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Characterization of PEP1-influenced transcriptional reprogramming at the Arabidopsis root meristem

ABSTRACT: The apical root growth is immensely affected by pathogen-associated molecular patterns (PAMPs) or plant-derived damage-associated molecular pattern (DAMPs). Upon perceiving the danger signals, elevated defense machinery often compromises root apical growth, resulting in the meristem's aberrant proliferative and formative divisions. In our previous study, we reported that one of the DAMP signals, PEP1, reprograms developmental pathways in the root apical meristem resulting in the reduction of stele cell numbers, alteration of the xylem vessel organizations, and disruption of cell-to-cell symplastic connections. However, a comprehensive atlas of the gene regulatory networks associated with the root growth-defense tradeoffs is yet to be elucidated. To gain an insight into the dynamic molecular framework that modulates root development under elevated pathogenic signals, we performed a time course RNA-sequencing analysis in the root meristem after PEP1 treatment. Based on expression dynamics of the DEGs (fold change ≥ 1.5; p < 0.05), 12 clusters were obtained following K-means algorithm. Intriguingly, among the PEP1-induced gene clusters, we observed that a group of zinc finger proteins, comprising one of the most prominent transcription factor families, are highly enriched. On the contrary, the PEP1-repressed gene clusters included various developmental regulators expressed in the vascular tissues. Indeed, an in vitro network analysis using selected PEP1-induced and repressed clusters indicated STZ as a potential key mediator of the defense-induced developmental reprogramming pathway in the root stele. We also revealed the involvement of two related homologs of STZ, ZAT6, and AZF3, in this trade-off pathway. Our study provides a comprehensive overview of transcription factors that respond to the early hours of PEP1 induction and hijack cellular machinery, thereby contributing to cellular reorganization and growth in the root apical meristem.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE252414 | GEO | 2025/01/08

REPOSITORIES: GEO

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Project description:The mechanisms ensuring balanced growth remain a critical question in developmental biology. In plants, this balance relies on spatiotemporal integration of hormonal signaling pathways, but the understanding of the precise contribution of each hormone is just beginning to take form. Brassinosteroid (BR) hormone, is shown here to have opposing effects on root meristem size, depending on its site of action. BR is demonstrated to both delay and promote onset of stem cell daughter differentiation, when acting in the outer tissue of the root meristem, the epidermis, and the inner-most tissue, the stele, respectively. To understand the molecular basis of this phenomenon, a comprehensive spatiotemporal translatome mapping of Arabidopsis roots was performed. Analyses of wild type and mutants featuring different distributions of BR, revealed autonomous, tissue-specific gene responses to BR, implying its contrasting tissue-dependent impact on growth. BR-induced genes were primarily detected in epidermal cells of the basal meristem zone and were enriched by auxin-related genes. In contrast, repressed BR genes prevailed in the stele of the apical meristem zone. Furthermore, auxin was found to mediate the growth-promoting impact of BR signaling originating in the epidermis, while BR signaling in the stele buffered this effect. We propose that context-specific BR activity and responses are oppositely interpreted at the organ level, ensuring coherent growth. 24 samples of polyribosome-associated mRNA (following 0, 3, and 8 hours of BR treatment, in two biological repetitions), were collected. RNA samples were sequenced on an Illumina HiSeq 2500, to obtain 50 bp single-end reads. These reads were aligned to the TAIR10 assembly of the Arabidopsis thaliana genome, using Tophat2 v2.0.9. Transcript coordinates from the TAIR10 reference set were used to guide the alignment process. After alignment, the numbers of reads per transcript were estimated using HTSeq v0.5.3p3, and DESeq2 v1.2.8 was used to normalize read counts and call differentially expressed genes.

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Characterization of PEP1-influenced transcriptional reprogramming at the Arabidopsis root meristem

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