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Microsatellite-centromere mapping in common carp through half-tetrad analysis in diploid meiogynogenetic families

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Abstract

Gene-centromere (G-C) mapping provides insights into the understanding of the composition, structure, and evolution of vertebrate genomes. Common carp (Cyprinus carpio) is an important aquaculture fish and has been proposed to undertake tetraploidization. In this study, we selected 214 informative microsatellite markers across 50 linkage groups of a common carp genetic map to perform gene-centromere mapping using half-tetrad analysis. A total of 199 microsatellites were segregated under the Mendelian expectations in at least one of the three gynogenetic families and were used for G-C distance estimation. The G-C recombination frequency (y) ranged from 0 to 0.99 (0.43 on average), corresponding to a fixation index (F) of 0.57 after one generation of gynogenesis. Large y values for some loci together with significant correlation between G-C distances and genetic linkage map distances suggested the presence of high interference in common carp. Under the assumption of complete interference, 50 centromeres were localized onto corresponding linkage groups (LGs) of common carp, with G-C distances of centromere-linked markers per LG ranging from 0 to 10.3 cM (2.9 cM on average). Based on the information for centromere positions, we proposed a chromosome formula of 2n = 100 = 58 m/sm + 42 t/st with 158 chromosome arms for common carp, which was similar to a study observed by cytogenetic method. The examination of crossover distributions along 10 LGs revealed that the proportion of crossover chromatids was overall higher than that of non-crossover chromatids in gynogenetic progenies, indicating high recombination levels across most LGs. Comparative genomics analyses suggested that the chromosomes of common carp have undergone extensive rearrangement after genome duplication. This study would be valuable to elucidate the mechanism of genome evolution and integrate physical and genetic maps in common carp.

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Acknowledgments

The authors thank J. Qian, H. Liu, W. Guo, C. Zhu, M. Pang, and Y. Sun for sample preparation and laboratory technical assistance. This work was supported by MOST (2010CB126305), FEBL (2011FBZ20), and MOA (2011-G12) of China.

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Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Xiu Feng, Xinhua Wang, Xiaomu Yu & Jingou Tong

  2. University of Chinese Academy of Sciences, Beijing, 100039, China

    Xiu Feng & Xinhua Wang

  3. Heilongjing River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, 150070, China

    Xiaofeng Zhang, Cuiyun Lu & Xiaowen Sun

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  1. Xiu Feng
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  2. Xinhua Wang
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  3. Xiaomu Yu
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  4. Xiaofeng Zhang
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  6. Xiaowen Sun
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  7. Jingou Tong
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Correspondence to Jingou Tong.

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Xiu Feng and Xinhua Wang contributed equally to this work.

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Fig. S1

A summary of linear relation between the two LGs in the map reported by Xu et al. (2013) and the LG23 in the map reported by Zhao et al. (2013). (PDF 409 kb)

Fig. S2

The crossover patterns in chromosomes of 11 LGs in diploid meiogynogenetic families (showed in parentheses) for common carp. The horizontal dotted lines stand for centromeres in 11 LGs. The right bars of each figure represent two chromosomes in dams of families. Each chromosome segment in progenies of each family is filled with grey or black color to indicate the genotype at microsatellite loci; changes in color within a bar represent exchanges between non-sister maternal chromatids. Double crossovers and triple crossovers are labelled by arrows and hollow arrows, respectively. n is the frequency of each four-locus genotype in gynogenetic families. (PDF 189 kb)

Fig. S3

The positions of centromeres on chromosomes of zebrafish and on LGs of common carp map reported by Xu et al. (2013). The chromosomes of zebrafish are showed in red on the left; two LGs (originating from the same chromosome on the left of zebrafish) of common carp map are showed on the right. (PDF 80 kb)

Fig. S4

Conserved regions of synteny between three pairs of common carp homeologous LGs and zebrafish chromosomes. The centromere regions of common carp homeologous LGs and zebrafish chromosomes are painted green, blue and red, respectively. (PDF 679 kb)

Table S1

Information of microsatellites used in this study. (XLS 66 kb)

Table S2

Gene-centromere (G-C) recombination rates (second meiosis segregation frequency, y) and G-C distances of 214 microsatellite markers examined in three meiogynogenetic families of common carp. (XLS 80 kb)

Table S3

Genotypic segregation in three control families at 214 microsatellite loci of common carp. (XLS 89 kb)

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Feng, X., Wang, X., Yu, X. et al. Microsatellite-centromere mapping in common carp through half-tetrad analysis in diploid meiogynogenetic families. Chromosoma 124, 67–79 (2015). https://doi.org/10.1007/s00412-014-0485-6

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