Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors

Pingtao Ding; Toshiyuki Sakai; Ram Krishna Shrestha; Nicolas Manosalva Perez; Wenbin Guo; Bruno Pok Man Ngou; Shengbo He; Chang Liu; Xiaoqi Feng; Runxuan Zhang; Klaas Vandepoele; Dan MacLean; Jonathan D. G. Jones

doi:10.1093/jxb/erab373

Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors

Pingtao Ding (Lead / Corresponding author)
, Toshiyuki Sakai
, Ram Krishna Shrestha
, Nicolas Manosalva Perez
, Wenbin Guo
, Bruno Pok Man Ngou
, Shengbo He
, Chang Liu
, Xiaoqi Feng
, Runxuan Zhang
, Klaas Vandepoele
, Dan MacLean
, Jonathan D. G. Jones (Lead / Corresponding author)

DArcy Thompson Unit

Research output: Contribution to journal › Article › peer-review

22 Citations (Scopus)

128 Downloads (Pure)

Abstract

Activation of cell-surface and intracellular receptor-mediated immunity results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which co-activation of both immune systems lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromatin accessibility. Activation of cell-surface or intracellular receptor-mediated immunity, or both, increases chromatin accessibility at induced defense genes. Analysis of ATAC-seq and RNA-seq data combined with publicly available information on transcription factor DNA-binding motifs enabled comparison of individual gene regulatory networks activated by cell-surface or intracellular receptor-mediated immunity, and by both. These results and analyses reveal overlapping and conserved transcriptional regulatory mechanisms between the two immune systems.

Original language	English
Pages (from-to)	7927-7941
Number of pages	15
Journal	Journal of Experimental Botany
Volume	72
Issue number	22
Early online date	13 Aug 2021
DOIs	https://doi.org/10.1093/jxb/erab373
Publication status	Published - 4 Dec 2021

Keywords

ATAC-seq and RNA-seq
cell surface immune receptors
chromatin accessibility
gene regulatory network
intracellular immune receptors
plant innate immunity
PRR and NLR
transcriptional regulation

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10.1093/jxb/erab373

Accepted Author ManuscriptAccepted author manuscript, 3.13 MB

Aref#d: 21408. In Silico Prediction of Pharmacology (Industrial CASE Studentship : Ian Carruthers)
Hopkins, A. (Investigator)
Project: Research

Cite this

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title = "Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors",

abstract = "Activation of cell-surface and intracellular receptor-mediated immunity results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which co-activation of both immune systems lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromatin accessibility. Activation of cell-surface or intracellular receptor-mediated immunity, or both, increases chromatin accessibility at induced defense genes. Analysis of ATAC-seq and RNA-seq data combined with publicly available information on transcription factor DNA-binding motifs enabled comparison of individual gene regulatory networks activated by cell-surface or intracellular receptor-mediated immunity, and by both. These results and analyses reveal overlapping and conserved transcriptional regulatory mechanisms between the two immune systems.",

keywords = "ATAC-seq and RNA-seq, cell surface immune receptors, chromatin accessibility, gene regulatory network, intracellular immune receptors, plant innate immunity, PRR and NLR, transcriptional regulation",

author = "Pingtao Ding and Toshiyuki Sakai and Shrestha, \{Ram Krishna\} and Perez, \{Nicolas Manosalva\} and Wenbin Guo and Ngou, \{Bruno Pok Man\} and Shengbo He and Chang Liu and Xiaoqi Feng and Runxuan Zhang and Klaas Vandepoele and Dan MacLean and Jones, \{Jonathan D. G.\}",

note = "We thank the Gatsby Foundation (United Kingdom) for funding to the JDGJ laboratory. PD acknowledges support from the European Union{\textquoteright}s Horizon 2020 Research and Innovation Program under Marie Sk{\l}odowska-Curie Actions (grant agreement: 656243) and a Future Leader Fellowship from the Biotechnology and Biological Sciences Research Council (BBSRC) (grant agreement: BB/R012172/1). TS, RKS, DM and JDGJ were supported by the Gatsby Foundation funding to the Sainsbury Laboratory. NMP and KV were supported by a BOF grant from Ghent University (grant agreement: BOF24Y2019001901). WG and RZ were supported by Scottish Government Rural and Environment Science and Analytical Services division (RESAS), and RZ also acknowledge the support from a BBSRC Bioinformatics and Biological Resources Fund (grant agreement: BB/S020160/1). BN was supported by the Norwich Research Park (NRP) Biosciences Doctoral Training Partnership (DTP) funded by BBSRC (grant agreement: BB/M011216/1). SH and XF were supported by a BBSRC Responsive Mode grant (grant agreement: BB/S009620/1) and a European Research Council Starting grant {\textquoteleft}SexMeth{\textquoteright} (grant agreement: 804981). CL was supported by Deutsche Forschungsgemeinschaft (grant agreement: LI 2862/4) {\textcopyright} The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: [email protected].",

