publication . Article . Other literature type . 2019

Evolution of the Auxin Response Factors from charophyte ancestors

Raquel Martin-Arevalillo; Emmanuel Thévenon; Fanny Jégu; Thomas Vinos-Poyo; Teva Vernoux; François Parcy; Renaud Dumas;
Open Access English
  • Published: 25 Sep 2019
  • Publisher: HAL CCSD
Abstract
Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most ‘ancient’ ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares man...
Subjects
Medical Subject Headings: food and beveragesfungi
free text keywords: Auxin, Auxin Response Factor, Evolution, Algae, [SDV.BDD]Life Sciences [q-bio]/Development Biology, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Research Article, Research and Analysis Methods, Database and Informatics Methods, Bioinformatics, Sequence Analysis, Sequence Motif Analysis, Biology and Life Sciences, Biochemistry, Hormones, Plant Hormones, Auxins, Plant Biochemistry, Plant Science, Evolutionary Biology, Organismal Evolution, Plant Evolution, Proteins, DNA-binding proteins, Animal Studies, Experimental Organism Systems, Model Organisms, Arabidopsis Thaliana, Organisms, Eukaryota, Plants, Brassica, Plant and Algal Models, Biological Databases, Sequence Databases, Sequence Alignment, auxine, QH426-470, Genetics(clinical), Genetics, Cancer Research, Ecology, Evolution, Behavior and Systematics, Molecular Biology, Transcription factor, chemistry.chemical_classification, chemistry, biology.organism_classification, biology, Chlorokybus, DNA-binding protein, Transcriptional regulation
56 references, page 1 of 4

1. Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, et al. Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. Cell. 2017 Oct; 171(2):287-304.e15. https://doi. org/10.1016/j.cell.2017.09.030 PMID: 28985561 [OpenAIRE]

2. Delwiche CF, Cooper ED. The evolutionary origin of a terrestrial flora. Current Biology. 2015; 25(19): R899-910. https://doi.org/10.1016/j.cub.2015.08.029 PMID: 26439353 [OpenAIRE]

3. Domozych DS, Popper ZA, Sørensen I. Charophytes: Evolutionary Giants and Emerging Model Organisms. Frontiers in plant science. 2016; 7(October):1470. https://doi.org/10.3389/fpls.2016.01470 PMID: 27777578

4. Finet C, Timme RE, Delwiche CF, Marle´taz F. Multigene Phylogeny of the Green Lineage Reveals the Origin and Diversification of Land Plants. Current Biology. 2010 Dec; 20(24):2217-22. https://doi.org/ 10.1016/j.cub.2010.11.035 PMID: 21145743 [OpenAIRE]

5. Vries J De Archibald JM. Plant evolution: landmarks on the path to terrestrial life. New Phytologist. 2018; 217(4):1428-34. https://doi.org/10.1111/nph.14975 PMID: 29318635

6. Lemieux C, Otis C, Turmel M. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biology [Internet]. 2007 Dec [cited 2019 Jun 3]; 5(1). Available from: https://bmcbiol. biomedcentral.com/articles/10.1186/1741-7007-5-2

7. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications [Internet]. 2014 Dec [cited 2018 Nov 21]; 5(1). Available from: http://www.nature.com/articles/ncomms4978

8. Domozych DS, Domozych CE. Multicellularity in green algae: upsizing in a walled complex. Frontiers in Plant Science. 2014; 5(649):1-8. https://doi.org/10.3389/fpls.2014.00649 PMID: 25477895 [OpenAIRE]

9. Umen JG. Green Algae and the Origins of Multicellularity in the Plant Kingdom. Cold Spring Harbor Perspectives in Biology. 2014; 6(11):1-27. https://doi.org/10.1101/cshperspect.a016170 PMID: 25324214

10. Timme RE, Bachvaroff TR, Delwiche CF. Broad Phylogenomic Sampling and the Sister Lineage of Land Plants. Joly S, editor. PLoS ONE. 2012 Jan 13; 7(1):e29696. https://doi.org/10.1371/journal.pone. 0029696 PMID: 22253761 [OpenAIRE]

11. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS. 2014; 111(45):4859-68. https://doi.org/10. 1073/pnas.1323926111 PMID: 25355905

12. Lavy M, Estelle M. Mechanisms of auxin signaling. Development. 2016; 143:3226-9. https://doi.org/10. 1242/dev.131870 PMID: 27624827 [OpenAIRE]

13. Leyser O. Auxin Signaling. Plant Physiology. 2018; 176(1):465-79. https://doi.org/10.1104/pp.17. 00765 PMID: 28818861

14. Finet C, Berne-Dedieu A, Scutt CP, Marletaz F. Evolution of the ARF gene family in land plants: Old domains, new tricks. Molecular Biology and Evolution. 2013; 30:45-56. https://doi.org/10.1093/molbev/ mss220 PMID: 22977118 [OpenAIRE]

15. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM. Isolation of the Arabidopsis ABI3 Gene by Positional Cloning. THE PLANT CELL ONLINE. 1992 Oct 1; 4(10):1251-61. https://doi.org/ 10.1105/tpc.4.10.1251 PMID: 1359917 [OpenAIRE]

