Evolution of gene dosage on the Z-chromosome of schistosome parasites

Picard, Marion; Cosseau, Céline; Ferré, Sabrina; Quack, Thomas; Grevelding, Christoph G.; Couté, Yohann; Vicoso, Beatriz

doi:10.7554/elife.35684

Cited by 34 publications

(48 citation statements)

References 85 publications

(151 reference statements)

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“…Finally, analyses of chromosome-scale assemblies allowed us to explore the distribution of genetic features throughout the genome and to speculate on the evolutionary events that have taken place to explain these distributions. For example, between species analyses have confirmed karyotype structures and/or revealed chromosomal rearrangements among rhabditine nematodes [65,66] , filarial nematodes [11] , and platyhelminths [67] . The V4…”

Section: Discussionmentioning

confidence: 99%

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Doyle

Tracey

Laing

et al. 2020

Preprint

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Background Haemonchus contortus is a globally distributed and economically important gastrointestinal pathogen of small ruminants, and has become the key nematode model for studying anthelmintic resistance and other parasite-specific traits among a wider group of parasites including major human pathogens. Two draft genome assemblies for H. contortus were reported in 2013, however, both were highly fragmented, incomplete, and differed from one another in important respects. While the introduction of long-read sequencing has significantly increased the rate of production and contiguity of de novo genome assemblies broadly, achieving high quality genome assemblies for small, genetically diverse, outcrossing eukaryotic organisms such as H. contortus remains a significant challenge. ResultsHere, we report using PacBio long read and OpGen and 10X Genomics long-molecule methods to generate a highly contiguous 283.4 Mbp chromosome-scale genome assembly including a resolved sex chromosome. We show a remarkable pattern of almost complete conservation of chromosome content (synteny) with Caenorhabditis elegans , but almost no conservation of gene order. Long-read transcriptome sequence data has allowed us to define coordinated transcriptional regulation throughout the life cycle of the parasite, and refine our understanding of cisand trans -splicing relative to that observed in C. elegans .Finally, we use this assembly to give a comprehensive picture of chromosome-wide genetic diversity both within a single isolate and globally. ConclusionsThe H. contortus MHco3(ISE).N1 genome assembly presented here represents the most contiguous and resolved nematode assembly outside of the Caenorhabditis genus to date, together with one of the highest-quality set of predicted gene features. These data provide a high-quality comparison for understanding the evolution and genomics of Caenorhabditis and other nematodes, and extends the experimental tractability of this model parasitic nematode in understanding pathogen biology, drug discovery and vaccine development, and important adaptive traits such as drug resistance.

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Section: Discussionmentioning

confidence: 99%

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Doyle

Tracey

Laing

et al. 2020

Preprint

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“…The detection of many Z-specific genes in the older stratum allowed us to probe their expression and test for the presence of mechanisms of dosage compensation. While common in XY species, mechanisms that balance Z expression and lead to a full equalization of expression between males and females have only been found in Lepidoptera (but see Picard et al. 2018 for evidence that a similar mechanism may be evolving on the Z chromosome of schistosome parasites).…”

Section: Discussionmentioning

confidence: 99%

Sex-Biased Gene Expression and Dosage Compensation on theArtemia franciscanaZ-Chromosome

Huylmans

Toups

Macon

et al. 2019

Genome Biology and Evolution

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Males and females of Artemia franciscana , a crustacean commonly used in the aquarium trade, are highly dimorphic. Sex is determined by a pair of ZW chromosomes, but the nature and extent of differentiation of these chromosomes is unknown. Here, we characterize the Z chromosome by detecting genomic regions that show lower genomic coverage in female than in male samples, and regions that harbor an excess of female-specific SNPs. We detect many Z-specific genes, which no longer have homologs on the W, but also Z-linked genes that appear to have diverged very recently from their existing W-linked homolog. We assess patterns of male and female expression in two tissues with extensive morphological dimorphism, gonads, and heads. In agreement with their morphology, sex-biased expression is common in both tissues. Interestingly, the Z chromosome is not enriched for sex-biased genes, and seems to in fact have a mechanism of dosage compensation that leads to equal expression in males and in females. Both of these patterns are contrary to most ZW systems studied so far, making A. franciscana an excellent model for investigating the interplay between the evolution of sexual dimorphism and dosage compensation, as well as Z chromosome evolution in general.

