1. Plant Biology

Convergent recruitment of TALE homeodomain life cycle regulators to direct sporophyte development in land plants and brown algae

  1. Alok Arun
  2. Susana M Coelho  Is a corresponding author
  3. Akira F Peters  Is a corresponding author
  4. Simon Bourdareau  Is a corresponding author
  5. Laurent Pérès  Is a corresponding author
  6. Delphine Scornet  Is a corresponding author
  7. Martina Strittmatter
  8. Agnieszka P Lipinska  Is a corresponding author
  9. Haiqin Yao  Is a corresponding author
  10. Olivier Godfroy  Is a corresponding author
  11. Gabriel J Montecinos  Is a corresponding author
  12. Komlan Avia
  13. Nicolas Macaisne
  14. Christelle Troadec  Is a corresponding author
  15. Abdelhafid Bendahmane  Is a corresponding author
  16. J Mark Cock  Is a corresponding author
  1. Sorbonne Université, CNRS, Algal Genetics Group, Integrative Biology of Marine Models (LBI2M), Station Biologique de Roscoff (SBR), France
  2. Bezhin Rosko, France
  3. Institut National de la Recherche Agronomique (INRA), Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, Université Paris-Sud, France
https://doi.org/10.7554/eLife.43101
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Cite this article
  1. Alok Arun
  2. Susana M Coelho
  3. Akira F Peters
  4. Simon Bourdareau
  5. Laurent Pérès
  6. Delphine Scornet
  7. Martina Strittmatter
  8. Agnieszka P Lipinska
  9. Haiqin Yao
  10. Olivier Godfroy
  11. Gabriel J Montecinos
  12. Komlan Avia
  13. Nicolas Macaisne
  14. Christelle Troadec
  15. Abdelhafid Bendahmane
  16. J Mark Cock
(2019)
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
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6 figures, 1 table and 11 additional files

Figures

Figure 1
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The oro life cycle mutation corresponds to a TALE homeodomain transcription factor gene.

(A) Life cycles of wild type and oro mutant Ectocarpus. The wild type sexual cycle (upper panel) involves production of meio-spores by the diploid sporophyte via meiosis in unilocular …

https://doi.org/10.7554/eLife.43101.003
Figure 2 with 1 supplement
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Phenotypic and genetic characterisation of sam life cycle mutants.

(A-C) The sam-1 mutant exhibits gametophyte-like morphological characteristics. Different stages of (A) wild type gametophyte (strain Ec32), (B) wild type partheno-sporophyte (strain Ec32) and (C) sa…

https://doi.org/10.7554/eLife.43101.004
Figure 2—figure supplement 1
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Morphological characteristics of sam mutants.

(A–J) The sam-2 and sam-3 mutants exhibit gametophyte-like morphological characteristics. (A-E) sam-2 mutant (strain Ec364); F-J, sam-3 mutant (strain Ec793); A-D and F-I, different stages of early …

https://doi.org/10.7554/eLife.43101.005
Figure 3 with 1 supplement
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Gene expression analysis.

(A) Abundance of ORO and SAM transcripts during different stages of the life cycle. Error bars, standard error of the mean (SEM); TPM, transcripts per million. (B) Quantitative reverse transcription …

https://doi.org/10.7554/eLife.43101.006
Figure 3—figure supplement 1
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Evidence for the production of full-length ORO and SAM transcripts during the gametophyte generation.

Immature and mature male and female gametophyte Illumina RNA-seq data was mapped onto the ORO and SAM gene sequences using Tophat2. Blue boxes, ORO and SAM coding exons; orange, RNA-seq reads; …

https://doi.org/10.7554/eLife.43101.007
Figure 4
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Detection of ORO-SAM heterodimerisation in vitro using a pull-down assay.

(A) ORO and SAM constructs used for the pull-down experiments. (B) Pull-down assay between SAM and different versions of the ORO protein. (C) Pull-down assay between different versions of the SAM …

https://doi.org/10.7554/eLife.43101.008
Figure 5 with 1 supplement
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ORO and SAM conservation and domain structure.

(A) Unrooted maximum likelihood tree of ORO, SAM and Ec-04_000450 orthologues from diverse brown algal species and the raphidophyte Heterosigma akashiwo. (B) Domain structure of the ORO and SAM TALE …

https://doi.org/10.7554/eLife.43101.009
Figure 5—figure supplement 1
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Intron conservation in homeobox genes.

(A) Conservation of introns in Ectocarpus (Ec), C. okamuranus (Co) and S. japonica (Sj) ORO and SAM genes. Schematic representation of the coding regions of ORO and SAM genes showing the positions …

https://doi.org/10.7554/eLife.43101.010
Author response image 1
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Abundance of ORO, SAM and Ec-04_000450 transcripts during different stages of the life cycle.

Error bars, standard error of the mean (SEM); TPM, transcripts per million.

