSFI3 in targeting a plant U‐Box‐kinase protein (StUBK) to suppress immunity.

We discovered that PiSFI3 is active in the host nucleus and interacts in yeast and in planta with StUBK. UBK is a positive regulator of specific PTI pathways in both potato and Nicotiana benthamiana. Importantly, it contributes to early transcriptional responses that are suppressed by PiSFI3. PiSFI3 forms an unusual trans‐homodimer. Mutation to disrupt dimerization prevents nucleolar localisation of PiSFI3 and attenuates both its interaction with StUBK and its ability to enhance P. infestans leaf colonisation.

PiSFI3 is a ‘WY domain’ RXLR effector that forms a novel trans‐homodimer which is required for its ability to suppress PTI via interaction with the U‐Box‐kinase protein StUBK.
Original languageEnglish
Number of pages18
JournalNew Phytologist
Early online date10 Dec 2018
DOIs
Publication statusE-pub ahead of print - 10 Dec 2018

Fingerprint

Phytophthora infestans
Solanum tuberosum
Immunity
immunity
potatoes
Aptitude
crystallography
Plant Proteins
dimerization
Nicotiana benthamiana
X Ray Crystallography
Dimerization
Gene Silencing
gene silencing
plant proteins
RNA Interference
Plantae
RNA interference
Reporter Genes
blight

Keywords

  • potato late blight
  • pathogenicity
  • virulence
  • disease resistance
  • effector-triggered susceptibility

Cite this

He, Qin ; McLellan, Hazel ; Hughes, Richard K. ; Boevink, Petra C. ; Armstrong, Miles ; Lu, Yuan ; Banfield, Mark J. ; Tian, Zhendong ; Birch, Paul R. J. / Phytophthora infestans effector SFI3 targets potato UBK to suppress early immune transcriptional responses. In: New Phytologist. 2018.
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abstract = "The potato blight agent Phytophthora infestans secretes a range of RXLR effectors to promote disease. Recent evidence indicates that some effectors suppress early pattern‐triggered immunity (PTI) following perception of Microbe‐Associated Molecular Patterns (MAMPs). Phytophthora infestans effector PiSFI3/Pi06087/PexRD16 was previously shown to suppress MAMP‐triggered pFRK1‐Luciferase reporter gene activity. How PiSFI3 suppresses immunity is unknown.We employed yeast‐two‐hybrid (Y2H) assays, co‐immunoprecipitation, transcriptional silencing by RNA interference and virus‐induced gene silencing (VIGS), and X‐ray crystallography for structure‐guided mutagenesis, to investigate the function of PiSFI3 in targeting a plant U‐Box‐kinase protein (StUBK) to suppress immunity.We discovered that PiSFI3 is active in the host nucleus and interacts in yeast and in planta with StUBK. UBK is a positive regulator of specific PTI pathways in both potato and Nicotiana benthamiana. Importantly, it contributes to early transcriptional responses that are suppressed by PiSFI3. PiSFI3 forms an unusual trans‐homodimer. Mutation to disrupt dimerization prevents nucleolar localisation of PiSFI3 and attenuates both its interaction with StUBK and its ability to enhance P. infestans leaf colonisation.PiSFI3 is a ‘WY domain’ RXLR effector that forms a novel trans‐homodimer which is required for its ability to suppress PTI via interaction with the U‐Box‐kinase protein StUBK.",
keywords = "potato late blight, pathogenicity, virulence, disease resistance, effector-triggered susceptibility",
author = "Qin He and Hazel McLellan and Hughes, {Richard K.} and Boevink, {Petra C.} and Miles Armstrong and Yuan Lu and Banfield, {Mark J.} and Zhendong Tian and Birch, {Paul R. J.}",
note = "Funding: We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1, BB/P020569/1), the Scottish Government Rural and Environment Science and Analytical Services Division (RESAS), and the National Natural Science Foundation of China (grants 31171603, 31471550), the National High Technology Research and Development Program of China (grants 2013AA102603), and the Fundamental Research Funds for the Central Universities of China (grants, 2662017PY069).",
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Phytophthora infestans effector SFI3 targets potato UBK to suppress early immune transcriptional responses. / He, Qin; McLellan, Hazel; Hughes, Richard K.; Boevink, Petra C.; Armstrong, Miles; Lu, Yuan; Banfield, Mark J.; Tian, Zhendong (Lead / Corresponding author); Birch, Paul R. J. (Lead / Corresponding author).

