Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

R, Li; Ren, Xiaoliang; Bi, Yu; Ho, Vincy Wing Sze; Hsieh, Chia‐Ling; Young, Amanda; Zhang, Zhihong; Lin, Tao; Zhao, Yanmei; Liu, Miao; Sarkies, Peter; Zhao, Zhongying

doi:10.1101/gr.204479.116

Cited by 26 publications

(46 citation statements)

References 74 publications

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“…These observations suggest that the process of X inactivation in male meiosis would be especially sensitive to disruption in hybrids (“fragile male” hypothesis; Wu & Davis, ), potentially leading to hybrid male sterility. The limited available data are consistent with this idea, based on X‐linked introgression lines between C. briggsae and C. nigoni that implicates chromatin misregulation via small RNA pathways (Li et al., ).…”

Section: Exceptionalismmentioning

confidence: 79%

“…However, these experiments with homozygous introgressions of C. briggsae DNA inserted into a C. nigoni genomic background demonstrated that the X‐chromosome is associated with all of the male‐specific hybrid dysfunction in terms of fertility and viability (Bi et al., ). Spermatogenesis, in particular, is perturbed by these X‐linked introgressions and leads to incompatibility mediated by misregulation of small RNAs (Li et al., ). The biogenesis of this particular class of small RNA, known as 22G RNAs, involves post‐transcriptional processing of coding sequences with subsequent targeting and modulation of chromatin in conjunction with the CSR‐1 and other argonaute proteins (Claycomb, ).…”

Section: Molecular Evolution and The Large‐x Effectmentioning

confidence: 99%

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X exceptionalism in Caenorhabditis speciation

Cutter

2017

Molecular Ecology

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Speciation genetics research in diverse organisms shows the X-chromosome to be exceptional in how it contributes to "rules" of speciation. Until recently, however, the nematode phylum has been nearly silent on this issue, despite the model organism Caenorhabditis elegans having touched most other topics in biology. Studies of speciation with Caenorhabditis accelerated with the recent discovery of species pairs showing partial interfertility. The resulting genetic analyses of reproductive isolation in nematodes demonstrate key roles for the X-chromosome in hybrid male sterility and inviability, opening up new understanding of the genetic causes of Haldane's rule, Darwin's corollary to Haldane's rule, and enabling tests of the large-X effect hypothesis. Studies to date implicate improper chromatin regulation of the X-chromosome by small RNA pathways as integral to hybrid male dysfunction. Sexual transitions in reproductive mode to self-fertilizing hermaphroditism inject distinctive molecular evolutionary features into the speciation process for some species. Caenorhabditis also provides unique opportunities for analysis in a system with XO sex determination that lacks a Y-chromosome, sex chromosome-dependent sperm competition differences and mechanisms of gametic isolation, exceptional accessibility to the development process and rapid experimental evolution. As genetic analysis of reproductive isolation matures with investigation of multiple pairs of Caenorhabditis species and new species discovery, nematodes will provide a powerful complement to more established study organisms for deciphering the genetic basis of and rules to speciation.

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Section: Exceptionalismmentioning

confidence: 79%

Section: Molecular Evolution and The Large‐x Effectmentioning

confidence: 99%

X exceptionalism in Caenorhabditis speciation

Cutter

2017

Molecular Ecology

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“…Notably, the introgression spans the entire region of the second piRNA cluster on the C. briggsae Chromosome IV [45,46], which raises the possibility that incompatibility of these piRNAs between C. briggsae and C. nigoni that is responsible for the hybrid F1 inviability caused by crossing in both directions. Consistent with this notion is another piRNA cluster unique to C. briggsae on the Chromosome I [46]. The homozygosity of the region covering this cluster led to inviability in the hybrid F1 male and female progeny regardless of the parent of origin (Fig.…”

Section: Discussionmentioning

confidence: 99%

Genome wide screen reveals a specific interaction between autosome and X that is essential for hybrid male sterility