year = "2021",

month = dec,

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doi = "10.1093/jxb/erab373",

language = "English",

volume = "72",

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journal = "Journal of Experimental Botany",

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T1 - Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors

AU - Ding, Pingtao

AU - Sakai, Toshiyuki

AU - Shrestha, Ram Krishna

AU - Perez, Nicolas Manosalva

AU - Guo, Wenbin

AU - Ngou, Bruno Pok Man

AU - He, Shengbo

AU - Liu, Chang

AU - Feng, Xiaoqi

AU - Zhang, Runxuan

AU - Vandepoele, Klaas

AU - MacLean, Dan

AU - Jones, Jonathan D. G.

N1 - We thank the Gatsby Foundation (United Kingdom) for funding to the JDGJ laboratory. PD acknowledges support from the European Union’s Horizon 2020 Research and Innovation Program under Marie Skłodowska-Curie Actions (grant agreement: 656243) and a Future Leader Fellowship from the Biotechnology and Biological Sciences Research Council (BBSRC) (grant agreement: BB/R012172/1). TS, RKS, DM and JDGJ were supported by the Gatsby Foundation funding to the Sainsbury Laboratory. NMP and KV were supported by a BOF grant from Ghent University (grant agreement: BOF24Y2019001901). WG and RZ were supported by Scottish Government Rural and Environment Science and Analytical Services division (RESAS), and RZ also acknowledge the support from a BBSRC Bioinformatics and Biological Resources Fund (grant agreement: BB/S020160/1). BN was supported by the Norwich Research Park (NRP) Biosciences Doctoral Training Partnership (DTP) funded by BBSRC (grant agreement: BB/M011216/1). SH and XF were supported by a BBSRC Responsive Mode grant (grant agreement: BB/S009620/1) and a European Research Council Starting grant ‘SexMeth’ (grant agreement: 804981). CL was supported by Deutsche Forschungsgemeinschaft (grant agreement: LI 2862/4) © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: [email protected].

PY - 2021/12/4

Y1 - 2021/12/4

N2 - Activation of cell-surface and intracellular receptor-mediated immunity results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which co-activation of both immune systems lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromatin accessibility. Activation of cell-surface or intracellular receptor-mediated immunity, or both, increases chromatin accessibility at induced defense genes. Analysis of ATAC-seq and RNA-seq data combined with publicly available information on transcription factor DNA-binding motifs enabled comparison of individual gene regulatory networks activated by cell-surface or intracellular receptor-mediated immunity, and by both. These results and analyses reveal overlapping and conserved transcriptional regulatory mechanisms between the two immune systems.

AB - Activation of cell-surface and intracellular receptor-mediated immunity results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which co-activation of both immune systems lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromatin accessibility. Activation of cell-surface or intracellular receptor-mediated immunity, or both, increases chromatin accessibility at induced defense genes. Analysis of ATAC-seq and RNA-seq data combined with publicly available information on transcription factor DNA-binding motifs enabled comparison of individual gene regulatory networks activated by cell-surface or intracellular receptor-mediated immunity, and by both. These results and analyses reveal overlapping and conserved transcriptional regulatory mechanisms between the two immune systems.

KW - ATAC-seq and RNA-seq

KW - cell surface immune receptors

KW - chromatin accessibility

KW - gene regulatory network

KW - intracellular immune receptors

KW - plant innate immunity

KW - PRR and NLR

KW - transcriptional regulation

U2 - 10.1093/jxb/erab373

DO - 10.1093/jxb/erab373

M3 - Article

C2 - 34387350

SN - 0022-0957

VL - 72

SP - 7927

EP - 7941

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

IS - 22

ER -

Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors

Abstract

Keywords

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Projects

Aref#d: 21408. In Silico Prediction of Pharmacology (Industrial CASE Studentship : Ian Carruthers)

Cite this