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A high resolution map of mammalian X chromosome fragile regions assessed by large-scale comparative genomics

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Abstract

Chromosomal evolution involves multiple changes at structural and numerical levels. These changes, which are related to the variation of the gene number and their location, can be tracked by the identification of syntenic blocks (SB). First reports proposed that ~180–280 SB might be shared by mouse and human species. More recently, further studies including additional genomes have identified up to ~1,400 SB during the evolution of eutherian species. A considerable number of studies regarding the X chromosome’s structure and evolution have been undertaken because of its extraordinary biological impact on reproductive fitness and speciation. Some have identified evolutionary breakpoint regions and fragile sites at specific locations in the human X chromosome. However, mapping these regions to date has involved using low-to-moderate resolution techniques. Such scenario might be related to underestimating their total number and giving an inaccurate location. The present study included using a combination of bioinformatics methods for identifying, at base-pair level, chromosomal rearrangements occurring during X chromosome evolution in 13 mammalian species. A comparative technique using four different algorithms was used for optimizing the detection of hotspot regions in the human X chromosome. We identified a significant interspecific variation in SB size which was related to genetic information gain regarding the human X chromosome. We found that human hotspot regions were enriched by LINE-1 and Alu transposable elements, which may have led to intraspecific chromosome rearrangement events. New fragile regions located in the human X chromosome have also been postulated. We estimate that the high resolution map of X chromosome fragile sites presented here constitutes useful data concerning future studies on mammalian evolution and human disease.

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Acknowledgments

PL and CFP are funded by the Universidad del Rosario. This study was supported by The Universidad del Rosario (Grant CS/Genetics 2013).

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  1. Unidad de Genética, Grupo GENIUROS, Escuela de Medicina y Ciencias de la Salud, Universidad del Rosario, Carrera 24 N° 63C-69, Bogotá, Colombia

    Carlos Fernando Prada & Paul Laissue

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335_2014_9537_MOESM1_ESM.tif

Figure S1. Cow X chromosome evolution. A minimum of 16 to 17 inversions wererequired to transform ancestral (A1) to cow X chromosome. A) GRIMM software (X1-X17); B) restricted DCJ model (X1-X16); C) HP model (X1-X17); D. inversion model(X1-X17). Inversion breakpoints are represented by arrows. Negative symbols representinverted syntenic blocks. Hypothetical cow ancestral X chromosomes (I to VII) areincluded in the Figure. The hypothetical (VIII) and real X chromosomes as well as the39 syntenic blocks are located at the bottom of the figure. (TIFF 1085 kb)

Figure S1. Continued (TIFF 984 kb)

Figure S1. Continued (TIFF 1067 kb)

Figure S1. Continued (TIFF 1048 kb)

335_2014_9537_MOESM5_ESM.tif

Figure S2. Mouse and rat X chromosome evolution. A minimum of three inversionswere required to transform the mammalian ancestral X chromosome (A1) to the mouseand rat ancestral X chromosome (A2); a minimum of seven inversions were required totransform A2 to mouse and rat X chromosome, respectively. A) GRIMM software; B)restricted DCJ model; C) HP model; D. inversion model. Inversion breakpoints arerepresented by an arrow. Negative symbols represent inverted syntenic blocks.Hypothetical mouse (III to V) and rat (VII to IX) ancestral X chromosomes (I and II) forA2 are included in the Figure. The real mouse and rat X chromosomes are located afterhypothetical chromosomae VI and X. Complete SB deletions in each species arerepresented by rectangles (TIFF 1012 kb)

Figure S2. Continued (TIFF 888 kb)

Figure S2. Continued (TIFF 1048 kb)

Figure S2. Continued (TIFF 1087 kb)

335_2014_9537_MOESM9_ESM.tif

Figure S3. Anthropoid primates, dog, horse, pig and rabbit X chromosome evolution. Aminimum of one inversion was required to transform the mammalian ancestral Xchromosome (A1) to the ancestral structure of these species (A3 anthropoid primates,dog and horse ancestral chromosome). A minimum of three inversions were required toobtain the rabbit and pig X chromosome. A) GRIMM software; B) restricted DCJmodel; C) HP model; D. inversion model. Inversion breakpoints are represented by anarrow. Negative symbols represent inverted syntenic blocks. The real pig and rabbit Xchromosomes are located after hypothetical chromosomes I and II. Complete syntenicblock deletions are represented by rectangles. Inversions shown in blue were exclusiveto the restricted DCJ model (TIFF 1081 kb)

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Prada, C.F., Laissue, P. A high resolution map of mammalian X chromosome fragile regions assessed by large-scale comparative genomics. Mamm Genome 25, 618–635 (2014). https://doi.org/10.1007/s00335-014-9537-8

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