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“…This implies that some genes are dosage sensitive (low heterozygote fitness or lethality) whereas others are less so. The lack of chromosome-wide dosage compensation and dosage balance has been documented in parasitic blood flukes, tonguefish, caenophidian snakes, birds, a trionychid turtle and the Komodo dragon, with lepidopteran insects and Artemia franciscana representing the only known exceptions here 6,11,15,16–18 and unpublished manuscript .…”

Section: Introductionmentioning

confidence: 95%

Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

Rovatsos

Gamble

Nielsen

et al. 2020

Preprint

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19Differentiation of sex chromosomes is thought to have evolved with cessation of 20 recombination and subsequent loss of genes from the degenerated partner (Y and W) of sex 21 chromosomes, which in turn leads to imbalance of gene dosage between sexes. Based on 22 work with traditional model species, theory suggests that unequal gene copy numbers lead to 23 the evolution of mechanisms to counter this imbalance. Dosage compensation, or at least 24 achieving dosage balance in expression of sex-linked genes between sexes, has largely been 25 documented in lineages with male heterogamety (XX/XY sex determination), while ZZ/ZW 26 systems are assumed to be usually associated with the lack of chromosome-wide gene dose 27 regulatory mechanisms. Here we document that although the pygopodid geckos evolved male 28 heterogamety with a degenerated Y chromosome 32-72 million years ago, one species in 29 particular, Burton's legless lizard (Lialis burtonis), does not possess dosage balance in the 30 expression of genes in its X-specific region. We summarize studies on gene dose regulatory 31 mechanisms in animals and conclude that there is in them no significant dichotomy between 32 male and female heterogamety. We speculate that gene dose regulatory mechanisms are likely 33 to be related to the general mechanisms of sex determination instead of type of heterogamety. 34Differentiated sex chromosomes evolved independently in numerous animal and plant 36 lineages 1 . The differentiation is connected with cessation of recombination and subsequent 37 loss of functional genes from the Y or W sex chromosomes which leads to gene dose 38 differences between sexes. Selection will favour the evolution of mechanisms that regulate 39 these differences at the cellular level, as alterations in gene copy number generally alters gene 40 expression, ultimately impacting cell physiology and organismal fitness 2-5 . Different taxa 41 have evolved distinct strategies to regulate the unequal gene copy numbers and the associated 42 gene dosage imbalances between the sexes related to differentiated sex chromosomes 6 . The 43 most well-known mechanism is dosage compensation, which restores the expression of X or 44 Z-specific genes in the heterogametic sex to the ancestral expression levels 7-9 . Dosage 45 compensation usually leads to dosage balance, i.e. equal expression levels of the X or Z-46 specific genes between the sexes, however some animal lineages can reach dosage balance in 47 the expression between sexes without keeping the ancestral expression level. Other animal 48 lineages do not compensate and balance expression in the majority of the sex-linked genes at 49 either the level of transcription or translation 10,11 . Dosage compensation or at least dosage 50 balance between sexes was documented largely in lineages with male heterogamety (XX/XY 51 sex determination) such as in several insect lineages, nematode worms, the green anole and 52 eutherian mammals, with sticklebacks, basilisks and platypus being exceptions 6,12,13 . On the 53 ...

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Evolution of gene dosage on the Z-chromosome of schistosome parasites

Cited by 34 publications

References 85 publications

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Extensive genomic and transcriptomic variation defines the chromosome-scale assembly ofHaemonchus contortus, a model gastrointestinal worm

Sex-Biased Gene Expression and Dosage Compensation on theArtemia franciscanaZ-Chromosome

Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

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