Common ancestry of heterodimerizing TALE homeobox transcription factors across Metazoa and Archaeplastida

Sunjoo Joo, Ming Hsiu Wang, Gary Lui, Jenny Lee, Andrew Barnas, Eunsoo Kim, Sebastian Sudek, Alexandra Z. Worden, Jae Hyeok Lee

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Background: Complex multicellularity requires elaborate developmental mechanisms, often based on the versatility of heterodimeric transcription factor (TF) interactions. Homeobox TFs in the TALE superclass are deeply embedded in the gene regulatory networks that orchestrate embryogenesis. Knotted-like homeobox (KNOX) TFs, homologous to animal MEIS, have been found to drive the haploid-to-diploid transition in both unicellular green algae and land plants via heterodimerization with other TALE superclass TFs, demonstrating remarkable functional conservation of a developmental TF across lineages that diverged one billion years ago. Here, we sought to delineate whether TALE-TALE heterodimerization is ancestral to eukaryotes. Results: We analyzed TALE endowment in the algal radiations of Archaeplastida, ancestral to land plants. Homeodomain phylogeny and bioinformatics analysis partitioned TALEs into two broad groups, KNOX and non-KNOX. Each group shares previously defined heterodimerization domains, plant KNOX-homology in the KNOX group and animal PBC-homology in the non-KNOX group, indicating their deep ancestry. Protein-protein interaction experiments showed that the TALEs in the two groups all participated in heterodimerization. Conclusions: Our study indicates that the TF dyads consisting of KNOX/MEIS and PBC-containing TALEs must have evolved early in eukaryotic evolution. Based on our results, we hypothesize that in early eukaryotes, the TALE heterodimeric configuration provided transcription-on switches via dimerization-dependent subcellular localization, ensuring execution of the haploid-to-diploid transition only when the gamete fusion is correctly executed between appropriate partner gametes. The TALE switch then diversified in the several lineages that engage in a complex multicellular organization.

Original languageEnglish
Article number136
JournalBMC Biology
Volume16
Issue number1
DOIs
StatePublished - 5 Nov 2018

Keywords

  • Archaeplastida evolution
  • Developmental mechanism
  • KNOX transcription factor
  • PBC-homology
  • TALE-class homeobox
  • Transcription factor heterodimerization

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