The origin and evolution of a two-component system of paralogous genes encoding the centromeric histone CENH3 in cereals

BACKGROUND: The cereal family Poaceae is one of the largest and most diverse angiosperm families. The central component of centromere specification and function is the centromere-specific histone H3 (CENH3). Some cereal species (maize, rice) have one copy of the gene encoding this protein, while some (wheat, barley, rye) have two. We applied a homology-based approach to sequenced cereal genomes, in order to finally trace the mutual evolution of the structure of the CENH3 genes and the nearby regions in various tribes. RESULTS: We have established that the syntenic group or the CENH3 locus with the CENH3 gene and the boundaries defined by the CDPK2 and bZIP genes first appeared around 50 Mya in a common ancestor of the subfamilies Bambusoideae, Oryzoideae and Pooideae. This locus came to Pooideae with one copy of CENH3 in the most ancient tribes Nardeae and Meliceae. The βCENH3 gene as a part of the locus appeared in the tribes Stipeae and Brachypodieae around 35–40 Mya. The duplication was accompanied by changes in the exon-intron structure. Purifying selection acts mostly on αCENH3s, while βCENH3s form more heterogeneous structures, in which clade-specific amino acid motifs are present. In barley species, the βCENH3 gene assumed an inverted orientation relative to αCENH3 and the CDPK2 gene was substituted with LHCB-l. As the evolution and domestication of plant species went on, the locus was growing in size due to an increasing distance between αCENH3 and βCENH3 because of a massive insertion of the main LTR-containing retrotransposon superfamilies, gypsy and copia, without any evolutionary preference on either of them. A comparison of the molecular structure of the locus in the A, B and D subgenomes of the hexaploid wheat T. aestivum showed that invasion by mobile elements and concomitant rearrangements took place in an independent way even in evolutionarily close species. CONCLUSIONS: The CENH3 duplication in cereals was accompanied by changes in the exon-intron structure of the βCENH3 paralog. The observed general tendency towards the expansion of the CENH3 locus reveals an amazing diversity of ways in which different species implement the scenario described in this paper. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03264-3.