Global or local? A pan-plastome perspective on intraspecific diversity across seed plants and genetic erosion during domestication

Genetic diversity of plant plastid genomes (plastomes) at the population level is understudied. Research has shown that plastomes are conserved at lower taxonomic levels, leading to the assumption that plastomic diversity is limited within species. By examining 6,484 plastomes from 17 representative seed plants, we show that intraspecific plastomic variation is far more extensive than previously thought. We describe decoupled variation in adjacent regions and diverse hypervariable locations across plastomes, likely shaped by lineage-specific mutational and selective pressures. This heterogeneity suggests that, even in the absence of biparental inheritance and recombination, plastomes should be treated as multi-locus markers with differing models of sequence evolution. By analyzing 2,306 soybean accessions as part of the largest plastid pangenome to date, we reveal previously overlooked erosion of plastomic diversity via maternal bottlenecks during domestication. Thus, the wild relatives of crops could be an untapped genetic resource for crop improvement via organellar selection including the matching of plastid and nuclear genomes to reduce cytonuclear incompatibility.