Zhao

Ren

et al. 2018

Preprint

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1Hybrid male progeny from interspecies cross are more prone to sterility or inviability than hybrid 2 female progeny, and the male sterility and inviability often demonstrate a parent-of-origin 3 asymmetry. However, the underlying mechanism of asymmetric sterility or inviability remains 4 elusive. We previously established a genome-wide hybrid incompatibility (HI) landscape between 5 Caenorhabditis briggsae and C. nigoni by phenotyping a large collection of C. nigoni strains each 6 carrying a C. briggsae introgression. In this study, we investigate the genetic mechanism of 7 asymmetric sterility and inviability in both hybrid male and female progeny between the two 8 species. Specifically, we performed reciprocal crosses between C. briggsae and different C. nigoni 9 strains that each carries a GFP-labeled C. briggsae genomic fragment referred to as introgression, 10 and scored the HI phenotypes in the F1 progeny. The aggregated introgressions cover 94.6% of 11 the C. briggsae genome, including 100% of the X chromosome. Surprisingly, we observed that 12 two C. briggsae X fragments that produce C. nigoni male sterility as an introgression rescued 13 hybrid F1 sterility in males fathered by C. briggsae, indicating that at least two separate X-14 autosome interactions are involved in the hybrid male sterility. In addition, we identified another 15 two C. briggsae genomic intervals on the Chromosome II or IV, respectively, which can rescue 16 the inviability, but not the sterility, of hybrid F1 males fathered by C. nigoni, suggesting the 17 involvement of differential epistatic interactions in the asymmetric hybrid male fertility and 18 inviability. Importantly, backcrossing of the rescued sterile males with C. nigoni led to isolation 19 of a 1.1-Mb genomic interval that specifically interacts with an X-linked introgression, which is 20 essential for hybrid male fertility. We further identified three C. briggsae genomic intervals on the 21 3 Chromosome I, II and III, respectively that produce inviability in all F1 progeny dependent or 1 independent of the parent-of-origin. Taken together, we identified multiple independent interacting 2 loci that are responsible for asymmetric hybrid male and female sterility and inviability, which 3 provides important insights into the asymmetric HI and lays a foundation for their molecular 4 characterization. 5 6 Author summary 7It is common that closely related species can mate with each other, but their hybrid progeny are 8 often sterile or inviable, especially in the male progeny. The mechanism underlying the 9 asymmetric sterility or inviability remains poorly understood. We previously addressed this 10 question between two nematodes, Caenorhabditis briggsae and C. nigoni, by systematic 11 substitution of various parts of the C. nigoni genome with its C. briggsae's equivalent followed by 12 phenotypic examination. Here we investigate the genetic mechanism of the asymmetric sterility 13 and inviability in the hybrid F1 male and female progeny between the two species. We achiev...

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“…Small RNAs perform multiple functions that are fundamental to genome stability, from gene expression regulation to heterochromatin assembly and dosage compensation – many of which have been reported as “broken down” in hybrids (previous section and [61]). The diverse functions of small RNAs have been extensively reviewed elsewhere [e.g.…”

Section: Mechanism 6: Small Rnas and Transposable Elementsmentioning

confidence: 99%

Beyond speciation genes: an overview of genome stability in evolution and speciation

Dion-Côté

Barbash

2017

Current Opinion in Genetics & Development

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Genome stability ensures individual fitness and reliable transmission of genetic information. Hybridization between diverging lineages can trigger genome instability, highlighting its potential role in post-zygotic reproductive isolation. We argue that genome instability is not merely one of several types of hybrid incompatibility, but rather that genome stability is one of the very first and most fundamental traits that can break down when two diverged genomes are combined. Future work will reveal how frequent and predictable genome instability is in hybrids, how it affects hybrid fitness, and whether it is a direct cause or consequence of speciation.

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Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Cited by 26 publications

References 74 publications

X exceptionalism in Caenorhabditis speciation

X exceptionalism in Caenorhabditis speciation

Genome wide screen reveals a specific interaction between autosome and X that is essential for hybrid male sterility

Beyond speciation genes: an overview of genome stability in evolution and speciation

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