Common features of analogous replacement histone H3 genes in animals and plants

Abstract

Phylogenetic analysis of histone H3 protein sequences demonstrates the independent origin of the replacement histone H3 genes in animals and in plants. Multiple introns in the replacement histone H3 genes of animals in a pattern distinct from that in plant replacement H3 genes supports this conclusion. It is suggested that replacement H3 genes arose at the same time that, independently, multicellular forms of animals and of plants evolved. Judged by the degree of invariant and functionally constrained amino acid positions, histones H3 and H4, which form together the tetramer kernel of the nucleosome, have co-evolved with equal rates of sequence divergence. Residues 31 and 87 in histone H3 are the only residues that consistently changed across each gene duplication event that created functional replacement histone H3 variant forms. Once changed, these residues have remained invariant across divergent speciation. This suggests that they are required to allow replacement histone H3 to participate in the assembly of nucleosomes in non-S-phase cells. The abundant occurrence of polypyrimidine sequences in the introns of all replacement H3 genes, and the replacement of an intron by a polypyrimidine motif upstream of the alfalfa replacement H3 gene, suggests a function. It is speculated that they may contribute to the characteristic cell-cycle-independent pattern of replacement histone H3 genes by binding nucleosome-excluding proteins.

Molecular cloning and expression analysis of the replacement histone H3 gene of Italian ryegrass (Lolium multiflorum)

“…The putative protein sequence of the Italian ryegrass histone H3 obtained in the present study had an amino acid sequence that was 100% identical to that of the plant replacement histone reported by Waterborg and Robertson (1996). This suggests that the isolated gene would be a functional replacement histone in Italian ryegrass.…”

“…The downstream region of the 5 0 -splice site of the gIRH3 intron frequently contained pyrimidines (data not shown). Such pyrimidine-rich sequences may be involved in polypyrimidine-binding proteins, such as the GAGA factor in Drosophila melanogaster (Lu et al, 1993) that has been shown to facilitate transcription Waterborg and Robertson, 1996). Using the 5 0 -untranslated region of the Arabidopsis replacement H3 gene and the first intron of alfalfa histone H3.2 gene the enhancement of transgene expression has recently been demonstrated (Chaubet-Gigot et al, 2001;Kelemen et al, 2002), suggesting that the involvement of the polypyrimidine-binding protein that targets such pyrimidine-rich sequences may be important for elevating transgene expression levels.…”

“…The deduced amino acid sequence of the EST clone was 100% identical to that of the consensus plant replacement histone H3 presented by Waterborg and Robertson (1996) and was distinguishable from cell-cycle dependent forms of plant histone H3 (data not shown). The primers used were designed from the nucleotide sequence of the EST clone, and a 784-bp fragment of the corresponding genomic clone (gIRH3) was cloned by PCR amplification.…”

Histone3 variants in plants

“…In plants, substitutions distinguishing H3.1 from H3.3 are only retained at positions 31, 87, and 90 and involve a distinct set of amino acids, showing that H3 variants arose independently in plants and animals (Waterborg and Robertson 1996;Malik and Henikoff 2003;Okada et al 2005). An additional plant-specific substitution at position 41 discriminates H3.3 from H3.1 proteins (Okada et al 2005).…”

“…CenH3s are essential for chromosome segregation during mitosis (Dalal et al 2007). In contrast to CenH3, the variants of histone H3 called H3.3 are similar in length and amino acid sequence with canonical H3.1 except at few positions (Waterborg and Robertson 1996;Malik and Henikoff 2003).…”