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Evolution and diversification of the ACT-like domain associated with plant basic helix–loop–helix transcription factors
Wednesday, 2023/05/17 | 08:22:46

Yun Sun LeeShin-Han Shiu, and Erich Grotewold

PNAS May 1, 2023; 120 (19) e2219469120


Basic helix–loop–helix (bHLH) proteins constitute one of the largest eukaryote transcription factor (TF) families. About 30% of flowering plants’ bHLH TFs have aspartate kinase, chorismate mutase, and TyrA (ACT)-like domains. Here, we show that ACT-like domains associated with bHLH domains are unique to the plant kingdom and derived from a common ancestor, likely by the fusion of bHLH and ancestor ACR (ACT DOMAIN REPEAT) genes early in the evolution of the green algae. Despite the fast evolution of ACT-like domains, our results show that ACT-like and associated bHLH domains coevolved, and that the association negatively affects the DNA-binding activity of the corresponding bHLH domains. These results unveil the evolutionary history of the ACT-like/bHLH association, providing insights on potential functional consequences.


Basic helix–loop–helix (bHLH) proteins are one of the largest families of transcription factor (TF) in eukaryotes, and ~30% of all flowering plants’ bHLH TFs contain the aspartate kinase, chorismate mutase, and TyrA (ACT)-like domain at variable distances C-terminal from the bHLH. However, the evolutionary history and functional consequences of the bHLH/ACT-like domain association remain unknown. Here, we show that this domain association is unique to the plantae kingdom with green algae (chlorophytes) harboring a small number of bHLH genes with variable frequency of ACT-like domain’s presence. bHLH-associated ACT-like domains form a monophyletic group, indicating a common origin. Indeed, phylogenetic analysis results suggest that the association of ACT-like and bHLH domains occurred early in Plantae by recruitment of an ACT-like domain in a common ancestor with widely distributed ACT DOMAIN REPEAT (ACR) genes by an ancestral bHLH gene. We determined the functional significance of this association by showing that Chlamydomonas reinhardtii ACT-like domains mediate homodimer formation and negatively affect DNA binding of the associated bHLH domains. We show that, while ACT-like domains have experienced faster selection than the associated bHLH domain, their rates of evolution are strongly and positively correlated, suggesting that the evolution of the ACT-like domains was constrained by the bHLH domains. This study proposes an evolutionary trajectory for the association of ACT-like and bHLH domains with the experimental characterization of the functional consequence in the regulation of plant-specific processes, highlighting the impacts of functional domain coevolution.


See https://www.pnas.org/doi/10.1073/pnas.2219469120


Fig. 1: Association of ACT-like and bHLH domains. (A) Schematic representation of bHLH and ACT-like domains. α and β represent the α-helices and β-sheets, respectively. The L within the gray box denotes the loop region. (B) Presence of bHLH-associated ACT-like domains in various species. Green and yellow circles indicate bHLH proteins with or without the ACT-like domains, respectively. The eukaryote phylogenetic tree was modified from the literature (3536). Species information and data source for the bHLH sequences used in this study are presented in Dataset S1, and Pfam analysis result is in Dataset S2. AlphaFold search result is in SI Appendix, Fig. S1B and Dataset S2. Numbers of the ACT-like domains in each species are described in Dataset S1.


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