56 references, page 1 of 4
Abstract
Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most ‘ancient’ ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares man...
Subjects
Medical Subject Headings: food and beveragesfungi
free text keywords: Auxin, Auxin Response Factor, Evolution, Algae, [SDV.BDD]Life Sciences [q-bio]/Development Biology, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Research Article, Research and Analysis Methods, Database and Informatics Methods, Bioinformatics, Sequence Analysis, Sequence Motif Analysis, Biology and Life Sciences, Biochemistry, Hormones, Plant Hormones, Auxins, Plant Biochemistry, Plant Science, Evolutionary Biology, Organismal Evolution, Plant Evolution, Proteins, DNA-binding proteins, Animal Studies, Experimental Organism Systems, Model Organisms, Arabidopsis Thaliana, Organisms, Eukaryota, Plants, Brassica, Plant and Algal Models, Biological Databases, Sequence Databases, Sequence Alignment, auxine, QH426-470, Genetics(clinical), Genetics, Cancer Research, Ecology, Evolution, Behavior and Systematics, Molecular Biology, Transcription factor, chemistry.chemical_classification, chemistry, biology.organism_classification, biology, Chlorokybus, DNA-binding protein, Transcriptional regulation
56 references, page 1 of 4

1. Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, et al. Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. Cell. 2017 Oct; 171(2):287-304.e15. https://doi. org/10.1016/j.cell.2017.09.030 PMID: 28985561 [OpenAIRE]

2. Delwiche CF, Cooper ED. The evolutionary origin of a terrestrial flora. Current Biology. 2015; 25(19): R899-910. https://doi.org/10.1016/j.cub.2015.08.029 PMID: 26439353 [OpenAIRE]

3. Domozych DS, Popper ZA, Sørensen I. Charophytes: Evolutionary Giants and Emerging Model Organisms. Frontiers in plant science. 2016; 7(October):1470. https://doi.org/10.3389/fpls.2016.01470 PMID: 27777578

4. Finet C, Timme RE, Delwiche CF, Marle´taz F. Multigene Phylogeny of the Green Lineage Reveals the Origin and Diversification of Land Plants. Current Biology. 2010 Dec; 20(24):2217-22. https://doi.org/ 10.1016/j.cub.2010.11.035 PMID: 21145743 [OpenAIRE]

5. Vries J De Archibald JM. Plant evolution: landmarks on the path to terrestrial life. New Phytologist. 2018; 217(4):1428-34. https://doi.org/10.1111/nph.14975 PMID: 29318635

6. Lemieux C, Otis C, Turmel M. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biology [Internet]. 2007 Dec [cited 2019 Jun 3]; 5(1). Available from: https://bmcbiol. biomedcentral.com/articles/10.1186/1741-7007-5-2

7. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications [Internet]. 2014 Dec [cited 2018 Nov 21]; 5(1). Available from: http://www.nature.com/articles/ncomms4978

8. Domozych DS, Domozych CE. Multicellularity in green algae: upsizing in a walled complex. Frontiers in Plant Science. 2014; 5(649):1-8. https://doi.org/10.3389/fpls.2014.00649 PMID: 25477895 [OpenAIRE]

9. Umen JG. Green Algae and the Origins of Multicellularity in the Plant Kingdom. Cold Spring Harbor Perspectives in Biology. 2014; 6(11):1-27. https://doi.org/10.1101/cshperspect.a016170 PMID: 25324214

10. Timme RE, Bachvaroff TR, Delwiche CF. Broad Phylogenomic Sampling and the Sister Lineage of Land Plants. Joly S, editor. PLoS ONE. 2012 Jan 13; 7(1):e29696. https://doi.org/10.1371/journal.pone. 0029696 PMID: 22253761 [OpenAIRE]

11. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS. 2014; 111(45):4859-68. https://doi.org/10. 1073/pnas.1323926111 PMID: 25355905

12. Lavy M, Estelle M. Mechanisms of auxin signaling. Development. 2016; 143:3226-9. https://doi.org/10. 1242/dev.131870 PMID: 27624827 [OpenAIRE]

13. Leyser O. Auxin Signaling. Plant Physiology. 2018; 176(1):465-79. https://doi.org/10.1104/pp.17. 00765 PMID: 28818861

14. Finet C, Berne-Dedieu A, Scutt CP, Marletaz F. Evolution of the ARF gene family in land plants: Old domains, new tricks. Molecular Biology and Evolution. 2013; 30:45-56. https://doi.org/10.1093/molbev/ mss220 PMID: 22977118 [OpenAIRE]

15. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM. Isolation of the Arabidopsis ABI3 Gene by Positional Cloning. THE PLANT CELL ONLINE. 1992 Oct 1; 4(10):1251-61. https://doi.org/ 10.1105/tpc.4.10.1251 PMID: 1359917 [OpenAIRE]

56 references, page 1 of 4
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publication . Article . Other literature type . 2019

Evolution of the Auxin Response Factors from charophyte ancestors

Raquel Martin-Arevalillo; Emmanuel Thévenon; Fanny Jégu; Thomas Vinos-Poyo; Teva Vernoux; François Parcy; Renaud Dumas;