# Evolutionary Dynamics and Functional Bifurcation of the C2H2 Gene Family in Basidiomycota

## TL;DR

This study explores how the C2H2 gene family evolved in fungi, revealing how these genes help fungi adapt to different environments and develop structures like fruiting bodies.

## Contribution

The study identifies lineage-specific gene expansions and functional roles of C2H2 genes in fungal development and adaptation.

## Key findings

- C2H2 genes show lineage-specific expansions in wood decayers and edible fungi.
- Saprotrophs retain long genes with many introns, while pathogens have streamlined genomes.
- Stage-specific C2H2 gene expression coordinates developmental transitions in Sarcomyxa edulis.

## Abstract

This study performed a phylogenomic analysis of the C2H2 gene family across 30 Basidiomycota species, identifying 1032 genes distributed across six evolutionary clades (Groups I–VI). Functional diversification and lineage-specific expansions were observed: Group II (37.1%) formed a conserved core, while wood decayers (e.g., Schizophyllum commune) and edible fungi (e.g., Pleurotus ostreatus) exhibited clade-specific expansions in Groups III and V, respectively. Physicochemical profiling revealed an acidic bias in Agaricomycotina proteins (pI 4.3–5.8) compared to alkaline trends in pathogens (Ustilaginomycotina/Pucciniomycotina; pI 8.3–8.6). Comparative genomics indicated that saprotrophs retained long genes (12.4 kb) with abundant introns (mean = 6.2/gene), whereas pathogens exhibited genomic streamlining (introns ≤ 2). Synteny network analysis revealed high ancestral conservation in core clusters (Cluster_1–2: 58% homologs) under strong purifying selection (Ka/Ks = 0.18–0.22), while peripheral clusters (Cluster_Mini) approached neutral evolution (Ka/Ks = 0.73). This study reveals stage-specific expression dynamics of 17 C2H2 zinc finger genes in Sarcomyxa edulis, highlighting their roles in coordinating developmental transitions (e.g., SeC2H2_1 in low-temperature adaptation, SeC2H2_7/12 in primordia initiation, and SeC2H2_8/9/13 in fruiting body maturation) through temporally partitioned regulatory programs, providing insights into fungal morphogenesis and stress-responsive adaptation. These findings underscore the dual role of C2H2 genes in sustaining conserved regulatory networks and facilitating ecological adaptation, providing new insights into fungal genome evolution.