Evolutionary correlation between linker histones and microtubular structures

Histones of the H1 group (linker histones) are abundant components of chrom atin in eukaryotes, occurring on average at one molecule per nucleosome. Th e recent reports on the lack of a clear phenotypic effect of knock-out muta tions as well as overexpression of histone H1 genes in different organisms have seriously undermined the long-held view that linker histones are essen tial for the basic functions of eukaryotic cells. In an attempt to resolve the paradox of an abundant conserved protein without a clear function, we r e-examined the molecular and phylogenetic data on linker histones to see if they could reveal any correlation between the features of H1 and the funct ional or morphological characteristics of cells or organisms. Because of an earlier demonstration that in sea urchin the chromatin-type histone HI is also found in the flagellar microtubules (Multigner et al. 1992), we focuse d on the correlation between the features of H1 and those of microtubular s tructures. A phylogenetic tree based on multiple alignment of over 100 avai lable H1 sequences suggests that the first divergence of the globular domai n of H1 (GH1) resulted in branching into separate types characteristic for plants/Dictyostelium and for animals/ascomycetes, respectively. The GH1s of these two types differ by a short region (usually 5 amino acids) placed at a specific location within the C-terminal wing subdomain of GH1. Evolution ary analysis of the diversification of H1 mRNA into cell-cycle-dependent (p olyA(-)) and independent (polyA(+)) forms showed a mosaic occurrence of the se two forms in plants and animals, despite the fact that the H1 proteins o f plants and animals belong to two well-distinguished groups. However, amon g organisms from both animal and plant kingdom, only those with H1 mRNA of a polyA- type have flagellated gametes. This correlation as well as the dem onstration that in Volvox carteri the accumulation of polyA- mRNA of H1 occ urs concurrently with the production of new flagella (Lindauer et al. 1993) , suggests a direct link between polyA- phenotype of histone H1 mRNA and fl agello-genesis.