Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity

Rayapuram, Naganand; Jarad, Mai; Alhoraibi, Hanna; Bigeard, Jean; Abulfaraj, Aala A.; Völz, Ronny; Mariappan, Kadarkaraisamy; Almeida‐Trapp, Marilia; Schlöffel, Maria A.; Lastrucci, Emmanuelle; Bonhomme, Ludovic; Gust, Andrea A.; Mithöfer, Axel; Arold, Stefan T.; Pflieger, Delphine; Hirt, Heribert

doi:10.1073/pnas.2004670118

Cited by 25 publications

(27 citation statements)

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“…Importantly, the AHL gene family also has been identified to regulate hormone balance in plants, especially gibberellin [ 12 ], jasmonic acid and auxin-related genes [ 13 – 15 ]. This is also illustrated by previous transcriptomic analysis showing that AtAHL13 is a key factor regulating jasmonic acid biosynthesis signal transduction and pathogen immunity [ 16 ]. Importantly, AHL proteins also can regulate the chromatin state.…”

Section: Introductionmentioning

confidence: 55%

Genome-wide identification and expression analysis of the AT-hook Motif Nuclear Localized gene family in soybean

et al. 2021

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Background Soybean is an important legume crop and has significant agricultural and economic value. Previous research has shown that the AT-Hook Motif Nuclear Localized (AHL) gene family is highly conserved in land plants, playing crucial roles in plant growth and development. To date, however, the AHL gene family has not been studied in soybean. Results To investigate the roles played by the AHL gene family in soybean, genome-wide identification, expression patterns and gene structures were performed to analyze. We identified a total of 63 AT-hook motif genes, which were characterized by the presence of the AT-hook motif and PPC domain in soybean. The AT-hook motif genes were distributed on 18 chromosomes and formed two distinct clades (A and B), as shown by phylogenetic analysis. All the AHL proteins were further classified into three types (I, II and III) based on the AT-hook motif. Type-I was belonged to Clade-A, while Type-II and Type-III were belonged to Clade-B. Our results also showed that the main type of duplication in the soybean AHL gene family was segmented duplication event. To discern whether the AHL gene family was involved in stress response in soybean, we performed cis-acting elements analysis and found that AHL genes were associated with light responsiveness, anaerobic induction, MYB and gibberellin-responsiveness elements. This suggest that AHL genes may participate in plant development and mediate stress response. Moreover, a co-expression network analysis showed that the AHL genes were also involved in energy transduction, and the associated with the gibberellin pathway and nuclear entry signal pathways in soybean. Transcription analysis revealed that AHL genes in Jack and Williams82 have a common expression pattern and are mostly expressed in roots, showing greater sensitivity under drought and submergence stress. Hence, the AHL gene family mainly reacts on mediating stress responses in the roots and provide comprehensive information for further understanding of the AT-hook motif gene family-mediated stress response in soybean. Conclusion Sixty-three AT-hook motif genes were identified in the soybean genome. These genes formed into two distinct phylogenetic clades and belonged to three different types. Cis-acting elements and co-expression network analyses suggested that AHL genes participated in significant biological processes. This work provides important theoretical basis for the understanding of AHLs biological functions in soybean.

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Section: Introductionmentioning

confidence: 55%

Genome-wide identification and expression analysis of the AT-hook Motif Nuclear Localized gene family in soybean

et al. 2021

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“…Additionally, the MAPK consensus motif P-X-[pS/pT]-P was overrepresented among MPK6 targets (p < 0.01). Several variants of the proline-directed phosphorylation motif [pS/pT]-P were significantly enriched among targets of MPK4 (p < 0.001), MPK10 (p < 0.001), and BIN2 (p < 0.001) (Amanchy et al, 2007; Lin et al, 2015; Rayapuram et al, 2021) (Figure 4B and Supplemental Data Set S9). Finally, 70% (7/10) of known BIN2 targets reported in the literature and present in our network were correctly predicted as BIN2 targets (either as direct targets or direct downstream second neighbor, Supplemental Data Set S8B).…”

Section: Resultsmentioning

confidence: 99%

Integration of multi-omics data reveals interplay between brassinosteroid and TORC signaling in Arabidopsis

Montes

Wang

Liao

et al. 2022

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Brassinosteroids (BR) and Target of Rapamycin Complex (TORC) are two major actors coordinating plant growth and stress responses. BRs function through a signaling pathway to extensively regulate gene expression and TORC is known to regulate translation and autophagy. Recent studies revealed that these two pathways crosstalk, but a system-wide view of their interplay is still missing. Thus, we quantified the level of 23,975 transcripts, 11,183 proteins, and 27,887 phosphorylation sites in wild-type Arabidopsis and in mutants with altered levels of either BRASSINOSTEROID INSENSITIVE 2 (BIN2) or REGULATORY ASSOCIATED PROTEIN OF TOR 1B (RAPTOR1B), two key players in BR and TORC signaling, respectively. We found that perturbation of BIN2 or RAPTOR1B levels affects a common set of gene-products involved in growth and stress responses. Furthermore, we used the multi-omic data to reconstruct an integrated signaling network. We screened 41 candidate genes identified from the reconstructed network and found that loss of function mutants of many of these proteins led to an altered BR response and/or modulated autophagy activity. Altogether, these results establish a predictive network that defines different layers of molecular interactions between BR- or TORC-regulated growth and autophagy.

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“…Botrytis cinerea infection was performed as previously described (Rayapuram et al , 2021). Briefly, 4-week-old plants were inoculated with Botrytis cinerea (strain: B05.10) by placing a 5 μL droplet of a spore suspension (5×10 5 spores/mL) on each rosette leaf (three fully expanded leaves per plant).…”

Section: Methodsmentioning

confidence: 99%

Linker histone H1 regulates defense priming and immunity in plants

Hirt

Sheikh

Nawaz

et al. 2022

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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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Chromatin phosphoproteomics unravels a function for AT-hook motif nuclear localized protein AHL13 in PAMP-triggered immunity

Cited by 25 publications

References 95 publications

Genome-wide identification and expression analysis of the AT-hook Motif Nuclear Localized gene family in soybean

Genome-wide identification and expression analysis of the AT-hook Motif Nuclear Localized gene family in soybean

Integration of multi-omics data reveals interplay between brassinosteroid and TORC signaling in Arabidopsis

Linker histone H1 regulates defense priming and immunity in plants

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