Abstract
Polyploidization results in genome duplication and is an important step in evolution and speciation. The Malus genome confirmed that this genus was derived through auto-polyploidization, yet the genetic and meiotic mechanisms for polyploidization, particularly for aneuploidization, are unclear in this genus or other woody perennials. In fact the contribution of aneuploidization remains poorly understood throughout Plantae. We add to this knowledge by characterization of eupolyploidization and aneuploidization in 27,542 F1 seedlings from seven diploid Malus populations using cytology and microsatellite markers. We provide the first evidence that aneuploidy exceeds eupolyploidy in the diploid crosses, suggesting aneuploidization is a leading cause of genome duplication. Gametes from diploid Malus had a unique combinational pattern; ova preserved euploidy exclusively, while spermatozoa presented both euploidy and aneuploidy. All non-reduced gametes were genetically heterozygous, indicating first-division restitution was the exclusive mode for Malus eupolyploidization and aneuploidization. Chromosome segregation pattern among aneuploids was non-uniform, however, certain chromosomes were associated for aneuploidization. This study is the first to provide molecular evidence for the contribution of heterozygous non-reduced gametes to fitness in polyploids and aneuploids. Aneuploidization can increase, while eupolyploidization may decrease genetic diversity in their newly established populations. Auto-triploidization is important for speciation in the extant Malus. The features of Malus polyploidization confer genetic stability and diversity, and present heterozygosity, heterosis and adaptability for evolutionary selection. A protocol using co-dominant markers was proposed for accelerating apple triploid breeding program. A path was postulated for evolution of numerically odd basic chromosomes. The model for Malus derivation was considerably revised. Impacts of aneuploidization on speciation and evolution, and potential applications of aneuploids and polyploids in breeding and genetics for other species were evaluated in depth. This study greatly improves our understanding of evolution, speciation, and adaptation of the Malus genus, and provides strategies to exploit polyploidization in other species.
Highlights
Whole or partial genome duplication can result from eupolyploidization and aneuploidization; first- and second-division restitutions are their primary paths [1]–[12]
Non-reduced gametes derived by first-division restitution (FDR) possess a higher heterozygosity and more complex epistatic combinations from their parents than those by second-division restitution (SDR) [1], [8], [11], [35]–[][37], the genetic differences between FDR and SDR may have an important influence on the fate of neopolyploids either in speciation or evolution [1], [8], [11], [37]
Aneuploidy exceeded eupolyploidy (Table 1), and ova only contributed euploidy while spermatozoa contributed both euploidy and aneuploidy (Figure 1) for apple polyploidization. These unique characters of polyploidization in the diploid Malus confer genetic diversity and multi-directions for evolution and speciation. This is the first demonstration of a strategy using co-dominant markers to successfully analyze meiotic mechanisms and cytotypic derivation of unreduced gametes contributing to polyploids and aneuploids
Summary
Whole or partial genome duplication can result from eupolyploidization and aneuploidization; first- and second-division restitutions are their primary paths [1]–[12]. Up to 15% of angiosperm speciation is associated with paleo-polyploidization [1]–[6], [10], [12], [16]– [18] It is being increasingly confirmed by genomics [4], [6], and supported by the recent release of Malus genome [7]. This contests historical views that neopolyploidy is low among woody perennials due to cambium formation constraining genomic duplication [2], [8]. Similar investigation in woody perennials has been problematic owing to long generation cycles, complex secondary metabolites and poor transferability of flow cytometry and cytological methods for sporogenesis [1], [14], [26]
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