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Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants

Yichun Qiu, Zhen Li (UGent) , Dirk Walther and Claudia Köhler
(2023) MOLECULAR BIOLOGY AND EVOLUTION. 40(9).
Author
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Abstract
MADS-box transcription factors (TFs), among the first TFs extensively studied, exhibit a wide distribution across eukaryotes and play diverse functional roles. Varying by domain architecture, MADS-box TFs in land plants are categorized into Type I (M-type) and Type II (MIKC-type). Type I and II genes have been considered orthologous to the SRF and MEF2 genes in animals, respectively, presumably originating from a duplication before the divergence of eukaryotes. Here, we exploited the increasing availability of eukaryotic MADS-box sequences and reassessed their evolution. While supporting the ancient duplication giving rise to SRF- and MEF2-types, we found that Type I and II genes originated from the MEF2-type genes through another duplication in the most recent common ancestor (MRCA) of land plants. Protein structures predicted by AlphaFold2 and OmegaFold support our phylogenetic analyses, with plant Type I and II TFs resembling the MEF2-type structure, rather than SRFs. We hypothesize that the ancestral SRF-type TFs were lost in the MRCA of Archaeplastida (the kingdom Plantae sensu lato). The retained MEF2-type TFs acquired a Keratin-like domain and became MIKC-type before the divergence of Streptophyta. Subsequently in the MRCA of land plants, M-type TFs evolved from a duplicated MIKC-type precursor through loss of the Keratin-like domain, leading to the Type I clade. Both Type I and II TFs expanded and functionally differentiated in concert with the increasing complexity of land plant body architecture. The recruitment of these originally stress-responsive TFs into developmental programs, including those underlying reproduction, may have facilitated the adaptation to the terrestrial environment.
Keywords
Genetics, Molecular Biology, Ecology, Evolution, Behavior and Systematics, MADS-box transcription factors, land plants, MEF2, Type I/M-type, gene duplication, MULTIPLE SEQUENCE ALIGNMENT, CELL-WALL INTEGRITY, FLOWER DEVELOPMENT, SEED DEVELOPMENT, GENE-EXPRESSION, EVOLUTION, FAMILY, ARABIDOPSIS, MUSCLE

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MLA
Qiu, Yichun, et al. “Updated Phylogeny and Protein Structure Predictions Revise the Hypothesis on the Origin of MADS-Box Transcription Factors in Land Plants.” MOLECULAR BIOLOGY AND EVOLUTION, edited by Mary O’Connell, vol. 40, no. 9, 2023, doi:10.1093/molbev/msad194.
APA
Qiu, Y., Li, Z., Walther, D., & Köhler, C. (2023). Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants. MOLECULAR BIOLOGY AND EVOLUTION, 40(9). https://doi.org/10.1093/molbev/msad194
Chicago author-date
Qiu, Yichun, Zhen Li, Dirk Walther, and Claudia Köhler. 2023. “Updated Phylogeny and Protein Structure Predictions Revise the Hypothesis on the Origin of MADS-Box Transcription Factors in Land Plants.” Edited by Mary O’Connell. MOLECULAR BIOLOGY AND EVOLUTION 40 (9). https://doi.org/10.1093/molbev/msad194.
Chicago author-date (all authors)
Qiu, Yichun, Zhen Li, Dirk Walther, and Claudia Köhler. 2023. “Updated Phylogeny and Protein Structure Predictions Revise the Hypothesis on the Origin of MADS-Box Transcription Factors in Land Plants.” Ed by. Mary O’Connell. MOLECULAR BIOLOGY AND EVOLUTION 40 (9). doi:10.1093/molbev/msad194.
Vancouver
1.
Qiu Y, Li Z, Walther D, Köhler C. Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants. O’Connell M, editor. MOLECULAR BIOLOGY AND EVOLUTION. 2023;40(9).
IEEE
[1]
Y. Qiu, Z. Li, D. Walther, and C. Köhler, “Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants,” MOLECULAR BIOLOGY AND EVOLUTION, vol. 40, no. 9, 2023.
@article{01HBBJ5P50WF9FCK82PY4XE93N,
  abstract     = {{MADS-box transcription factors (TFs), among the first TFs extensively studied, exhibit a wide distribution across eukaryotes and play diverse functional roles. Varying by domain architecture, MADS-box TFs in land plants are categorized into Type I (M-type) and Type II (MIKC-type). Type I and II genes have been considered orthologous to the SRF and MEF2 genes in animals, respectively, presumably originating from a duplication before the divergence of eukaryotes. Here, we exploited the increasing availability of eukaryotic MADS-box sequences and reassessed their evolution. While supporting the ancient duplication giving rise to SRF- and MEF2-types, we found that Type I and II genes originated from the MEF2-type genes through another duplication in the most recent common ancestor (MRCA) of land plants. Protein structures predicted by AlphaFold2 and OmegaFold support our phylogenetic analyses, with plant Type I and II TFs resembling the MEF2-type structure, rather than SRFs. We hypothesize that the ancestral SRF-type TFs were lost in the MRCA of Archaeplastida (the kingdom Plantae sensu lato). The retained MEF2-type TFs acquired a Keratin-like domain and became MIKC-type before the divergence of Streptophyta. Subsequently in the MRCA of land plants, M-type TFs evolved from a duplicated MIKC-type precursor through loss of the Keratin-like domain, leading to the Type I clade. Both Type I and II TFs expanded and functionally differentiated in concert with the increasing complexity of land plant body architecture. The recruitment of these originally stress-responsive TFs into developmental programs, including those underlying reproduction, may have facilitated the adaptation to the terrestrial environment.}},
  articleno    = {{msad194}},
  author       = {{Qiu, Yichun and Li, Zhen and Walther, Dirk and Köhler, Claudia}},
  editor       = {{O'Connell, Mary}},
  issn         = {{0737-4038}},
  journal      = {{MOLECULAR BIOLOGY AND EVOLUTION}},
  keywords     = {{Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics,MADS-box transcription factors,land plants,MEF2,Type I/M-type,gene duplication,MULTIPLE SEQUENCE ALIGNMENT,CELL-WALL INTEGRITY,FLOWER DEVELOPMENT,SEED DEVELOPMENT,GENE-EXPRESSION,EVOLUTION,FAMILY,ARABIDOPSIS,MUSCLE}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{12}},
  title        = {{Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants}},
  url          = {{http://doi.org/10.1093/molbev/msad194}},
  volume       = {{40}},
  year         = {{2023}},
}
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