Repeatome landscapes and cytogenetics of hortensias provide a framework to trace Hydrangea evolution and domestication.

BACKGROUND AND AIMS: Ornamental hortensias are bred from a reservoir of over 200 species in the genus Hydrangea s.l. (Hydrangeaceae), and are valued in gardens, households and landscapes across the globe. The phenotypic diversity of hortensia cultivars, hybrids and wild relatives is mirrored by their genomic variation, with differences in genome size, base chromosome numbers and ploidy level. We aim to understand the genomic and chromosomal basis of hortensia genome variation. Therefore, we analysed six hortensias with different origins and chromosomal setups for repeatome divergence, the genome fraction with the highest sequence turnover. This holds information from the hortensias' evolutionary paths and can guide breeding initiatives. METHODS: We compiled a hortensia genotype panel representing members of the sections Macrophyllae, Hydrangea, Asperae and Heteromallae and reconstructed a plastome-based phylogenetic hypothesis as the evolutionary basis for all our analyses. We comprehensively characterized the repeatomes by whole-genome sequencing and comparative repeat clustering. Major tandem repeats were localized by multicolour FISH. KEY RESULTS: The Hydrangea species show differing repeat profiles reflecting their separation into the two major Hydrangea clades: diploid Hydrangea species from Japan show a conserved repeat profile, distinguishing them from Japanese polyploids as well as Chinese and American hortensias. These results are in line with plastome-based phylogenies. The presence of specific repeats indicates that H. paniculata was not polyploidized directly from the common ancestor of Japanese Hydrangea species, but evolved from a distinct progenitor. Major satellite DNAs were detected over all H. macrophylla chromosomes. CONCLUSIONS: Repeat composition among the Hydrangea species varies in congruence with their origins and phylogeny. Identified species-specific satDNAs may be used as cytogenetic markers to identify Hydrangea species and cultivars, and to infer parental species of old Hydrangea varieties. This repeatome and cytogenetics information helps to expand the genetic toolbox for tracing hortensia evolution and guiding future hortensia breeding.