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

Abstract

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.

Keywords: Differentiation; Genetic resources; Malus x domestica Borkh.; Parentage analysis; Population structure; SSR markers; Variability.

Fig. 1

Graphical display of the results of the Structure analyses. a1) Proportions of ancestry of 1859 unique diploid apple genotypes for K = 3 groups inferred with Structure v.2.3.4 software [67]. Each genotype is represented by a vertical bar partitioned into K = 3 segments representing the estimated membership fraction in three groups. The three groups are depicted using the following color codes: Red = group K1; Blue = group K2; Green = group K3. a2) Proportions of ancestry of the same 1859 genotypes following a nested Structure analysis within each previously defined group. For K1 and K3 three subgroups are shown and for K2 two subgroups are shown. Each genotype is represented by a vertical bar partitioned into K = 2 or 3 subgroups representing the estimated membership fraction in each subgroup. Genotypes are presented in the same order than in a1. The subgroups are depicted using the following color codes: light Pink = K1.1; Purple = K1.2; dark Pink = K1.3; light Blue = K2.1; dark Blue = K2.2; fluorescent Green = K3.1; dark Green = K3.2; light Green = K3.3. b) Proportions of ancestry of 1653 unique diploid apple genotypes with known European region of origin for K = 3 groups inferred with the same Structure analysis as in a. The genotypes are sorted according to their European region of origin (North + East, West, and South)

Fig. 2

Scatter plot of the Principal Coordinate Analysis (PCoA) of the 1859 apple accessions based on the 16 SSR data. The three groups are depicted using the following color codes: Red = group K1; Blue = group K2; Green = group K3

Fig. 3

Neighbor-joining dendrogram based on simple matching dissimilarity matrix calculated from the dataset of 16 SSR markers for the 1859 genotypes clustered in the three groups revealed by the Bayesian model-based clustering method. The three groups are depicted using the following color codes: Red = group K1; Blue = group K2; Green = group K3

Fig. 4

Genetic composition of the groups of cultivars clustered by country of origin for K = 3 groups inferred with Structure. For the detailed country list, see Additional file 1. The pies represent the proportion of each group in each country; color codes are as per Fig. 1 a1