G-quadruplex (G4) DNA structures are depleted from coding sequences (CDS) and enriched in regulatory regions across diverse genomes (the "G4 paradox"), but the selection regime maintaining this architecture across eukaryotes remains unclear. Analysing 198 reference genomes balanced across the four kingdoms (Animalia 86, Fungi 49, Plantae 33, Protozoa 30), we propose a two-regime architecture in which the dominant selective force depends on the genomic compartment. In CDS, codon-adaptation selection takes priority: naive Nei-Gojobori comparison shows 5-16% synonymous-rate (dS) suppression at G4 codons in six of seven unsaturated species pairs, but the signal is absorbed by per-gene codon-adaptation-index (CAI) adjustment (0/7 pairs retain a G4 odds ratio below 1; five reverse to OR>1). In introns and promoters, where no codons exist, selection acts directly on G4 structure: phylogenetic generalised least-squares (PGLS) yields five Benjamini-Hochberg-significant kingdom-specific helicase associations (q<0.10), all at intronic or promoter G4s, including context-dependent FANCJ/BRIP1 (beta=+1.60, q=0.057 for intron G4 in Plantae; beta=-2.49, q=0.004 for promoter G4 in Protozoa); three of five remain significant on an independent Open Tree of Life backbone. Intronic G4 are concentrated in deeply conserved orthologue groups (>=87.5% in every kingdom), consistent with maintenance of regulatory G4 host-gene context since early eukaryotic evolution.
Tanigawa, M., Iwaki, T.
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