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Title: Chloroplast heterogeneity and historical admixture within the genus Malus

item Volk, Gayle
item Henk, Adam
item Baldo, Angela
item Fazio, Gennaro
item Chao, Chihcheng
item Richards, Christopher

Submitted to: American Journal of Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2015
Publication Date: 7/1/2015
Citation: Volk, G.M., Henk, A.D., Baldo, A.M., Fazio, G., Chao, C.T., Richards, C.M. 2015. Chloroplast heterogeneity and historical admixture within the genus Malus. American Journal of Botany. 102(7):1198-1208. DOI: 10.3732/ajb.1500095.

Interpretive Summary: The use of crop wild relatives has great potential for breeding programs aimed at developing resistances to environmental and disease stress. The utility of these related species requires a solid understanding of the species phylogenetic history which assists in structuring their diversity. In the genus Malus, the species designation based on morphological characters has been problematic and subjected to rounds of revisions. Species have been split and lumped together as taxonomic approaches have changed. Because of this ambiguity, this study was designed to resolve the phylogenetic history of this genus using sequences from the maternally inherited chloroplast genome. This kind of sequence is particularly useful in reconstructing historical relationships between species due to its slowly evolving genome (retains historical variation) and a lack of recombination. The study included 30 species within the genus Malus and included 412 individual samples allowing for multiple samples per species. Variants of the sequences (known as haplotypes) were used to infer genetic relationships. The results revealed that the major divisions in chloroplast diversity did not correspond to their morphological species designation. Many chloroplast haplotypes were shared between species reflecting a complex history of biogeography and hybridization. Importantly the cultivars of domesticated apple contain haplotypes that are phylogeneticly distinct reflecting a diverse domestication history. These results help clarify the relationship between species in this important genus and help identify sources of novel variation critical for apple breeding programs.

Technical Abstract: Premise of the study: We examined chloroplast DNA sequence variation in 412 samples representing 30 Malus species (including Malus x domestica Borkh.). Malus wild species are of particular interest for providing novel alleles and traits in apple breeding programs, yet the taxonomic status of these species is problematic. Methods: Four regions of the chloroplast (1681 bp total) were sequenced and aligned for each accession. Phylogenetic relationships were resolved with maximum parsimony using a strict consensus tree using only nodes with bootstrap support greater than 50%. Haplotypes were also analyzed with statistical parsimony and visualized with both a dendogram and median joining network. Key results: Three primary sub-networks were identified. Sub-network A includes species native to China, western North America, as well as M. x domestica and its four primary progenitor species, M. sieversii (Ledeb.) M. Roem., M. orientalis Uglitzk., M. sylvestris (L.) Mill., and M. prunifolia (Willd.) Borkh. Sub-network B includes five Chinese Malus species, and sub-network C includes the three Malus species native to eastern North America. Conclusions: The genetic divergence estimated with cpDNA sequence variation does not correspond to the named species identities. Many haplotypes are shared among sets of species. While regional geographic differentiation is observed among two of the three primary sub-networks, the samples of Malus x domestica originate in a sub-network that is highly admixed. Haplotypes are shared by the domestic apple and its progenitors, which may reflect admixture or incomplete lineage sorting. Sampling must account for haplotype heterogeneity within and among taxa to reconstruct the maternal contributions to speciation in Malus.