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Unique sequence organization and small RNA expression of a “selfish” B chromosome

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An Erratum to this article was published on 19 August 2017

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Abstract

B chromosomes are found in numerous plants and animals. These nonessential, supernumerary chromosomes are often composed primarily of noncoding DNA repeats similar to those found within transcriptionally “silenced” heterochromatin. In order to persist within their resident genomes, many B chromosomes exhibit exceptional cellular behaviors, including asymmetric segregation into gametes and induction of genome elimination during early development. An important goal in understanding these behaviors is to identify unique B chromosome sequences and characterize their transcriptional contributions. We investigated these properties by examining a paternally transmitted B chromosome known as paternal sex ratio (PSR), which is present in natural populations of the jewel wasp Nasonia vitripennis. To facilitate its own transmission, PSR severely biases the sex ratio by disrupting early chromatin remodeling processes. Through cytological mapping and other approaches, we identified multiple DNA repeats unique to PSR, as well as those found on the A chromosomes, suggesting that PSR arose through a merger of sequences from both within and outside the N. vitripennis genome. The majority of PSR-specific repeats are interspersed among each other across PSR’s long arm, in contrast with the distinct “blocks” observed in other organisms’ heterochromatin. Through transcriptional profiling, we identified a subset of repeat-associated, small RNAs expressed by PSR, most of which map to a single PSR-specific repeat. These RNAs are expressed at much higher levels than those arising from A chromosome-linked repeats, suggesting that in addition to its sequence organization, PSR’s transcriptional properties differ substantially from the pericentromeric regions of the normal chromosomes.

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  • 19 August 2017

    An erratum to this article has been published.

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Authors and Affiliations

  1. Key Laboratory of Stem Cell Biology Institute of Health Sciences, Shanghai Institute for Biological Science, Chinese Academy of Sciences and Shanghai Jiao-Tong University School of Medicine, 320 Yue-Yang Road, Shanghai, 200031, China

    Yue Li & Jian Chen

  2. W. M. Keck Science Department, Claremont McKenna, Pitzer, and Scripps Colleges, 925 N. Mills Avenue, Claremont, CA, 91711, USA

    Xueyuan A. Jing, John C. Aldrich, C. Clifford & Patrick M. Ferree

  3. Department of Entomology and Riverside Center for Disease Vector Research, Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, 92521, USA

    Omar S. Akbari

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  1. Yue Li
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  2. Xueyuan A. Jing
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  4. C. Clifford
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  5. Jian Chen
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  6. Omar S. Akbari
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  7. Patrick M. Ferree
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Correspondence to Patrick M. Ferree.

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Funding

This work was funded by a USDA National Institute of Food and Agriculture (NIFA) Hatch Project grant (1009509) to O. S. A. and a US National Science Foundation CAREER award (NSF-1451839) to P.M.F.

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All authors declare that they have no conflict of interest.

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This article does not present any studies with human participants or animals performed by any of the authors.

Additional information

The original version of this article was revised: During the steps of corrections, the author name “Omar A. Akbari” went wrong. The corrected author name is shown above.

An erratum to this article is available at https://doi.org/10.1007/s00412-017-0642-9.

Electronic supplementary material

Fig. S1

The PSR chromosome contains abundant copies of repeats that are also present on the A chromosomes. DNA FISH shows that NV79 and NV126 (both in red) are present on a single A chromosome that uniquely contains PSR104 (green). (GIF 85 kb)

High Resolution Image (TIFF 591 kb)

Fig. S2

DNA FISH shows that PSR harbors repeats (PSR4656 and PSR8495) that generate polyadenylated transcripts. These repeats co-localize across PSR’s long arm, and are not detectable on the A chromosomes using this method. (GIF 65 kb)

High Resolution Image (TIFF 497 kb)

Fig. S3

PSR-specific repeats generate small RNAs at levels much higher than those expressed by repeats in the PSR(−) genome. Levels of small RNAs from A chromosome repeats and PSR-specific repeats are shown in grey and red, respectively. The Y axis portrays the total amount of small RNA traces per repeat in the testis. (GIF 15 kb)

High Resolution Image (TIFF 219 kb)

Fig. S4

Depiction of small RNAs deriving from PSR105. (A) Alignment of small RNAs corresponding to PSR105 (red text). (B) The canonical PSR105 repeat is shown, with the sequence of the corresponding small RNAs (highlighted in red text). The two highly conserved palindromic regions of this repeat are underlined. (C) A long RNA precursor for the PSR105-matching small RNAs is shown, with the region generating the small RNAs highlighted in red, and the complementary region shown in black underline. This RNA is predicted to form an imperfect hairpin (below arrow). The region matching to the small RNAs is marked by a red line. (GIF 356 kb)

High Resolution Image (TIFF 2202 kb)

Fig. S5

Depiction of small RNAs deriving from PSR2. (A) Alignment of small RNAs corresponding to PSR2 (red text). These RNAs form two distinct ‘clusters.’ (B) The canonical PSR2 repeat is shown, with the sequences of the corresponding small RNAs (highlighted in green text and underlined in blue). The two highly conserved palindromic regions of this repeat are underlined). (C) Two long RNA precursors for the PSR2-matching small RNAs are shown, with the region generating each cluster of small RNAs heighted in green and blue, respectively. Each of these RNAs is predicted to form hairpin structures (shown below each arrow). The regions matching to the small RNAs are marked by either a green or a blue line. (GIF 299 kb)

High Resolution Image (TIFF 1511 kb)

Fig. S6

Control conditions for RNA FISH of the 4317 transcript. Top row depicts PSR4317 probe hybridization to PSR(−) testes, resulting in no signal. Similarly, no signal results from hybridization of this same probe to PSR(+) testes pre-treated with RNase A (bottom row). Only the PSR(+) untreated testes show punctate hybridization signals with this probe. (GIF 434 kb)

High Resolution Image (TIFF 3490 kb)

Fig. S7

Large nuclei in the N. vitripennis testis are polyploid. (A) The large nuclei show multiple, distinct foci of PSR22, in addition to rDNA located at a single locus on an A chromosome. Nuclei of cyst cells following S-phase (B) and mature sperm (C) have exactly two foci and one focus, respectively, of PSR22 and rDNA. (GIF 89 kb)

High Resolution Image (TIFF 649 kb)

Table S1

Identification of a new PSR-specific transcript from unfiltered total RNA (XLSX 11 kb)

Table S2

miRNAs, siRNAs, and rasi−/putative piRNAs identified from N. vitripennis testis and carcass (somatic tissues) of PSR(−) and PSR(+) males. Each of these small RNA classes is shown in a separate tab. (XLSX 103 kb)

Table S3

Additional information for N. vitripennis miRNAs and piRNAs. (XLSX 159 kb)

Table S4

Small RNAs that are exclusive to the PSR(+) genotype. (XLSX 72 kb)

Table S5

Putative precursor RNAs for small RNAs derived from PSR repeats PSR2, PSR22, and PSR105. (XLSX 47 kb)

Table S6

Oligonucleotides used for DNA FISH (XLSX 89 kb)

Table S7

Oligonucleotides used for PCR (XLSX 112 kb)

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Li, Y., Jing, X.A., Aldrich, J.C. et al. Unique sequence organization and small RNA expression of a “selfish” B chromosome. Chromosoma 126, 753–768 (2017). https://doi.org/10.1007/s00412-017-0641-x

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