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Genomic basis of multiphase evolution driving divergent selection of zinc-finger homeodomain genes.

ABSTRACT: Gene families divergently evolve and become adapted as different genes with specific structures and functions in living organisms. We performed comprehensive structural and functional analyses of Zinc-finger homeodomain genes (ZF-HDs), including Mini zinc-finger genes (MIFs) and Zinc-finger with homeodomain genes (ZHDs), displaying competitive functions each other. Intensive annotation updates for 90 plant genomes verified that most MIFs (MIF-Is) exhibited distinct motif compositions from ZHDs, although some MIFs (MIF-Zs) contained ZHD-specific motifs. Phylogenetic analyses suggested that MIF-Zs and ZHDs originated from the same ancestral gene, whereas MIF-Is emerged from a distinct progenitor. We used a gene-editing system to identify a novel function of MIF-Is in rice: regulating the surface material patterns in anthers and pollen through transcriptional regulation by interacting ZHDs. Kingdom-wide investigations determined that (i) ancestral MIFs diverged into MIF-Is and MIF-Zs in the last universal common ancestor, (ii) integration of HD into the C-terminal of MIF-Zs created ZHDs after emergence of green plants and (iii) MIF-Is and ZHDs subsequently expanded independently into specific plant lineages, with additional formation of MIF-Zs from ZHDs. Our comprehensive analysis provides genomic evidence for multiphase evolution driving divergent selection of ZF-HDs.

SUBMITTER: Jang MJ

PROVIDER: S-EPMC10415114 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Genomic basis of multiphase evolution driving divergent selection of zinc-finger homeodomain genes.

Jang Min-Jeong MJ Hong Woo-Jong WJ Park Young-Soo YS Jung Ki-Hong KH Kim Seungill S

Nucleic acids research 20230801 14

Gene families divergently evolve and become adapted as different genes with specific structures and functions in living organisms. We performed comprehensive structural and functional analyses of Zinc-finger homeodomain genes (ZF-HDs), including Mini zinc-finger genes (MIFs) and Zinc-finger with homeodomain genes (ZHDs), displaying competitive functions each other. Intensive annotation updates for 90 plant genomes verified that most MIFs (MIF-Is) exhibited distinct motif compositions from ZHDs, ...[more]

PMID: 37394281

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Project description:deltaEF1, a representative of the zinc finger-homeodomain protein family, is a transcriptional repressor which binds E2-box (CACCTG) and related sequences and counteracts the activators through transrepression mechanisms. It has been shown that the N-proximal region of the protein is involved in the transrepression. Here we demonstrate that deltaEF1 has a second mechanism of transrepression recruiting CtBP1 or CtBP2 as its corepressor. A two-hybrid screen of mouse cDNAs with various portions of deltaEF1 identified these proteins, which bind to deltaEF1 in a manner dependent on the PLDLSL sequence located in the short medial (MS) portion of deltaEF1. CtBP1 is the mouse orthologue of human CtBP, known as the C-terminal binding protein of adenovirus E1A, while CtBP2 is the second homologue. Fusion of mouse CtBP1 or CtBP2 to Gal4DBD (Gal4 DNA binding domain) made them Gal4 binding site-dependent transcriptional repressors in transfected 10T1/2 cells, indicating their involvement in a transcriptional repression mechanism. When the MS portion of deltaEF1 was used to Gal4DBD and used to transfect cells, a strong transrepression activity was generated, but this activity was totally dependent on the PLDLSL sequence which served as the site for interaction with endogenous CtBP proteins, indicating that CtBP1 and -2 can act as corepressors. Exogenous CtBP1/2 significantly enhanced transcriptional repression by deltaEF1, and this enhancement was lost if the PLDLSL sequence was altered, demonstrating that CtBP1 and -2 act as corepressors of deltaEF1. In the mouse, CtBP1 is expressed from embryo to adult, but CtBP2 is mainly expressed during embryogenesis. In developing embryos, CtBP1 and CtBP2 are expressed broadly with different tissue preferences. Remarkably, their high expression occurs in subsets of deltaEF1-expressing tissues, e.g., cephalic and dorsal root ganglia, spinal cord, posterior-distal halves of the limb bud mesenchyme, and perichondrium of forming digits, supporting the conclusion that CtBP1 and -2 play crucial roles in the repressor action of deltaEF1 in these tissues.

Dataset Information

Genomic basis of multiphase evolution driving divergent selection of zinc-finger homeodomain genes.

Publications

Genomic basis of multiphase evolution driving divergent selection of zinc-finger homeodomain genes.

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