Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression
- Runsheng Li1,7,
- Xiaoliang Ren1,7,
- Yu Bi1,
- Vincy Wing Sze Ho1,
- Chia-Ling Hsieh2,
- Amanda Young2,
- Zhihong Zhang2,
- Tingting Lin3,
- Yanmei Zhao3,
- Long Miao3,
- Peter Sarkies4,5 and
- Zhongying Zhao1,6
- 1Department of Biology, Hong Kong Baptist University, Hong Kong, China;
- 2Illumina Incorporated, San Diego, California 92122, USA;
- 3Institute of Biophysics, Chinese Academy of Sciences, Beijing 100190, China;
- 4MRC Clinical Sciences Centre, London W12 0NN, United Kingdom;
- 5Institute of Clinical Sciences, Imperial College London, London SW7 2AZ, United Kingdom;
- 6State Key Laboratory of Environmental and Biological Analysis, Hong Kong Baptist University, Hong Kong, China
- Corresponding authors: p.sarkies{at}csc.mrc.ac.uk, zyzhao{at}hkbu.edu.hk
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↵7 These authors contributed equally to this work.
Abstract
Hybrid incompatibility (HI) prevents gene flow between species, thus lying at the heart of speciation genetics. One of the most common HIs is male sterility. Two superficially contradictory observations exist for hybrid male sterility. First, an introgression on the X Chromosome is more likely to produce male sterility than on autosome (so-called large-X theory); second, spermatogenesis genes are enriched on the autosomes but depleted on the X Chromosome (demasculinization of X Chromosome). Analysis of gene expression in Drosophila hybrids suggests a genetic interaction between the X Chromosome and autosomes that is essential for male fertility. However, the prevalence of such an interaction and its underlying mechanism remain largely unknown. Here we examine the interaction in nematode species by contrasting the expression of both coding genes and transposable elements (TEs) between hybrid sterile males and its parental nematode males. We use two lines of hybrid sterile males, each carrying an independent introgression fragment from Caenorhabditis briggsae X Chromosome in an otherwise Caenorhabditis nigoni background, which demonstrate similar defects in spermatogenesis. We observe a similar pattern of down-regulated genes that are specific for spermatogenesis between the two hybrids. Importantly, the down-regulated genes caused by the X Chromosome introgressions show a significant enrichment on the autosomes, supporting an epistatic interaction between the X Chromosome and autosomes. We investigate the underlying mechanism of the interaction by measuring small RNAs and find that a subset of 22G RNAs specifically targeting the down-regulated spermatogenesis genes is significantly up-regulated in hybrids, suggesting that perturbation of small RNA-mediated regulation may contribute to the X-autosome interaction.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.204479.116.
- Received January 18, 2016.
- Accepted May 16, 2016.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
