Molecular, genetic and evolutionary analysis of a paracentric inversion in Arabidopsis thaliana

Abstract

SummaryChromosomal inversions can provide windows onto the cytogenetic, molecular, evolutionary and demographic histories of a species. Here we investigate a paracentric 1.17‐Mb inversion on chromosome 4 of Arabidopsis thaliana with nucleotide precision of its borders. The inversion is created by Vandal transposon activity, splitting an F‐box and relocating a pericentric heterochromatin segment in juxtaposition with euchromatin without affecting the epigenetic landscape. Examination of the RegMap panel and the 1001 Arabidopsis genomes revealed more than 170 inversion accessions in Europe and North America. The SNP patterns revealed historical recombinations from which we infer diverse haplotype patterns, ancient introgression events and phylogenetic relationships. We find a robust association between the inversion and fecundity under drought. We also find linkage disequilibrium between the inverted region and the early flowering Col‐FRIGIDA allele. Finally, SNP analysis elucidates the origin of the inversion to South‐Eastern Europe approximately 5000 years ago and the FRI‐Col allele to North‐West Europe, and reveals the spreading of a single haplotype to North America during the 17th to 19th century. The ‘American haplotype’ was identified from several European localities, potentially due to return migration.

Epigenetic activation of meiotic recombination near Arabidopsis thaliana centromeres via loss of H3K9me2 and non-CG DNA methylation

“…For example, the inhibitory effect of structural polymorphism is evident within the ∼1.17-Mb heterochromatic knob inversion on Chromosome 4, which is suppressed for crossovers in both wild-type and cmt3 populations ( Fig. 2D; Fransz et al 2000Fransz et al , 2016. Following DSB formation, resection occurs to generate 3 ′ single-stranded DNA that can perform strand invasion of homologous chromosomes (Keeney and Neale 2006).…”

Genetic and epigenetic variation of transposable elements in Arabidopsis

“…For instance, in oil palm DNA hypomethylation of an intronic LINE retrotransposon during tissue culture leads to palm mantling and associated drastic yield reduction [62]. Transposition events can also lead to structural rearrangements including inversions and segmental duplications which can have phenotypic effects [63,64]. The advent of economical long-read sequencing technology will make complete genomic assemblies, and the full assessment of structural differences, a reality, even in crops with large TE complements and genome sizes.…”

On the postglacial spread of human commensal Arabidopsis thaliana: journey to the East

“…The follow-up study showed that the nonrelicts originated recently near the Balkans and spread along the eastÀwest axis of Eurasia, wiping out continental-wide relict populations while incorporating locally adaptive alleles from these (Franc ßois et al, 2008;Lee et al, 2017). For the New World, the North American population arrived at around AD 1600 (Exposito-Alonso et al, 2018a), and most of these probably came from the region near southeastern England and northwestern Germany, carrying an inversion in chromosome 4 (Fransz et al, 2016). Durvasula et al (2017) investigated African A. thaliana and suggested an 'out-of-Africa' demographic model, given the highest genomic variation and numbers of private alleles observed in African accessions.…”