Genomic basis of recombination suppression in the hybrid between Caenorhabditis briggsae and C. nigoni

Ren, Xiaoliang; R, Li; Wei, Xiaolin; Bi, Yu; Ho, Vincy Wing Sze; Ding, Qiutao; Xu, Zhichao; Zhang, Zhihong; Hsieh, Chia‐Ling; Young, Amanda; Zeng, Jianyang; Liu, Xiao; Zhao, Zhongying

doi:10.1093/nar/gkx1277

Cited by 34 publications

(43 citation statements)

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“…As a biomedical model organism, the free-living soil nematode Caenorhabditis elegans is the first model nematode, and the first eukaryotic animal ever had its whole genome sequenced (The Caenorhabditis elegans Sequencing Consortium 1998). Other free-living nematodes had their genome sequenced subsequently in the last two decades (Stein et al 2003;Dieterich et al 2008;Kanzaki et al 2018;Ren et al 2018;Yin et al 2018;Stevens et al 2019;Weinstein et al 2019). Aside from C. elegans, Pristionchus pacificus is the only satellite model nematode with advanced functional genomic resources, bioinformatics and genetic tools (Rödelsperger et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Xie

Zhang

Xue

et al. 2020

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Nematodes play key roles in marine ecosystem. Although oceans cover 71% of the Earth's surface, none of marine model nematode has been reported. Here, we constructed the first inbred line of free-living marine nematode Litoditis marina, sequenced and assembled its genome. Furthermore, we successfully applied CRISPR/Cas9 genome editing in L. marina.Comparative genomics revealed that immunity and oxygen regulation genes are expanded, which is probably central to its sediment adaptation. While L. marina exhibits massive gene contractions in NHRs, chemoreceptors, xenobiotics detoxification and core histones, which could explain the more defined marine environment. Our experiments showed that dozens of H4 genes in Caenorhabditis elegans might contribute to its adaptation to the complex terrestrial environments, while two H4 genes in L. marina are involved in salinity stress adaptation. Additionally, ninety-two conserved genes appear to be positively selected in L. marina, which may underpin its osmotic, neuronal and epigenetic changes in the sea. With short generation time, highly inbred lines, and genomic resources, our report brings L. marina a promising marine animal model, and a unique satellite marine model to the wellknown biomedical model nematode C. elegans. This study will underpin ongoing work on animal functional genomics, environmental adaptation and developmental evolution. 4 marine nematodes have had their genomes sequenced and analysed (International Helminth Genomes Consortium 2019; Smythe et al. 2019; Weinstein et al. 2019). Oceans cover 71% of the Earth's surface, and represents almost 99% of available habitat, which are a key element for the existence and evolution of life (Robert 1999; Peng et al. 2020). In marine sediments, free-living nematodes abound both in numbers and in local species diversity, comprising about 80% of the abundance of meiofauna (Heip et al. 1985; Danovaro et al. 2010; Nascimento et al. 2012), they play a key role in the benthic food web and ecosystem. However, the study of marine nematodes is largely limited to taxonomy and ecology (De Meester et al. 2016; Derycke et al. 2016). Molecular mechanisms underlying their evolution, development regulation and adaptation mechanisms are rarely reported, and none of marine model nematode has been reported. The bacterivorous marine nematode Litoditis marina (Bastian, 1865) Sudhaus, 2011, formerly known as Rhabditis marina or Pellioditis marina, is found widely distributed in the littoral zone of coasts and estuaries of European, American, African and Asian countries, and play an important role in these marine ecosystems (Tietjen et al. 1970; Kito 1981; Houthoofd et al. 2003; Derycke et al. 2016). In addition, the embryonic cell lineage of L. marina has been reported by Houthoofd et al. (2003). In comparison with C. elegans, the overall L. marina lineage homology is 95.5%, whereas the fate homology is only 76.4%, and most of the differences in fate homology concern nervous, epidermal, and pharyngeal tissues, suggesting that L. marina wil...

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Section: Introductionmentioning

confidence: 99%

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Xie

Zhang

Xue

et al. 2020

Preprint

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“…The publication of the C. briggsae genome in 2003 enabled the first comparative genomics studies of Caenorhabditis, which revealed an unusually high rate of intrachromosomal rearrangement but comparatively rare interchromosomal rearrangement (Stein et al 2003). Additional genome sequences have been published from species across the genus (Mortazavi et al 2010;Fierst et al 2015;Slos et al 2017;Kanzaki et al 2018;Ren et al 2018;Yin et al 2018). Comparisons between genomes of hermaphroditic species such as C. elegans and their outcrossing relatives have exposed the genomic consequences of a switch in reproductive mode from gonochorism to autogamous hermaphroditism, including changes in overall genome structure, gene structure, and protein-coding gene content (Thomas et al 2012;Fierst et al 2015;Kanzaki et al 2018;Yin et al 2018).…”

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Comparative genomics of 10 newCaenorhabditisspecies

et al. 2019

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The nematode Caenorhabditis elegans has been central to the understanding of metazoan biology. However, C. elegans is but one species among millions and the significance of this important model organism will only be fully revealed if it is placed in a rich evolutionary context. Global sampling efforts have led to the discovery of over 50 putative species from the genus Caenorhabditis , many of which await formal species description. Here, we present species descriptions for 10 new Caenorhabditis species. We also present draft genome sequences for nine of these new species, along with a transcriptome assembly for one. We exploit these whole‐genome data to reconstruct the Caenorhabditis phylogeny and use this phylogenetic tree to dissect the evolution of morphology in the genus. We reveal extensive variation in genome size and investigate the molecular processes that underlie this variation. We show unexpected complexity in the evolutionary history of key developmental pathway genes. These new species and the associated genomic resources will be essential in our attempts to understand the evolutionary origins of the C. elegans model.

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“…Intriguingly, Drosopphila genes translocated from autosome to the Y Chromosome are undergoing rapid degeneration and pseudogenization, suggesting a differential selection pressure of bidirectional gene translocation between the autosome and the X Chromosome. Given that the size of the hermaphroditic C. briggsae genome is substantially smaller than that of the dioecious C. nigoni and [41,42], and other Caenorhabditis species [43], it remains to be determined whether differential gene translocation exists between the X Chromosome and the autosomes between the two species, which is responsible for the observed X-autosome interaction.…”

Section: Discussionmentioning

confidence: 99%

“…Rescue of the male sterility caused by zzyIR10330 would be indicative of the two loci. It is worth noting that the genomic sequences between C. briggsae and C. nigoni diverge substantially from each other in both sequence identity and size [41,44], which significantly inhibits DNA recombination frequency. Selective loss of male-specific genes in hermaphroditic species and its subsequent reinforcement further complicates the precise mapping of HI loci using backcrossing.…”

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

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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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Genomic basis of recombination suppression in the hybrid between Caenorhabditis briggsae and C. nigoni

Cited by 34 publications

References 48 publications

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Comparative genomics of 10 newCaenorhabditisspecies

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

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