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Cytogenetic comparison of heteromorphic and homomorphic sex chromosomes in Coccinia (Cucurbitaceae) points to sex chromosome turnover

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Abstract

Our understanding of the evolution of plant sex chromosomes is increasing rapidly due to high-throughput sequencing data and phylogenetic and molecular-cytogenetic approaches that make it possible to infer the evolutionary direction and steps leading from homomorphic to heteromorphic sex chromosomes. Here, we focus on four species of Coccinia, a genus of 25 dioecious species, including Coccinia grandis, the species with the largest known plant Y chromosome. Based on a phylogeny for the genus, we selected three species close to C. grandis to test the distribution of eight repetitive elements including two satellites, and several plastid and mitochondrial probes, that we had previously found to have distinct accumulation patterns in the C. grandis genome. Additionally, we determined C-values and performed immunostaining experiments with (peri-)centromere-specific antibodies on two species (for comparison with C. grandis). In spite of no microscopic chromosomal heteromorphism, single pairs of chromosomes in male cells of all three species accumulate some of the very same repeats that are enriched on the C. grandis Y chromosome, pointing to either old (previous) sex chromosomes or incipient (newly arising) ones, that is, to sex chromosome turnover. A 144-bp centromeric satellite repeat (CgCent) that characterizes all C. grandis chromosomes except the Y is highly abundant in all centromeric regions of the other species, indicating that the centromeric sequence of the Y chromosome diverged very recently.

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Abbreviations

BAC:

Bacterial artificial chromosome

FISH:

Fluorescent in situ hybridization

PCR:

Polymerase chain reaction

rDNA:

Ribosomal DNA

SDR:

Sex-determining region

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Acknowledgements

We thank Martina Silber for help in the lab, Andreas Houben and two anonymous reviewers for comments on the manuscript, and the German Science Foundation for funding (DFG RE-603/19-1).

Author information

Authors and Affiliations

  1. Department of Biology, University of Munich (LMU), 80638, Munich, Germany

    Aretuza Sousa & Susanne S. Renner

  2. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, 06466, Stadt Seeland, Germany

    Jörg Fuchs

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  1. Aretuza Sousa
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  2. Jörg Fuchs
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Correspondence to Aretuza Sousa or Susanne S. Renner.

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Responsible Editor: Hans de Jong.

Electronic supplementary material

Fig. S1.

Distribution of 5S and 45S rDNA and Arabidopsis-type telomere sequences on mitotic metaphase chromosomes of Coccinia hirtella (a–c), C. sessilifolia (d–i), and mitotic metaphase (j) and meiotic metaphase I (l, l) of C. trilobata, using FISH. Arrows point to chromosomes with weak 45S rDNA signals. The sex of each karyotype is indicated in the upper right-hand corner. Bars correspond to 5 μm and apply to all metaphases of a row (JPEG 486 kb)

Fig. S2.

Phylogenetic relationships of the studied Coccinia species modified from Holstein and Renner (2011). Red dots mark nodes with molecular-clock inferred divergence times, while the black dot marks the inferred age of the most recent common ancestor of all 25 living species of Coccinia (JPEG 137 kb)

Fig. S3.

Distribution of repeats in Coccinia grandis (e-h; from Sousa et al. 2016) and in C. sessilifolia, using fluorescence in situ hybridization. Compare Table 2 for probe names; an asterisk stands for Ty3/gypsy/, a § stands for Ty1/copia/. The sex of each karyotype is indicated in the upper right-hand corner. Bars correspond to 5 μm (JPEG 301 kb)

Fig. S4.

Distribution of repeats in Coccinia grandis (d-f; from Sousa et al. 2016) and in C. sessilifolia, using fluorescence in situ hybridization. Compare Table 2 for probe names; an asterisk stands for Ty3/gypsy/. Arrows in A point to two chromosomes enriched with the CL86 element. The sex of each karyotype is indicated in the upper right-hand corner. Bars correspond to 5 μm (JPEG 233 kb)

Fig. S5.

Distribution of a Coccinia grandis centromere repeat, called CgCent (CL1 in Table 2), in C. sessilifolia and C. hirtella, using fluorescence in situ hybridization. The arrow in C. grandis points to the Y chromosome. The sex of each karyotype is indicated in the upper right-hand corner. Bars correspond to 5 μm (JPEG 167 kb)

Fig. S6.

Distribution of plastid and mitochondrial sequences in mitotic metaphase chromosomes of Coccinia sessilifolia (a–c) and C. grandis (d-f; from Sousa et al. 2016). IR stands for inverted repeat and SSC for small single copy region. The sex of each karyotype is indicated in the upper right-hand corner. Bars correspond to 5 μm (JPEG 266 kb)

Fig. S7.

Immunostaining with antibodies against phosphorylated serine 10 of histone H3 (H3Ser10ph), and phosphorylated threonine 120 of histone H2A (H2AThr120ph) on mitotic metaphase chromosomes of Coccinia sessilifolia, C. hirtella, and C. grandis (e-f, from Sousa et al. 2016). Arrows in C. grandis point to its Y chromosome. The sex of each karyotype is indicated in the upper right-hand corner. Bars corresponds to 5 μm (JPEG 272 kb)

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Sousa, A., Fuchs, J. & Renner, S.S. Cytogenetic comparison of heteromorphic and homomorphic sex chromosomes in Coccinia (Cucurbitaceae) points to sex chromosome turnover. Chromosome Res 25, 191–200 (2017). https://doi.org/10.1007/s10577-017-9555-y

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