Linker histone H1 modulates defense priming and immunity in plants

Arsheed H. Sheikh; Kashif Nawaz; Naheed Tabassum; Marilia Almeida-Trapp; Kiruthiga G. Mariappan; Hanna Alhoraibi; Naganand Rayapuram; Manuel Aranda; Martin Groth; Heribert Hirt

doi:10.1093/nar/gkad106

Linker histone H1 modulates defense priming and immunity in plants

Arsheed H. Sheikh^*, Kashif Nawaz, Naheed Tabassum, Marilia Almeida-Trapp, Kiruthiga G. Mariappan, Hanna Alhoraibi, Naganand Rayapuram, Manuel Aranda, Martin Groth, Heribert Hirt

^*Corresponding author for this work

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

11 Scopus citations

Abstract

Linker H1 histones play an important role in animal and human pathogenesis, but their function in plant immunity is poorly understood. Here, we analyzed mutants of the three canonical variants of Arabidopsis H1 histones, namely H1.1, H1.2 and H1.3. We observed that double h1.1h1.2 and triple h1.1h1.2h1.3 (3h1) mutants were resistant to Pseudomonas syringae and Botrytis cinerea infections. Transcriptome analysis of 3h1 mutant plants showed H1s play a key role in regulating the expression of early and late defense genes upon pathogen challenge. Moreover, 3h1 mutant plants showed enhanced production of reactive oxygen species and activation of mitogen activated protein kinases upon pathogen-Associated molecular pattern (PAMP) treatment. However, 3h1 mutant plants were insensitive to priming with flg22, a well-known bacterial PAMP which induces enhanced resistance in WT plants. The defective defense response in 3h1 upon priming was correlated with altered DNA methylation and reduced global H3K56ac levels. Our data place H1 as a molecular gatekeeper in governing dynamic changes in the chromatin landscape of defense genes during plant pathogen interaction.

Original language	English (US)
Pages (from-to)	4252-4265
Number of pages	14
Journal	NUCLEIC ACIDS RESEARCH
Volume	51
Issue number	9
DOIs	https://doi.org/10.1093/nar/gkad106
State	Published - May 22 2023

Bibliographical note

Funding Information:
King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.]. Funding for open access charge: King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.].

Publisher Copyright:
© 2023 The Author(s). Published by Oxford University Press on behalf of Nucleic Acids Research.

ASJC Scopus subject areas

Genetics

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10.1093/nar/gkad106

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title = "Linker histone H1 modulates defense priming and immunity in plants",

abstract = "Linker H1 histones play an important role in animal and human pathogenesis, but their function in plant immunity is poorly understood. Here, we analyzed mutants of the three canonical variants of Arabidopsis H1 histones, namely H1.1, H1.2 and H1.3. We observed that double h1.1h1.2 and triple h1.1h1.2h1.3 (3h1) mutants were resistant to Pseudomonas syringae and Botrytis cinerea infections. Transcriptome analysis of 3h1 mutant plants showed H1s play a key role in regulating the expression of early and late defense genes upon pathogen challenge. Moreover, 3h1 mutant plants showed enhanced production of reactive oxygen species and activation of mitogen activated protein kinases upon pathogen-Associated molecular pattern (PAMP) treatment. However, 3h1 mutant plants were insensitive to priming with flg22, a well-known bacterial PAMP which induces enhanced resistance in WT plants. The defective defense response in 3h1 upon priming was correlated with altered DNA methylation and reduced global H3K56ac levels. Our data place H1 as a molecular gatekeeper in governing dynamic changes in the chromatin landscape of defense genes during plant pathogen interaction.",

author = "Sheikh, {Arsheed H.} and Kashif Nawaz and Naheed Tabassum and Marilia Almeida-Trapp and Mariappan, {Kiruthiga G.} and Hanna Alhoraibi and Naganand Rayapuram and Manuel Aranda and Martin Groth and Heribert Hirt",

note = "Funding Information: King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.]. Funding for open access charge: King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.]. Publisher Copyright: {\textcopyright} 2023 The Author(s). Published by Oxford University Press on behalf of Nucleic Acids Research.",

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AU - Sheikh, Arsheed H.

AU - Nawaz, Kashif

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AU - Almeida-Trapp, Marilia

AU - Mariappan, Kiruthiga G.

AU - Alhoraibi, Hanna

AU - Rayapuram, Naganand

AU - Aranda, Manuel

AU - Groth, Martin

AU - Hirt, Heribert

N1 - Funding Information: King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.]. Funding for open access charge: King Abdullah University of Science and Technology (KAUST) [BAS/1/1062-01-01 to H.H.]. Publisher Copyright: © 2023 The Author(s). Published by Oxford University Press on behalf of Nucleic Acids Research.

PY - 2023/5/22

Y1 - 2023/5/22

N2 - Linker H1 histones play an important role in animal and human pathogenesis, but their function in plant immunity is poorly understood. Here, we analyzed mutants of the three canonical variants of Arabidopsis H1 histones, namely H1.1, H1.2 and H1.3. We observed that double h1.1h1.2 and triple h1.1h1.2h1.3 (3h1) mutants were resistant to Pseudomonas syringae and Botrytis cinerea infections. Transcriptome analysis of 3h1 mutant plants showed H1s play a key role in regulating the expression of early and late defense genes upon pathogen challenge. Moreover, 3h1 mutant plants showed enhanced production of reactive oxygen species and activation of mitogen activated protein kinases upon pathogen-Associated molecular pattern (PAMP) treatment. However, 3h1 mutant plants were insensitive to priming with flg22, a well-known bacterial PAMP which induces enhanced resistance in WT plants. The defective defense response in 3h1 upon priming was correlated with altered DNA methylation and reduced global H3K56ac levels. Our data place H1 as a molecular gatekeeper in governing dynamic changes in the chromatin landscape of defense genes during plant pathogen interaction.

AB - Linker H1 histones play an important role in animal and human pathogenesis, but their function in plant immunity is poorly understood. Here, we analyzed mutants of the three canonical variants of Arabidopsis H1 histones, namely H1.1, H1.2 and H1.3. We observed that double h1.1h1.2 and triple h1.1h1.2h1.3 (3h1) mutants were resistant to Pseudomonas syringae and Botrytis cinerea infections. Transcriptome analysis of 3h1 mutant plants showed H1s play a key role in regulating the expression of early and late defense genes upon pathogen challenge. Moreover, 3h1 mutant plants showed enhanced production of reactive oxygen species and activation of mitogen activated protein kinases upon pathogen-Associated molecular pattern (PAMP) treatment. However, 3h1 mutant plants were insensitive to priming with flg22, a well-known bacterial PAMP which induces enhanced resistance in WT plants. The defective defense response in 3h1 upon priming was correlated with altered DNA methylation and reduced global H3K56ac levels. Our data place H1 as a molecular gatekeeper in governing dynamic changes in the chromatin landscape of defense genes during plant pathogen interaction.

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Linker histone H1 modulates defense priming and immunity in plants

Abstract

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