Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae
- French National Centre for Scientific Research, France
- Bezhin Rosko, France
- Collège de France, France
- Institut National de la Recherche Agronomique, France
Abstract
Three amino acid loop extension homeodomain transcription factors (TALE HD TFs) act as life cycle regulators in green algae and land plants. In mosses these regulators are required for the deployment of the sporophyte developmental program. We demonstrate that mutations in either of two TALE HD TF genes, OUROBOROS or SAMSARA, in the brown alga Ectocarpus result in conversion of the sporophyte generation into a gametophyte. The OUROBOROS and SAMSARA proteins heterodimerise in a similar manner to TALE HD TF life cycle regulators in the green lineage. These observations demonstrate that TALE-HD-TF-based life cycle regulation systems have an extremely ancient origin, and that these systems have been independently recruited to regulate sporophyte developmental programs in at least two different complex multicellular eukaryotic supergroups, Archaeplastida and Chromalveolata.
Data availability
All the sequencing data that has been generated by or used in this study is described in Supplementary file 9. SRA accession numbers are provided for all samples. Genbank accession numbers for the corrected ORO and SAM genes are provided in the results section.
Article and author information
Author details
Funding
Centre National de la Recherche Scientifique
- Alok Arun
- Susana M Coelho
- Akira F Peters
- Simon Bourdareau
- Laurent Pérès
- Delphine Scornet
- Martina Strittmatter
- Agnieszka P Lipinska
- Haiqin Yao
- Olivier Godfroy
- Gabriel J Montecinos
- Komlan Avia
- Nicolas Macaisne
- Christelle Troadec
- Abdelhafid Bendahmane
- J Mark Cock
European Research Council (ERC-SEXYPARTH)
- Abdelhafid Bendahmane
Agence Nationale de la Recherche (ANR-10-BLAN-1727)
- J Mark Cock
Interreg Program France -England (Marinexus)
- J Mark Cock
University Pierre and Marie Curie
- Alok Arun
- Susana M Coelho
- Akira F Peters
- Simon Bourdareau
- Laurent Pérès
- Delphine Scornet
- Martina Strittmatter
- Agnieszka P Lipinska
- Haiqin Yao
- Olivier Godfroy
- Gabriel J Montecinos
- Komlan Avia
- Nicolas Macaisne
- J Mark Cock
European Research Council (638240)
- Susana M Coelho
European Erasmus Mundus program
- J Mark Cock
China Scholarship Council
- J Mark Cock
Agence Nationale de la Recherche (ANR-10-BTBR-04-01)
- J Mark Cock
Agence Nationale de la Recherche (ANR-10-LABX-40)
- Abdelhafid Bendahmane
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Arun et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,006
- views
-
- 390
- downloads
-
- 48
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae
eLife 8:e43101.
https://doi.org/10.7554/eLife.43101
Further reading
-
- Microbiology and Infectious Disease
- Plant Biology
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 a transcriptional control mechanism that facilitates the accommodation of beneficial microbes in the roots.
-
- Cell Biology
- Plant Biology
Plants distribute many nutrients to chloroplasts during leaf development and maturation. When leaves senesce or experience sugar starvation, the autophagy machinery degrades chloroplast proteins to facilitate efficient nutrient reuse. Here, we report on the intracellular dynamics of an autophagy pathway responsible for piecemeal degradation of chloroplast components. Through live-cell monitoring of chloroplast morphology, we observed the formation of chloroplast budding structures in sugar-starved leaves. These buds were then released and incorporated into the vacuolar lumen as an autophagic cargo termed a Rubisco-containing body. The budding structures did not accumulate in mutants of core autophagy machinery, suggesting that autophagosome creation is required for forming chloroplast buds. Simultaneous tracking of chloroplast morphology and autophagosome development revealed that the isolation membranes of autophagosomes interact closely with part of the chloroplast surface before forming chloroplast buds. Chloroplasts then protrude at the site associated with the isolation membranes, which divide synchronously with autophagosome maturation. This autophagy-related division does not require DYNAMIN-RELATED PROTEIN 5B, which constitutes the division ring for chloroplast proliferation in growing leaves. An unidentified division machinery may thus fragment chloroplasts for degradation in coordination with the development of the chloroplast-associated isolation membrane.
