Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution

Abstract

The comparison of the chromosome numbers of today's species with common reconstructed paleo-ancestors has led to intense speculation of how chromosomes have been rearranged over time in mammals. However, similar studies in plants with respect to genome evolution as well as molecular mechanisms leading to mosaic synteny blocks have been lacking due to relevant examples of evolutionary zooms from genomic sequences. Such studies require genomes of species that belong to the same family but are diverged to fall into different subfamilies. Our most important crops belong to the family of the grasses, where a number of genomes have now been sequenced. Based on detailed paleogenomics, using inference from n = 5-12 grass ancestral karyotypes (AGKs) in terms of gene content and order, we delineated sequence intervals comprising a complete set of junction break points of orthologous regions from rice, maize, sorghum, and Brachypodium genomes, representing three different subfamilies and different polyploidization events. By focusing on these sequence intervals, we could show that the chromosome number variation/reduction from the n = 12 common paleo-ancestor was driven by nonrandom centric double-strand break repair events. It appeared that the centromeric/telomeric illegitimate recombination between nonhomologous chromosomes led to nested chromosome fusions (NCFs) and synteny break points (SBPs). When intervals comprising NCFs were compared in their structure, we concluded that SBPs (1) were meiotic recombination hotspots, (2) corresponded to high sequence turnover loci through repeat invasion, and (3) might be considered as hotspots of evolutionary novelty that could act as a reservoir for producing adaptive phenotypes.

The ZmASR1 Protein Influences Branched-Chain Amino Acid Biosynthesis and Maintains Kernel Yield in Maize under Water-Limited Conditions

“…Thus, sequences from the subclades I-1, I-2, I-3, II-1, and II-2 trace back to chromosomes A11/A12, A4, A1, A2/A4, and A1, respectively. Consequently, the data support the idea that the Poaceae intermediate ancestor with 12 protochromosomes (Murat et al, 2010) already had seven ASR genes. The sequence of events raising this small gene family in grasses might have taken place during the diploidization process following the Poaceaespecific whole-genome duplication (Murat et al, 2010).…”

“…Consequently, the data support the idea that the Poaceae intermediate ancestor with 12 protochromosomes (Murat et al, 2010) already had seven ASR genes. The sequence of events raising this small gene family in grasses might have taken place during the diploidization process following the Poaceaespecific whole-genome duplication (Murat et al, 2010). A larger sample of sequence data from monocots other than Poaceae might help to further elucidate this point.…”

Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential

“…The average ratio of genetic-to-physical distance in low-and high-recombination regions was 0.44 cM/Mb and 6.77 cM/Mb, respectively. In the low-recombination regions, we identified a clustered 155-bp repeat unit, which was similar in sequence to the 140-bp centromere elements in sorghum 29 . This repeat unit is likely to be a constitutive, centromererelated element.…”

“…(a) Evolutionary relationships of the three subfamilies of grasses, including divergence times, whole genome duplication (WGD) events and nested chromosomes fusion (NCF) events. WGD and NCF events were reported in a previous study 29 …”

Analysis of Gene Order Evolution Beyond Single-Copy Genes

“…For this reason many protocols for grouping genes into families involve a second step, after filtering by sequence similarity, which takes accounts for the immediate neighbourhood of each gene copy [76,82]. Only copies in similar neighbourhoods are kept as potential orthologs.…”