Analysis of the genetic diversity and structure across a wide range of germplasm reveals prominent gene flow in apple at the European level

Background: The amount and structure of genetic diversity in dessert apple germplasm conserved at a European level is mostly unknown, since all diversity studies conducted in Europe until now have been performed on regional or national collections. Here, we applied a common set of 16 SSR markers to genotype more than 2,400 accessions across 14 collections representing three broad European geographic regions (North + East, West and South) with the aim to analyze the extent, distribution and structure of variation in the apple genetic resources in Europe. Results: A Bayesian model-based clustering approach showed that diversity was organized in three groups, although these were only moderately differentiated (FST = 0.031). A nested Bayesian clustering approach allowed identification of subgroups which revealed internal patterns of substructure within the groups, allowing a finer delineation of the variation into eight subgroups (FST = 0.044). The first level of stratification revealed an asymmetric division of the germplasm among the three groups, and a clear association was found with the geographical regions of origin of the cultivars. The substructure revealed clear partitioning of genetic groups among countries, but also interesting associations between subgroups and breeding purposes of recent cultivars or particular usage such as cider production. Additional parentage analyses allowed us to identify both putative parents of more than 40 old and/or local cultivars giving interesting insights in the pedigree of some emblematic cultivars. Conclusions: The variation found at group and subgroup levels may reflect a combination of historical processes of migration/selection and adaptive factors to diverse agricultural environments that, together with genetic drift, have resulted in extensive genetic variation but limited population structure. The European dessert apple germplasm represents an important source of genetic diversity with a strong historical and patrimonial value. The present work thus constitutes a decisive step in the field of conservation genetics. Moreover, the obtained data can be used for defining a European apple core collection useful for further identification of genomic regions associated with commercially important horticultural traits in apple through genome-wide association studies.

This work has been partly funded under the EU seventh Framework Programme by the FruitBreedomics project N°265582: “Integrated approach for increasing breeding efficiency in fruit tree crops”. Genotyping of the Spanish collection was partially funded by INIA, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (project grant no RF2004-008-C03-00). Genotyping of the Swiss collection was funded by the Swiss Federal Office for Agriculture. Genotyping of the French collection was funded by the FRB, ‘Fondation pour la Recherche sur la Biodiversité’. Initial genotyping of the UKNFC material was funded by the UK Depart for the Environment Food and Rural Affairs (Defra), grant GC0140. Providing of VNIISPK material (DNA isolation and delivery) have been done with support of Russian Scientific Fund, Project 14- 1600127. JU has been partially supported by an Early Stage Research Fellowship of the Institute of Advanced Studies (University of Bologna).