Heritable epigenetic diversity for conservation and utilization of epigenetic germplasm resources of clonal East African Highland banana (EAHB) accessions

KEY MESSAGE: Genetically identical East African Highland banana (EAHB) clones are epigenetically diverse with heritable epialleles that can contribute to morphological diversity. ABSTRACT: Heritable epigenetic variation can contribute to agronomic traits in crops and should be considered in germplasm conservation. Despite the genetic uniformity arising from a genetic bottleneck of one ancestral clone, followed by subsequent vegetative propagation, East African Highland bananas (EAHBs) display significant phenotypic diversity potentially arising from somatic mutations, heritable epialleles and/or genotype-by-environment interactions. Here, we use DNA methylation profiling across EAHB accessions representing most of the primary EAHB genepool to demonstrate that the genetically uniform EAHB genepool harbours significant epigenetic diversity. By analysing 724 polymorphic DNA methylation sites by methylation-sensitive AFLP across 90 EAHB cultivars, we could differentiate the EAHB varieties according to their regions (Kenya and Uganda). In contrast, there was minimal association of DNA methylation variation with the five morphological groups that are used to classify EAHBs. We further analysed DNA methylation patterns in parent–offspring cohort, which were maintained in offspring generated by sexual (seed) and asexual (vegetative) propagation, with higher levels of altered DNA methylation observed in vegetatively generated offspring. Our results indicate that the phenotypic diversity of near-isogenic EAHBs is mirrored by considerable DNA methylation variation, which is transmitted between generations by both vegetative reproduction and seed reproduction. Genetically uniform vegetatively propagated crops such as EAHBs harbour considerable heritable epigenetic variation, where heritable epialleles could arise in offspring and contribute to functional traits. This study provides a basis for developing strategies for conservation of epigenetic resources and for integration of epimarkers into crop breeding programmes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s00122-020-03620-1) contains supplementary material, which is available to authorized users.