Prevalence of small inversions in yeast gene order evolution - PubMed (original) (raw)

. 2000 Dec 19;97(26):14433-7.

doi: 10.1073/pnas.240462997.

N Federspiel, T Jones, N Hansen, V Bivolarovic, R Surzycki, R Tamse, C Komp, L Huizar, R W Davis, S Scherer, E Tait, D J Shaw, D Harris, L Murphy, K Oliver, K Taylor, M A Rajandream, B G Barrell, K H Wolfe

Affiliations

Prevalence of small inversions in yeast gene order evolution

C Seoighe et al. Proc Natl Acad Sci U S A. 2000.

Abstract

Gene order evolution in two eukaryotes was studied by comparing the Saccharomyces cerevisiae genome sequence to extensive new data from whole-genome shotgun and cosmid sequencing of Candida albicans. Gene order is substantially different between these two yeasts, with only 9% of gene pairs that are adjacent in one species being conserved as adjacent in the other. Inversion of small segments of DNA, less than 10 genes long, has been a major cause of rearrangement, which means that even where a pair of genes has been conserved as adjacent, the transcriptional orientations of the two genes relative to one another are often different. We estimate that about 1,100 single-gene inversions have occurred since the divergence between these species. Other genes that are adjacent in one species are in the same neighborhood in the other, but their precise arrangement has been disrupted, probably by multiple successive multigene inversions. We estimate that gene adjacencies have been broken as frequently by local rearrangements as by chromosomal translocations or long-distance transpositions. A bias toward small inversions has been suggested by other studies on animals and plants and may be general among eukaryotes.

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Figures

Figure 1

Figure 1

Order and orientation relationships between 298 gene pairs that are adjacent in both S. cerevisiae and C. albicans. All 10 possible relationships between two adjacent genes are shown, with the number of inversions needed to convert any combination into any other. The names of gene pairs in each category are listed at

www.gen.tcd.ie/khwolfe/candida

. The categories labeled as “2 inversions” also could be explained by one gene leapfrogging over the other, but we consider this unlikely.

Figure 2

Figure 2

Examples of single-gene inversions. The three genes in each set are adjacent (ignoring any C. albicans genes without homologs) and in the same order in the two species. Directions of transcription in S. cerevisiae and C. albicans are shown above and below gene names, respectively. Genes named in bold italics have different orientations in the two species. S. cerevisiae gene names are used.

Figure 3

Figure 3

Histogram showing the distance apart in S. cerevisiae of the orthologs of gene pairs that are adjacent in C. albicans. The distance between two genes is expressed in terms of the number of other genes between them on the chromosome.

Figure 4

Figure 4

Gene order relationships of four C. albicans cosmids, sequenced at the Sanger Centre, to parts of the S. cerevisiae genome. Vertical lines connect orthologous genes. Curved arrows indicate genes with inverted orientations. C. albicans genes are named after their S. cerevisiae orthologs; unnamed genes have no close relative in_S. cerevisiae_. Numbers in parentheses indicate numbers of intervening genes in S. cerevisiae that are not shown. S. cerevisiae regions in or near duplicated chromosomal blocks (26) are labeled. The scale at the top refers to_C. albicans_ only.

Figure 5

Figure 5

Relationship between the maximum permitted number of intervening genes (_I_max) between near-neighbors (gene pairs in state B), and the estimate of the proportion of rearrangements that are small (S/S+L). Calculated numerically from Eqs. 3 and 4 using data for PB at different values of_I_max from Fig. 3.

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