Rapid large-scale genomic introgression in Arabidopsis suecica via an autoallohexaploid bridge

Gene flow between species in the genus Arabidopsis occurs in significant amounts, but how exactly gene flow is achieved is not well understood. Polyploidization may be one avenue to explain gene flow between species. One problem, however, with polyploidization as a satisfying explanation is the occurrence of lethal genomic instabilities in neopolyploids as a result of genomic exchange, erratic meiotic behavior, and genomic shock. We have created an autoallohexaploid by pollinating naturally co-occurring diploid Arabidopsis thaliana with allotetraploid Arabidopsis suecica (an allotetraploid composed of A. thaliana and Arabidopsis arenosa). Its triploid offspring underwent spontaneous genome duplication and was used to generate a multigenerational pedigree. Using genome resequencing, we show that 2 major mechanisms promote stable genomic exchange in this population. Legitimate meiotic recombination and chromosome segregation between the autopolyploid chromosomes of the 2 A. thaliana genomes occur without any obvious bias for the parental origin and combine the A. thaliana haplotypes from the A. thaliana parent with the A. thaliana haplotypes from A. suecica similar to purely autopolyploid plants. In addition, we repeatedly observed that occasional exchanges between regions of the homoeologous chromosomes are tolerated. The combination of these mechanisms may result in gene flow leading to stable introgression in natural populations. Unlike the previously reported resynthesized neoallotetraploid A. suecica, this population of autoallohexaploids contains mostly vigorous, and genetically, cytotypically, and phenotypically variable individuals. We propose that naturally formed autoallohexaploid populations might serve as an intermediate bridge between diploid and polyploid species, which can facilitate gene flow rapidly and efficiently.

Automated summary

Gene flow between species in the genus Arabidopsis is significant and may be achieved through polyploidization. However, polyploidization poses challenges due to genomic instabilities. In this study, an autoallohexaploid population was created by crossing diploid Arabidopsis thaliana with allotetraploid Arabidopsis suecica. Genome resequencing revealed two major mechanisms promoting stable genomic exchange in this population. Legitimate meiotic recombination and chromosome segregation between autopolyploid chromosomes of A. thaliana genomes occurred without a bias for parental origin, while occasional exchanges between homoeologous chromosomes were tolerated. These mechanisms may facilitate gene flow and stable introgression in natural populations.