The hidden duplication past of Arabidopsis thaliana

Abstract

Analysis of the genome sequence of Arabidopsis thaliana shows that this genome, like that of many other eukaryotic organisms, has undergone large-scale gene duplications or even duplications of the entire genome. However, the high frequency of gene loss after duplication events reduces colinearity and therefore the chance of finding duplicated regions that, at the extreme, no longer share homologous genes. In this study we show that heavily degenerated block duplications that can no longer be recognized by directly comparing two segments because of differential gene loss, can still be detected through indirect comparison with other segments. When these so-called hidden duplications in Arabidopsis are taken into account, many homologous genomic regions can be found in five to eight copies. This finding strongly implies that Arabidopsis has undergone three, but probably no more, rounds of genome duplications. Therefore, adding such hidden blocks to the duplication landscape of Arabidopsis sheds light on the number of polyploidy events that this model plant genome has undergone in its evolutionary past.

Fig 1.

Determination of the borders of a hypothetical hidden duplication. Gene coordinates increase from left to right. See Materials and Methods for details.

Fig 2.

Overview of the chromosomal location of all multiplicons detected in the Arabidopsis genome. Baselines (black) represent all genes on the five chromosomes of Arabidopsis. Boxes on the baselines indicate segments that are part of a multiplicon (group of homologous segments). The number of boxes above the baselines indicates the number of additional segments that are homologous to the segment marked on the baseline. Filled boxes represent nonhidden duplications, whereas empty boxes denote hidden duplications, compared with the chromosome segment (see text for details). For all multiplicons with a multiplication level (the number of homologous segments in a multiplicon) greater than four (i.e., in agreement with three duplication events), a different color was used. Multiplicons with multiplication levels of three or four (in agreement with two rounds of duplication events) are marked in dark gray, whereas a multiplication level of two (a single duplication) is marked in light gray. Vertical black bars denote the number of genes, whereas arrows indicate the putative positions of the (collapsed) centromeres, which were removed from the initial dataset.

Fig 3.

Nonhidden and hidden duplicated blocks. (A) Example of a multiplicon in which nonhidden duplications can be observed between all three segments involved. Several genes can be distinguished that have homologs (indicated by black bands) on all segments. Light gray bands show homologs on two of three segments. (B) Example of a multiplicon in which no nonhidden duplication can be observed between the two segments of chromosome IV. Both segments have only one homologous gene in common (dark gray band). However, both segments still share several, but different, homologous genes with a segment on chromosome II. Therefore, it can be concluded that both segments on chromosome IV form a hidden duplication.

Fig 4.

Multiplication levels and contribution of nonhidden and hidden duplications. Bars indicate the number of multiplicons (groups of homologous segments) for each multiplication level. The relative amount of nonhidden duplications within all multiplicons of a given multiplication level is represented as a black square, whereas white circles denote the contribution of hidden duplications. The multiplication levels supporting three rounds of duplication (mutiplication levels five to eight) are shaded in light gray, those supporting only two duplication events (multiplication levels three to four) are in gray, and the multiplication level of two (a single duplication) is marked in dark gray.