Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33

Meng Xie; Jin Zhang; Tao Yao; Anthony C. Bryan; Yunqiao Pu; Jessy Labbé; Dale A. Pelletier; Nancy Engle; Jennifer L. Morrell-Falvey; Jeremy Schmutz; Arthur J. Ragauskas; Timothy J. Tschaplinski; Feng Chen; Gerald A. Tuskan; Wellington Muchero; Jin Gui Chen

doi:10.1111/nph.16826

Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33

Meng Xie, Jin Zhang, Tao Yao, Anthony C. Bryan, Yunqiao Pu, Jessy Labbé, Dale A. Pelletier, Nancy Engle, Jennifer L. Morrell-Falvey, Jeremy Schmutz, Arthur J. Ragauskas, Timothy J. Tschaplinski, Feng Chen, Gerald A. Tuskan, Wellington Muchero, Jin Gui Chen

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17 Scopus citations

Abstract

The apparent antagonism between salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET) signalling resulting in trade-offs between defence against (hemi)biotrophic and necrotrophic pathogens has been widely described across multiple plant species. However, the underlying mechanism remains to be fully established. The molecular and cellular functions of ANGUSTIFOLIA (AN) were characterised, and its role in regulating the pathogenic response was studied in Arabidopsis. We demonstrated that AN, a plant homologue of mammalian C-TERMINAL BINDING PROTEIN (CtBP), antagonistically regulates plant resistance to the hemibiotrophic pathogen Pseudomonas syringae and the necrotrophic pathogen Botrytis cinerea. Consistent with phenotypic observations, transcription of genes involved in SA and JA/ET pathways was antagonistically regulated by AN. By interacting with another nuclear protein TYROSYL-DNA PHOSPHODIESTERASE1 (TDP1), AN imposes transcriptional repression on MYB46, encoding a transcriptional activator of PHENYLALANINE AMMONIA-LYASE (PAL) genes which are required for SA biosynthesis, while releasing TDP1-imposed transcriptional repression on WRKY33, a master regulator of the JA/ET signalling pathway. These findings demonstrate that transcriptional co-regulation of MYB46 and WRKY33 by AN mediates the coordination of SA and JA/ET pathways to optimise defences against (hemi)biotrophic and necrotrophic pathogens.

Original language	English
Pages (from-to)	1627-1639
Number of pages	13
Journal	New Phytologist
Volume	228
Issue number	5
DOIs	https://doi.org/10.1111/nph.16826
State	Published - Dec 1 2020

Funding

This work was supported by the Plant–Microbe Interfaces Scientific Focus Area, the Center for Bioenergy Innovation, and the BioEnergy Science Center by the Office of Biological and Environmental Research in the US Department of Energy Office of Science. Oak Ridge National Laboratory is managed by UT‐Battelle, LLC, for the United States Department of Energy under contract DE‐AC05‐00OR22725. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE‐AC02‐05CH11231. The authors declare no competing financial interests. This work was supported by the Plant?Microbe Interfaces Scientific Focus Area, the Center for Bioenergy Innovation, and the BioEnergy Science Center by the Office of Biological and Environmental Research in the US Department of Energy Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the United States Department of Energy under contract DE-AC05-00OR22725. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. The authors declare no competing financial interests.

Keywords

(hemi)biotrophic and necrotrophic pathogens
ANGUSTIFOLIA
Arabidopsis
CtBP
SA and JA/ET antagonism
transcriptional reprogramming

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10.1111/nph.16826

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Xie, M., Zhang, J., Yao, T., Bryan, A. C., Pu, Y., Labbé, J., Pelletier, D. A., Engle, N., Morrell-Falvey, J. L., Schmutz, J., Ragauskas, A. J., Tschaplinski, T. J., Chen, F., Tuskan, G. A., Muchero, W., & Chen, J. G. (2020). Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33. New Phytologist, 228(5), 1627-1639. https://doi.org/10.1111/nph.16826

@article{fc29ab21df384f0f918f1c164a32fc90,

title = "Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33",

abstract = "The apparent antagonism between salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET) signalling resulting in trade-offs between defence against (hemi)biotrophic and necrotrophic pathogens has been widely described across multiple plant species. However, the underlying mechanism remains to be fully established. The molecular and cellular functions of ANGUSTIFOLIA (AN) were characterised, and its role in regulating the pathogenic response was studied in Arabidopsis. We demonstrated that AN, a plant homologue of mammalian C-TERMINAL BINDING PROTEIN (CtBP), antagonistically regulates plant resistance to the hemibiotrophic pathogen Pseudomonas syringae and the necrotrophic pathogen Botrytis cinerea. Consistent with phenotypic observations, transcription of genes involved in SA and JA/ET pathways was antagonistically regulated by AN. By interacting with another nuclear protein TYROSYL-DNA PHOSPHODIESTERASE1 (TDP1), AN imposes transcriptional repression on MYB46, encoding a transcriptional activator of PHENYLALANINE AMMONIA-LYASE (PAL) genes which are required for SA biosynthesis, while releasing TDP1-imposed transcriptional repression on WRKY33, a master regulator of the JA/ET signalling pathway. These findings demonstrate that transcriptional co-regulation of MYB46 and WRKY33 by AN mediates the coordination of SA and JA/ET pathways to optimise defences against (hemi)biotrophic and necrotrophic pathogens.",

