Celebrating Mendel, McClintock, and Darlington: On end-to-end chromosome fusions and nested chromosome fusions

The evolution of eukaryotic genomes is accompanied by fluctuations in chromosome number, reflecting cycles of chromosome number increase (polyploidy and centric fissions) and decrease (chromosome fusions). Although all chromosome fusions result from DNA recombination between two or more nonhomologous chromosomes, several mechanisms of descending dysploidy are exploited by eukaryotes to reduce their chromosome number. Genome sequencing and comparative genomics have accelerated the identification of inter-genome chromosome collinearity and gross chromosomal rearrangements and have shown that end-to-end chromosome fusions (EEFs) and nested chromosome fusions (NCFs) may have played a more important role in the evolution of eukaryotic karyotypes than previously thought. The present review aims to summarize the limited knowledge on the origin, frequency, and evolutionary implications of EEF and NCF events in eukaryotes and especially in land plants. The interactions between nonhomologous chromosomes in interphase nuclei and chromosome (mis)pairing during meiosis are examined for their potential importance in the origin of EEFs and NCFs. The remaining open questions that need to be addressed are discussed. Comparative (cyto)genomics have shown that end-to-end chromosome fusions and nested chromosome fusions played a more important role in the evolution of eukaryotic genomes than previously thought.

Automated summary

The evolution of eukaryotic genomes involves fluctuations in chromosome number, with cycles of increase and decrease in chromosome number. Chromosome fusions result from DNA recombination between nonhomologous chromosomes. End-to-end chromosome fusions and nested chromosome fusions have played a more significant role in the evolution of eukaryotic genomes than previously thought. This review summarizes the limited knowledge on the origin, frequency, and evolutionary implications of these fusion events in eukaryotes, with a focus on land plants. The potential importance of interactions between nonhomologous chromosomes and chromosome pairing during meiosis in the origin of these fusions is discussed.