Tables

Key resources table
Reagent type
(species) or
resource		DesignationSource or referenceIdentifiersAdditional information
Commercial
assay or kit		GoTaq-polymerasePromegaPromega:M3001
Commercial assay or kitQiagen RNeasy Plant mini kitQiagenQiagen:74903
Commercial assay or kitImPro-II Reverse Transcription SystemPromegaPromega:A3800
Commercial assay or kitMagneGSTTMPull-Down SystemPromegaPromega:V8870
Commercial assay or kitTNT Coupled Wheat Germ Extract SystemPromegaPromega:L4130
Commercial assay or kitClarityTM chemiluminescent detectionBioradBiorad:1705060S
Chemical compound, drugCongo redSigmaSigma:C6767-25G
Chemical compound, druganti-GST antibodyOzymeOzyme:91G1
Software,
algorithm		RStudio Version 1.1.463RStudioRRID:SCR_000432http://www.rstudio.com/
Software,
algorithm		GraphPad Prism5GraphPadhttp://graphpad.com/scientific-software/prism
Software,
algorithm		TrimmomaticTrimmomaticRRID:SCR_011848http://www.usadellab.org/cms/index.php?page=trimmomatic
Software,
algorithm		Tophat2TophatRRID:SCR_013035https://ccb.jhu.edu/software/tophat/index.shtml
Software,
algorithm		HTSeqHTSeqRRID:SCR_005514http://htseq.readthedocs.io/en/release_0.9.1/
Software,
algorithm		DESeq2BioconductorRRID:SCR_015687https://bioconductor.org/packages/release/bioc/html/DESeq2.html
Software,
algorithm		Heatplus package for RBioconductor 10.18129/B9.bioc.Heatplushttp://bioconductor.org/packages/release/bioc/html/Heatplus.html
Software,
algorithm		ColorBrewerColorBrewer
project		http://colorbrewer.org
Software,
algorithm		Blast2GOBlast2GORRID:SCR_005828http://www.blast2go.com/b2ghome
Software,
algorithm		HectarDOI: 10.1186/1471-2105-9-393http://webtools.sb-roscoff.fr/root?tool_id=abims_hectar
Software,
algorithm		BlastNational Center
for Biotechnology
Information		https://blast.ncbi.nlm.nih.gov/Blast.cgi
Software,
algorithm		HMMsearchEBIhttps://www.ebi.ac.uk/Tools/hmmer/search/hmmsearch
Software,
algorithm		GenomeViewGenomeViewRRID:SCR_012968http://genomeview.org/
Software,
algorithm		MEGA7DOI: 10.1093/molbev/msr121https://www.megasoftware.net/
Software,
algorithm		RAxMLDOI: 10.1002/0471250953.bi0614s51RRID:SCR_006086https://github.com/stamatak/standard-RAxML
Software,
algorithm		JalviewRRID:SCR_006459http://www.jalview.org/
Software,
algorithm		WebLogoRRID:SCR_010236http://weblogo.berkeley.edu
Software,
algorithm		SPINE-DDOI: 10.1080/073911012010525022http://sparks-lab.org/SPINE-D/
Software,
algorithm		SEGPMID:7952898http://www.biology.wustl.edu/gcg/seg.html
Software,
algorithm		PSIPREDDOI: 10.1093/nar/gkt381RRID:SCR_010246http://bioinf.cs.ucl.ac.uk/psipred/

Additional files

Supplementary file 1

Ectocarpus strains used in this study.

https://doi.org/10.7554/eLife.43101.011
Supplementary file 2

Congo red staining of wild type or sam-1 protoplasts following regeneration in sporophyte-conditioned medium (SCM) or gametophyte-conditioned medium (GCM).

https://doi.org/10.7554/eLife.43101.012
Supplementary file 3

Analysis of genes that are differentially expressed in the gametophyte and sporophyte generations.

https://doi.org/10.7554/eLife.43101.013
Supplementary file 4

Gene ontology analysis of the gametophyte versus sporophyte differentially regulated genes.

https://doi.org/10.7554/eLife.43101.014
Supplementary file 5

Kyoto encyclopaedia of genes and genomes (KEGG) pathway analysis of the gametophyte versus sporophyte differentially regulated genes.

https://doi.org/10.7554/eLife.43101.015
Supplementary file 6

TALE homeodomain transcription factors in brown algae and other stramenopiles.

https://doi.org/10.7554/eLife.43101.016
Supplementary file 7

New microsatellite markers developed to map the ORO gene.

https://doi.org/10.7554/eLife.43101.017
Supplementary file 8

Oligonucleotides used for the qRT-PCR analysis.

https://doi.org/10.7554/eLife.43101.018
Supplementary file 9

Ectocarpus RNA-seq data used in this study.

https://doi.org/10.7554/eLife.43101.019
Supplementary file 10

Manual functional assignments and Hectar subcellular targeting predictions for all Ectocarpus nucleus-encoded proteins

https://doi.org/10.7554/eLife.43101.020
Transparent reporting form
https://doi.org/10.7554/eLife.43101.021

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