Gene expression evolution in pattern-triggered immunity within<i>Arabidopsis thaliana</i>and across Brassicaceae species

Winkelmüller, Thomas M.; Entila, Frederickson; Anver, Shajahan; Piasecka, Anna; Song, Baoxing; Dahms, Eik; Sakakibara, Hitoshi; Gan, Xiangchao; Kułak, Karolina; Sawikowska, Aneta; Krajewski, Paweł; Tsiantis, Miltos; Garrido‐Oter, Ruben; Fukushima, Kenji; Schulze‐Lefert, Paul; Laurent, Stefan; Bednarek, Paweł; Tsuda, Kazuhiko

doi:10.1101/2020.07.29.227397

Cited by 4 publications

(3 citation statements)

References 107 publications

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“…S3A and Dataset S3) (27), modulation of this sector of the plant immune system is likely to be a common strategy employed by root commensals. Cluster SC1 also overlaps significantly (84 of 281 genes; P = 3.27E-58) (Dataset S3) with a set of 868 genes that are flg22-regulated across four Brassicaceae species (28), indicating that SynCom35 has the potential to modulate an evolutionarily conserved sector of MTI. Although defense-related genes were not activated by flg22 in plants grown with SynCom35 at day 12, they were up-regulated on the first day of treatment (SI Appendix, Fig.…”

Section: Resultsmentioning

confidence: 96%

Specific modulation of the root immune system by a community of commensal bacteria

Teixeira

Colaianni

Law

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

107

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Plants have an innate immune system to fight off potential invaders that is based on the perception of nonself or modified-self molecules. Microbe-associated molecular patterns (MAMPs) are evolutionarily conserved microbial molecules whose extracellular detection by specific cell surface receptors initiates an array of biochemical responses collectively known as MAMP-triggered immunity (MTI). Well-characterized MAMPs include chitin, peptidoglycan, and flg22, a 22-amino acid epitope found in the major building block of the bacterial flagellum, FliC. The importance of MAMP detection by the plant immune system is underscored by the large diversity of strategies used by pathogens to interfere with MTI and that failure to do so is often associated with loss of virulence. Yet, whether or how MTI functions beyond pathogenic interactions is not well understood. Here we demonstrate that a community of root commensal bacteria modulates a specific and evolutionarily conserved sector of the Arabidopsis immune system. We identify a set of robust, taxonomically diverse MTI suppressor strains that are efficient root colonizers and, notably, can enhance the colonization capacity of other tested commensal bacteria. We highlight the importance of extracellular strategies for MTI suppression by showing that the type 2, not the type 3, secretion system is required for the immunomodulatory activity of one robust MTI suppressor. Our findings reveal that root colonization by commensals is controlled by MTI, which, in turn, can be selectively modulated by specific members of a representative bacterial root microbiota.

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Section: Resultsmentioning

confidence: 96%

Specific modulation of the root immune system by a community of commensal bacteria

Teixeira

Colaianni

Law

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

107

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“…We observed high intraspecific diversity in the above-mentioned components early after elicitation with laminarin, and at basal levels. Large-scale intraspecific variation in basal immunity has also been reported on a transcriptional level in A. thaliana accessions, upon elicitation with the bacterial PAMP flg22 (Winkelmüller et al ., 2021).…”

Section: Discussionmentioning

confidence: 96%

Laminarin-triggered defence responses are geographically dependent for natural populations ofSolanum chilense

Kahlon

Förner

Muser

et al. 2021

Preprint

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Natural plant populations are highly polymorphic and often show intraspecific quantitative, variation in resistance properties against pathogens. The activation of the underlying defence responses can depend on the perception of conserved pathogen-associated molecular patterns (PAMPs). To dissect and understand such variation, we evaluated the diversity of responses induced by laminarin (representing a general glucan elicitor of plant immune responses) in the wild tomato species Solanum chilense. We confirm considerable overlap of the plant's global transcriptional responses to laminarin and to the oomycete pathogen Phytophthora infestans. We further measured key components of basal defence responses such as reactive oxygen species (ROS) production and levels of diverse phytohormones and their derivatives upon elicitation with laminarin in 83 plants originating from nine natural populations of S. chilense from distinct geographic origin. We found high diversity in these components at basal and elicitor-induced levels. We generated generalised linear mixed models (GLMMs) with these components to explain the observed resistance phenotype against P. infestans in the plants and found that additive effects of multiple components best explain resistance at the species level. For individual components, we observed the strongest positive correlation between the resistance phenotype and ethylene (ET) production upon laminarin elicitation. The strength of this correlation differed between individual populations. Chemical inhibition of ET production in individuals from a population, in which ET production was associated with resistance, provoked more severe disease symptoms. Our findings reveal high diversity in the strength of induced defence responses within a species and in the basal levels of other stress-related phytohormones. We show the involvement of multiple components with a quantitatively different contribution of individual components to resistance in geographically separated populations of S. chilense against P. infestans.

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“…The execution of early and late immune responses upon pathogen recognition are fundamentally modulated by optimal gene expression (Birkenbihl et al , 2017; Winkelmüller et al , 2021). Chromatin changes and nucleosome dynamics fine-tune gene expression in stress conditions.…”

Section: Introductionmentioning

confidence: 99%

Linker histone H1 regulates defense priming and immunity in plants

Hirt

Sheikh

Nawaz

et al. 2022

Preprint

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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 that histone 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 was correlated with the enhanced DNA methylation and reduced H3K56ac levels upon priming. 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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Gene expression evolution in pattern-triggered immunity withinArabidopsis thalianaand across Brassicaceae species

Cited by 4 publications

References 107 publications

Specific modulation of the root immune system by a community of commensal bacteria

Specific modulation of the root immune system by a community of commensal bacteria

Laminarin-triggered defence responses are geographically dependent for natural populations ofSolanum chilense

Linker histone H1 regulates defense priming and immunity in plants

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