Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution

Abstract

Polyploidy is a major force in plant evolution and speciation. In newly formed allopolyploids, pairing between related chromosomes from different subgenomes (homoeologous chromosomes) during meiosis is common. The initial stages of allopolyploid formation are characterized by a spectrum of saltational genomic and regulatory alterations that are responsible for evolutionary novelty. Here we highlight the possible effects and roles of recombination between homoeologous chromosomes during the early stages of allopolyploid stabilization. Homoeologous exchanges (HEs) have been reported in young allopolyploids from across the angiosperms. Although all lineages undergo karyotype change via chromosome rearrangements over time, the early generations after allopolyploid formation are predicted to show an accelerated rate of genomic change. HEs can also cause changes in allele dosage, genome-wide methylation patterns, and downstream phenotypes, and can hence be responsible for speciation and genome stabilization events. Additionally, we propose that fixation of duplication - deletion events resulting from HEs could lead to the production of genomes which appear to be a mix of autopolyploid and allopolyploid segments, sometimes termed "segmental allopolyploids." We discuss the implications of these findings for our understanding of the relationship between genome instability in novel polyploids and genome evolution.

Keywords: chromosome behavior; genome evolution; homoeologous exchanges; polyploidy; synthetics.

FIGURE 1

Meiosis in an example allopolyploid with 2n = 4x = 2 chromosomes (subgenomes indicated in red and blue), showing the most probable outcome of a single crossover event between homoeologous (ancestrally homologous) chromosomes. All such events will most likely be heterozygous in the first generation, even under self-pollination, as gametes with a homoeologous recombination event (duplication/deletion) will unite with gametes from a different meiosis (i.e., pollen with ovules), but may become fixed in subsequent generations after self-pollination.

FIGURE 2

Homoeologous exchanges can generate a diverse spectrum of genomic mosaics over the generations, where some regions of the genome retain homoeologous segments and others become genomically homozygous for a single parental homoeolog, as illustrated here for one pair of homoeologous chromosomes. Thus, some regions of the genome might appear to be “autopolyploid” whereas others appear “allopolyploid.” At the population level and over time, HEs may generate highly variable progeny that may be subject to natural selection, thus fixing specific chromosomal recombinants. In the limit, directional selection may favor one progenitor homoeolog, which may thus appear to have an autopolyploid origin. Genic divergence for duplicates is expected to reflect this history.