Root cap cell corpse clearance limits microbial colonization in Arabidopsis thaliana
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Curated by eLife
eLife assessment
This study explores the interplay between fungal colonization and controlled programmed cell death in Arabidopsis thaliana root cells. The authors reveal how this process is affected by corpse clearance in the root cap, highlighting some of the key elements in this process including a root cap-specific transcription factor. With this, the authors have discovered an important relationship between transcriptional regulation of developmentally controlled cell death and the beneficial colonization of plants by fungi. The work thus establishes a solid basis for further studies of plant-microbiome associations along the root axis.
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- Evaluated articles (eLife)
- Plant Biology (eLife)
Abstract
Programmed cell death occurring during plant development (dPCD) is a fundamental process integral for plant growth and reproduction. Here, we investigate the connection between developmentally controlled PCD and fungal accommodation in Arabidopsis thaliana roots, focusing on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB) and the senescence-associated nuclease BFN1. Mutations of both dPCD regulators increase colonization by the beneficial fungus Serendipita indica , primarily in the differentiation zone. smb-3 mutants additionally exhibit hypercolonization around the meristematic zone and a delay of S. indica -induced root-growth promotion. This demonstrates that root cap dPCD and rapid post-mortem clearance of cellular corpses represent a physical defense mechanism restricting microbial invasion of the root. Additionally, reporter lines and transcriptional analysis revealed that BFN1 expression is downregulated during S. indica colonization in mature root epidermal cells, suggesting transcriptional control as a means for microbial regulation of host dPCD. The process of programmed cell death in root development (dPCD) influences the extent and outcomes of fungal symbiosis Fungal colonization of the root tip and differentiation zone is restricted by SMB-mediated clearance of dead cells, which preserves the meristem and regulates symbiosis The plant nuclease BFN1, which is associated with senescence, is exploited by beneficial microbes to facilitate their root accommodation
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eLife assessment
This study explores the interplay between fungal colonization and controlled programmed cell death in Arabidopsis thaliana root cells. The authors reveal how this process is affected by corpse clearance in the root cap, highlighting some of the key elements in this process including a root cap-specific transcription factor. With this, the authors have discovered an important relationship between transcriptional regulation of developmentally controlled cell death and the beneficial colonization of plants by fungi. The work thus establishes a solid basis for further studies of plant-microbiome associations along the root axis.
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Reviewer #1 (Public Review):
Summary:
The study investigated how root cap cell corpse removal affects the ability of microbes to colonize Arabidopsis thaliana plants. The findings demonstrate how programmed cell death and its control in root cap cells affect the establishment of symbiotic relationships between plants and fungi. Key details on molecular mechanisms and transcription factors involved are also given. The study suggests reevaluating microbiome assembly from the root tip, thus challenging traditional ideas about this process. While the work presents a key foundation, more research along the root axis is recommended to gain a better understanding of the spatial and temporal aspects of microbiome recruitment.
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Reviewer #2 (Public Review):
Summary:
The authors identify the root cap as an important key region for establishing microbial symbioses with roots. By highlighting for the first time the crucial importance of tight regulation of a specific form of programmed cell death of root cap cells and the clearance of their cell corpses, they start unraveling the molecular mechanisms and its regulation at the root cap (e.g. by identifying an important transcription factor) for the establishment of symbioses with fungi (and potentially also bacterial microbiomes).
Strengths:
It is often believed that the recruitment of plant microbiomes occurs from bulk soil to rhizosphere to endosphere. These authors demonstrate that we have to re-think microbiome assembly as a process starting and regulated at the root tip and proceeding along the root axis.
Weakn…
Reviewer #2 (Public Review):
Summary:
The authors identify the root cap as an important key region for establishing microbial symbioses with roots. By highlighting for the first time the crucial importance of tight regulation of a specific form of programmed cell death of root cap cells and the clearance of their cell corpses, they start unraveling the molecular mechanisms and its regulation at the root cap (e.g. by identifying an important transcription factor) for the establishment of symbioses with fungi (and potentially also bacterial microbiomes).
Strengths:
It is often believed that the recruitment of plant microbiomes occurs from bulk soil to rhizosphere to endosphere. These authors demonstrate that we have to re-think microbiome assembly as a process starting and regulated at the root tip and proceeding along the root axis.
Weaknesses:
The study is a first crucial starting point to investigate the spatial recruitment of beneficial microorganisms along the root axis of plants. It identifies e.g. an important transcription factor for programmed cell death, but more detailed investigations along the root axis are now needed to better understand - spatially and temporally - the orchestration of microbiome recruitment.
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