Luca Comai: Unstable by Design: Mutation and Centromere Evolution in Polyploid Plants

Polyploid plant genomes provide a powerful system to study how mutations and genome instability arise, persist, and shape evolution. In the first part of this talk, I will examine how mutations accumulate during perennial growth and how shoot apical meristem (SAM) organization influences this process. By analyzing long-term clonal propagation in potato, we show that somatic mutations accumulate largely independently across SAM layers, with elevated mutation rates in the epidermal L1 layer, reduced rates in germline-contributing L2/3 layers, and strong depletion within genic regions. In hexaploid peppermint, induced mutagenesis allowed us to investigate the spatial organization and phenotypic consequences of somatic mutations. Mutations frequently formed stable periclinal chimeras restricted to individual layers and, in some cases, altered secondary metabolite production through layer-specific haplotype loss. These findings suggest that somatic mutations can be exposed to selection before meiosis, even in the presence of six homeologous gene copies.

In the second part, I will discuss how centromere evolution reshapes polyploid genomes and influences genome stability. Analysis of leaf twin spots in allotetraploid tobacco, previously attributed to somatic recombination, revealed that these sectors predominantly arise from genome instability--including deletions, translocations, and aneuploidy--rather than homologous recombination. Many events involve centromeric breaks, highlighting centromeres as rapidly evolving and structurally fragile genomic regions. In allohexaploid Camelina sativa, divergence among centromeric regions is associated with differential sensitivity to CENH3-mediated genome elimination. Two independent haploid inducers selectively eliminated different parental subgenomes carrying distinct centromeric haplotypes, whereas the subgenome with more homogeneous centromeric repeats appeared resistant.

Together, these studies demonstrate how developmental organization and centromere evolution shape genome plasticity in polyploid plants, with both genic and repetitive variation capable of producing immediate phenotypic and evolutionary consequences.