Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae
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.
Reviewing Editor
- Sheila McCormick, University of California, Berkeley, United States
Version history
- Received: October 24, 2018
- Accepted: January 13, 2019
- Accepted Manuscript published: January 15, 2019 (version 1)
- Version of Record published: February 8, 2019 (version 2)
- Version of Record updated: March 18, 2019 (version 3)
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
-
- 2,893
- views
-
- 367
- downloads
-
- 46
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Plant Biology
Urea is intensively utilized as a nitrogen fertilizer in agriculture, originating either from root uptake or from catabolism of arginine by arginase. Despite its extensive use, the underlying physiological mechanisms of urea, particularly its adverse effects on seed germination and seedling growth under salt stress remains unclear. In this study, we demonstrate that salt stress induces excessive hydrolysis of arginine-derived urea, leading to an increase in cytoplasmic pH within seed radical cells, which, in turn, triggers salt-induced inhibition of seed germination (SISG) and hampers seedling growth. Our findings challenge the long-held belief that ammonium accumulation and toxicity are the primary causes of SISG, offering a novel perspective on the mechanism underlying these processes. This study provides significant insights into the physiological impact of urea hydrolysis under salt stress, contributing to a better understanding of SISG.
-
- Biochemistry and Chemical Biology
- Plant Biology
Transmembrane signaling by plant receptor kinases (RKs) has long been thought to involve reciprocal trans-phosphorylation of their intracellular kinase domains. The fact that many of these are pseudokinase domains, however, suggests that additional mechanisms must govern RK signaling activation. Non-catalytic signaling mechanisms of protein kinase domains have been described in metazoans, but information is scarce for plants. Recently, a non-catalytic function was reported for the leucine-rich repeat (LRR)-RK subfamily XIIa member EFR (elongation factor Tu receptor) and phosphorylation-dependent conformational changes were proposed to regulate signaling of RKs with non-RD kinase domains. Here, using EFR as a model, we describe a non-catalytic activation mechanism for LRR-RKs with non-RD kinase domains. EFR is an active kinase, but a kinase-dead variant retains the ability to enhance catalytic activity of its co-receptor kinase BAK1/SERK3 (brassinosteroid insensitive 1-associated kinase 1/somatic embryogenesis receptor kinase 3). Applying hydrogen-deuterium exchange mass spectrometry (HDX-MS) analysis and designing homology-based intragenic suppressor mutations, we provide evidence that the EFR kinase domain must adopt its active conformation in order to activate BAK1 allosterically, likely by supporting αC-helix positioning in BAK1. Our results suggest a conformational toggle model for signaling, in which BAK1 first phosphorylates EFR in the activation loop to stabilize its active conformation, allowing EFR in turn to allosterically activate BAK1.