keywords = "(hemi)biotrophic and necrotrophic pathogens, ANGUSTIFOLIA, Arabidopsis, CtBP, SA and JA/ET antagonism, transcriptional reprogramming",

author = "Meng Xie and Jin Zhang and Tao Yao and Bryan, {Anthony C.} and Yunqiao Pu and Jessy Labb{\'e} and Pelletier, {Dale A.} and Nancy Engle and Morrell-Falvey, {Jennifer L.} and Jeremy Schmutz and Ragauskas, {Arthur J.} and Tschaplinski, {Timothy J.} and Feng Chen and Tuskan, {Gerald A.} and Wellington Muchero and Chen, {Jin Gui}",

note = "Publisher Copyright: 2020 UT-Batelle. New Phytologist {\textcopyright} 2020 New Phytologist Trust",

year = "2020",

month = dec,

day = "1",

doi = "10.1111/nph.16826",

language = "English",

volume = "228",

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Xie, M, Zhang, J, Yao, T, Bryan, AC, Pu, Y, Labbé, J, Pelletier, DA , Engle, N , Morrell-Falvey, JL, Schmutz, J, Ragauskas, AJ, Tschaplinski, TJ, Chen, F, Tuskan, GA, Muchero, W & Chen, JG 2020, 'Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33', New Phytologist, vol. 228, no. 5, pp. 1627-1639. https://doi.org/10.1111/nph.16826

TY - JOUR

T1 - Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33

AU - Xie, Meng

AU - Zhang, Jin

AU - Yao, Tao

AU - Bryan, Anthony C.

AU - Pu, Yunqiao

AU - Labbé, Jessy

AU - Pelletier, Dale A.

AU - Engle, Nancy

AU - Morrell-Falvey, Jennifer L.

AU - Schmutz, Jeremy

AU - Ragauskas, Arthur J.

AU - Tschaplinski, Timothy J.

AU - Chen, Feng

AU - Tuskan, Gerald A.

AU - Muchero, Wellington

AU - Chen, Jin Gui

PY - 2020/12/1

Y1 - 2020/12/1

N2 - The apparent antagonism between salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET) signalling resulting in trade-offs between defence against (hemi)biotrophic and necrotrophic pathogens has been widely described across multiple plant species. However, the underlying mechanism remains to be fully established. The molecular and cellular functions of ANGUSTIFOLIA (AN) were characterised, and its role in regulating the pathogenic response was studied in Arabidopsis. We demonstrated that AN, a plant homologue of mammalian C-TERMINAL BINDING PROTEIN (CtBP), antagonistically regulates plant resistance to the hemibiotrophic pathogen Pseudomonas syringae and the necrotrophic pathogen Botrytis cinerea. Consistent with phenotypic observations, transcription of genes involved in SA and JA/ET pathways was antagonistically regulated by AN. By interacting with another nuclear protein TYROSYL-DNA PHOSPHODIESTERASE1 (TDP1), AN imposes transcriptional repression on MYB46, encoding a transcriptional activator of PHENYLALANINE AMMONIA-LYASE (PAL) genes which are required for SA biosynthesis, while releasing TDP1-imposed transcriptional repression on WRKY33, a master regulator of the JA/ET signalling pathway. These findings demonstrate that transcriptional co-regulation of MYB46 and WRKY33 by AN mediates the coordination of SA and JA/ET pathways to optimise defences against (hemi)biotrophic and necrotrophic pathogens.

AB - The apparent antagonism between salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET) signalling resulting in trade-offs between defence against (hemi)biotrophic and necrotrophic pathogens has been widely described across multiple plant species. However, the underlying mechanism remains to be fully established. The molecular and cellular functions of ANGUSTIFOLIA (AN) were characterised, and its role in regulating the pathogenic response was studied in Arabidopsis. We demonstrated that AN, a plant homologue of mammalian C-TERMINAL BINDING PROTEIN (CtBP), antagonistically regulates plant resistance to the hemibiotrophic pathogen Pseudomonas syringae and the necrotrophic pathogen Botrytis cinerea. Consistent with phenotypic observations, transcription of genes involved in SA and JA/ET pathways was antagonistically regulated by AN. By interacting with another nuclear protein TYROSYL-DNA PHOSPHODIESTERASE1 (TDP1), AN imposes transcriptional repression on MYB46, encoding a transcriptional activator of PHENYLALANINE AMMONIA-LYASE (PAL) genes which are required for SA biosynthesis, while releasing TDP1-imposed transcriptional repression on WRKY33, a master regulator of the JA/ET signalling pathway. These findings demonstrate that transcriptional co-regulation of MYB46 and WRKY33 by AN mediates the coordination of SA and JA/ET pathways to optimise defences against (hemi)biotrophic and necrotrophic pathogens.

KW - (hemi)biotrophic and necrotrophic pathogens

KW - ANGUSTIFOLIA

KW - Arabidopsis

KW - CtBP

KW - SA and JA/ET antagonism

KW - transcriptional reprogramming

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M3 - Article

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AN - SCOPUS:85089555093

SN - 0028-646X

VL - 228

SP - 1627

EP - 1639

JO - New Phytologist

JF - New Phytologist

IS - 5

ER -

Arabidopsis C-terminal binding protein ANGUSTIFOLIA modulates transcriptional co-regulation of MYB46 and WRKY33

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