In: New Phytologist, 10.12.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Phytophthora infestans effector SFI3 targets potato UBK to suppress early immune transcriptional responses

AU - He, Qin

AU - McLellan, Hazel

AU - Hughes, Richard K.

AU - Boevink, Petra C.

AU - Armstrong, Miles

AU - Lu, Yuan

AU - Banfield, Mark J.

AU - Tian, Zhendong

AU - Birch, Paul R. J.

N1 - Funding: We are grateful for financial support from the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/G015244/1, BB/K018183/1, BB/L026880/1, BB/P020569/1), the Scottish Government Rural and Environment Science and Analytical Services Division (RESAS), and the National Natural Science Foundation of China (grants 31171603, 31471550), the National High Technology Research and Development Program of China (grants 2013AA102603), and the Fundamental Research Funds for the Central Universities of China (grants, 2662017PY069).

PY - 2018/12/10

Y1 - 2018/12/10

N2 - The potato blight agent Phytophthora infestans secretes a range of RXLR effectors to promote disease. Recent evidence indicates that some effectors suppress early pattern‐triggered immunity (PTI) following perception of Microbe‐Associated Molecular Patterns (MAMPs). Phytophthora infestans effector PiSFI3/Pi06087/PexRD16 was previously shown to suppress MAMP‐triggered pFRK1‐Luciferase reporter gene activity. How PiSFI3 suppresses immunity is unknown.We employed yeast‐two‐hybrid (Y2H) assays, co‐immunoprecipitation, transcriptional silencing by RNA interference and virus‐induced gene silencing (VIGS), and X‐ray crystallography for structure‐guided mutagenesis, to investigate the function of PiSFI3 in targeting a plant U‐Box‐kinase protein (StUBK) to suppress immunity.We discovered that PiSFI3 is active in the host nucleus and interacts in yeast and in planta with StUBK. UBK is a positive regulator of specific PTI pathways in both potato and Nicotiana benthamiana. Importantly, it contributes to early transcriptional responses that are suppressed by PiSFI3. PiSFI3 forms an unusual trans‐homodimer. Mutation to disrupt dimerization prevents nucleolar localisation of PiSFI3 and attenuates both its interaction with StUBK and its ability to enhance P. infestans leaf colonisation.PiSFI3 is a ‘WY domain’ RXLR effector that forms a novel trans‐homodimer which is required for its ability to suppress PTI via interaction with the U‐Box‐kinase protein StUBK.

AB - The potato blight agent Phytophthora infestans secretes a range of RXLR effectors to promote disease. Recent evidence indicates that some effectors suppress early pattern‐triggered immunity (PTI) following perception of Microbe‐Associated Molecular Patterns (MAMPs). Phytophthora infestans effector PiSFI3/Pi06087/PexRD16 was previously shown to suppress MAMP‐triggered pFRK1‐Luciferase reporter gene activity. How PiSFI3 suppresses immunity is unknown.We employed yeast‐two‐hybrid (Y2H) assays, co‐immunoprecipitation, transcriptional silencing by RNA interference and virus‐induced gene silencing (VIGS), and X‐ray crystallography for structure‐guided mutagenesis, to investigate the function of PiSFI3 in targeting a plant U‐Box‐kinase protein (StUBK) to suppress immunity.We discovered that PiSFI3 is active in the host nucleus and interacts in yeast and in planta with StUBK. UBK is a positive regulator of specific PTI pathways in both potato and Nicotiana benthamiana. Importantly, it contributes to early transcriptional responses that are suppressed by PiSFI3. PiSFI3 forms an unusual trans‐homodimer. Mutation to disrupt dimerization prevents nucleolar localisation of PiSFI3 and attenuates both its interaction with StUBK and its ability to enhance P. infestans leaf colonisation.PiSFI3 is a ‘WY domain’ RXLR effector that forms a novel trans‐homodimer which is required for its ability to suppress PTI via interaction with the U‐Box‐kinase protein StUBK.

KW - potato late blight

KW - pathogenicity

KW - virulence

KW - disease resistance

KW - effector-triggered susceptibility

U2 - 10.1111/nph.15635

DO - 10.1111/nph.15635

M3 - Article

C2 - 30536576

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

ER -