Recurrence of Chromosome Rearrangements and Reuse of DNA Breakpoints in the Evolution of the Triticeae Genomes

Abstract

Chromosomal rearrangements (CRs) play important roles in karyotype diversity and speciation. While many CR breakpoints have been characterized at the sequence level in yeast, insects, and primates, little is known about the structure of evolutionary CR breakpoints in plant genomes, which are much more dynamic in genome size and sequence organization. Here, we report identification of breakpoints of a translocation between chromosome arms 4L and 5L of Triticeae, which is fixed in several species, including diploid wheat and rye, by comparative mapping and analysis of the draft genome and chromosome survey sequences of the Triticeae species. The wheat translocation joined the ends of breakpoints downstream of a WD40 gene on 4AL and a gene of the PMEI family on 5AL. A basic helix-loop-helix transcription factor gene in 5AL junction was significantly restructured. Rye and wheat share the same position for the 4L breakpoint, but the 5L breakpoint positions are not identical, although very close in these two species, indicating the recurrence of 4L/5L translocations in the Triticeae. Although barley does not carry the translocation, collinearity across the breakpoints was violated by putative inversions and/or transpositions. Alignment with model grass genomes indicated that the translocation breakpoints coincided with ancient inversion junctions in the Triticeae ancestor. Our results show that the 4L/5L translocation breakpoints represent two CR hotspots reused during Triticeae evolution, and support breakpoint reuse as a widespread mechanism in all eukaryotes. The mechanisms of the recurrent translocation and its role in Triticeae evolution are also discussed.

Hybridization‐facilitated genome merger and repeated chromosome fusion after 8 million years

“…Moreover, our data demonstrate that a recurrent chromosome fusion can take place in a diploid ancestral genome as well as within the same (sub)genome several million years after a polyploidization event. The recurrence of the reciprocal translocation between chromosome arms 4L and 5L, accompanied by the reuse of breakpoints, was reported for Triticeae species (Li et al ., ). Although these were much simpler CRs than the independent formation of AK5/8/6 chromosomes, both instances suggest that some recurrent CRs can be selected for repeatedly.…”

From gene editing to genome engineering: restructuring plant chromosomes via CRISPR/Cas

“…As a result, two independent chromosomes can then be linked by a T-DNA. (D) Due to the presence of two DSBs within a chromosome, the area between the two DSBs can be inversely integrated into the genome through NHEJ-based repair this type of translocation was formed by the NAHR mechanism (Li et al 2016). A second rearrangement mechanism based on HR can lead to translocations between two intact chromosomes, induced by a lesion on a third chromosome (Fig.…”

“…Dependent on the type of rearrangement, changes in chromosomes can result in hybrid sterility, centromere shifts, formation of new open reading frames, disruption of already existing genes, removal of chromosomal fragments, alteration of expression profiles, miRNA silencing, as well as the linkage and delinkage of genes (Allen et al 2004;Lowry and Willis 2010;Rodríguez-Leal et al 2017;Schubert 2018). The majority of CRs are more or less randomly distributed across the entire chromosome but some rearrangements occur repeatedly in the same areas of the chromosome, with these ''rearrangement hotspots'' often being linked to the occurrence of repetitive sequences or heterochromatin-euchromatin borders (Lupski and Stankiewicz 2005;Badaeva et al 2007;Li et al 2016;Zapata et al 2016). In the context of plant breeding, CRs often represent a major obstacle because recombination is inhibited in inverted regions and thus, the transfer of resistance markers from one cultivar to the other is not feasible.…”

Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system

“…Genome rearrangements occur regularly in plants (Udall et al ., ; Szinay et al ., ; Li et al ., ; Zapata et al ., ), in particular inversions are associated across species mainly with adaptation, specification and genome evolution (Blanc et al ., ; Navarro and Barton, ; Kirkpatrick and Barton, ; Fang et al ., ; Schubert and Vu, ). In natural populations, the most common large‐scale chromosomal structural variations are inversions, with changes leading to hybrid sterility, centromere shifting, the formation of new open reading frames (ORFs), disruption of already existing genes, alteration of expression profiles, and also the formation or breakage of genetic linkages (Madan, ; Lowry and Willis, ; Schubert, ).…”