X-chromosome silencing in the germline of<i>C. elegans</i>

Kelly, William G.; Schaner, Christine E; Dernburg, Abby F.; Lee, Minho; Kim, Stuart K.; Villeneuve, Anne M.; Reinke, V

doi:10.1242/dev.129.2.479

Cited by 292 publications

(45 citation statements)

References 57 publications

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“…More specifically, the 'out of the X' pattern for retrogenes was found to be only started after eutherian lineages were split, which was taken as evidence for the origin of MSCI in the eutherian ancestor [14]. Similar patterns of precocious silencing of X-linked genes in spermatocytes have also been reported in C. elegans [15] and Drosophila [16] by cytogenetic or transgenic studies. A second factor is the sexually antagonistic selection that is also expected to drive nascent male-biased genes off the female-biasedly transmitted X chromosome [17].…”

Section: Introductionsupporting

confidence: 59%

On the Origin and Evolution of Drosophila New Genes during Spermatogenesis

Zhou

2021

Genes

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The origin of functional new genes is a basic biological process that has significant contribution to organismal diversity. Previous studies in both Drosophila and mammals showed that new genes tend to be expressed in testes and avoid the X chromosome, presumably because of meiotic sex chromosome inactivation (MSCI). Here, we analyze the published single-cell transcriptome data of Drosophila adult testis and find an enrichment of male germline mitotic genes, but an underrepresentation of meiotic genes on the X chromosome. This can be attributed to an excess of autosomal meiotic genes that were derived from their X-linked mitotic progenitors, which provides direct cell-level evidence for MSCI in Drosophila. We reveal that new genes, particularly those produced by retrotransposition, tend to exhibit an expression shift toward late spermatogenesis compared with their parental copies, probably due to the more intensive sperm competition or sexual conflict. Our results dissect the complex factors including age, the origination mechanisms and the chromosomal locations that influence the new gene origination and evolution in testes, and identify new gene cases that show divergent cell-level expression patterns from their progenitors for future functional studies.

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Section: Introductionsupporting

confidence: 59%

On the Origin and Evolution of Drosophila New Genes during Spermatogenesis

Zhou

2021

Genes

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“…While most X-linked genes are repressed during germline proliferation and spermatogenesis, some are normally turned-on during oogenesis (Kelly et al, 2002; Arico et al, 2011; Tzur et al, 2018, Figure 1—figure supplement 2E). We examined whether X-linked UP genes are those that are normally turned-on during oogenesis by comparing our set of X-linked UP genes to a set of ‘oogenesis’ genes, defined as 470 X-linked and 1201 autosomal genes that are expressed at higher levels in dissected adult oogenic germlines than in dissected spermatogenic germlines (Ortiz et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

“…In contrast, some mes-4 mutant males that inherited their single X from an oocyte (X oo males) had either partial or full germlines (21% and 4%, respectively). Since X chromosomes turn on during oogenesis (Kelly et al, 2002; Arico et al, 2011; Tzur et al, 2018, Figure 1—figure supplement 2E), X oo males inherited an X with a history of expression. Using a him-8 mutant, we generated wild-type and mes-4 mutant males that instead inherited their X from a sperm (X sp males), which has a history of repression because the X was not turned on previously during spermatogenesis.…”

Section: Resultsmentioning

confidence: 99%

“…Second, profiling transcripts in the gonads of fertile mes-4 M+Z- mutant hermaphrodites revealed that the most dramatic effect of losing zygotic MES-4 is up-regulation of genes on the X (Bender et al, 2006; Gaydos et al, 2012). Notably, the X chromosomes are normally kept globally repressed during all stages of germline development in males and during most stages of germline development in hermaphrodites (Kelly et al, 2002; Reinke et al, 2004; Wang et al, 2009, Arico et al, 2011; Strome et al, 2014; Tzur et al, 2018), and likely as a consequence, most germline-expressed genes are located on the autosomes. These findings focused attention on the X chromosome and raised the question – what role does maternal MES-4 serve to ensure that PGCs survive and develop into a full and healthy germline?…”

Section: Introductionmentioning

confidence: 99%

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Maternal H3K36 and H3K27 HMTs protect germline immortality via regulation of the transcription factor LIN-15B

Cockrum

Strome

2022

Preprint

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Maternally synthesized products play critical roles in development of offspring. A premier example is the C. elegans H3K36 methyltransferase MES-4, which is essential for germline survival and development in offspring. How maternal MES-4 protects germline immortality is not well understood, but its role in H3K36 methylation hinted that it may regulate gene expression in Primordial Germ Cells (PGCs). We tested this hypothesis by profiling transcripts from single pairs of PGCs dissected from wild-type and mes-4 mutant (lacking maternal and zygotic MES-4) newly hatched larvae. We found that mes-4 PGCs display normal turn-on of most germline genes and normal repression of somatic genes, but dramatically up-regulate hundreds of genes on the X chromosome. We demonstrated that X mis-expression is the cause of germline death by generating and analyzing mes-4 mutants that inherited different endowments of X chromosome(s). Intriguingly, removal of the THAP transcription factor LIN-15B from mes-4 mutants reduced X mis-expression and prevented germline death. lin-15B is X-linked and mis-expressed in mes-4 PGCs, identifying it as a critical target for MES-4 repression. The above findings extend to the H3K27 methyltransferase MES-2/3/6, the C. elegans version of Polycomb Repressive Complex 2. We propose that maternal MES-4 and PRC2 cooperate to protect germline survival by preventing synthesis of germline-toxic products encoded by genes on the X chromosome, including the key transcription factor LIN-15B.

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“…The extent of dosage compensation may also differ by tissue type, with reduced dosage compensation observed in the reproductive tracts of e.g. C. elegans (Kelly et al ., 2002; Pirrotta, 2002) or D. melanogaster (Oliver, 2002; Meiklejohn et al ., 2011; Mahadevaraju et al ., 2021). However, it is not clear how widespread tissue-specific dosage compensation is, as work in non-model species often use whole-body samples for examining expression (Gu & Walters, 2017).…”

Section: Introductionmentioning

confidence: 99%

X chromosomes show relaxed selection and complete somatic dosage compensation acrossTimemastick insect species

Parker

Jaroň

Dumas

et al. 2021

Preprint

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Sex chromosomes have evolved repeatedly across the tree of life. As they are present in different copy numbers in males and females, they are expected to experience different selection pressures than the autosomes, with consequences including a faster rate of evolution, increased accumulation of sexually antagonistic alleles, and the evolution of dosage compensation. Whether these consequences are general or linked to idiosyncrasies of specific taxa is not clear as relatively few taxa have been studied thus far. Here we use whole-genome sequencing to identify and characterize the evolution of the X chromosome in five species of Timema stick insects with XX:X0 sex determination. The X chromosome had a similar size (approximately 11% of the genome) and gene content across all five species, suggesting that the X chromosome originated prior to the diversification of the genus. Genes on the X showed evidence of a faster evolutionary rate than genes on the autosomes, likely due to less effective purifying selection. Genes on the X also showed almost complete dosage compensation in somatic tissues (heads and legs), but dosage compensation was absent in the reproductive tracts. Contrary to prediction, sex-biased genes showed little enrichment on the X, suggesting that the advantage X-linkage provides to the accumulation of sexually antagonistic alleles is weak. Overall, we found the consequences of X-linkage on gene sequences and expression to be similar across Timema species, showing the characteristics of the X chromosome are surprisingly consistent over 30 million years of evolution.

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X-chromosome silencing in the germline ofC. elegans

Cited by 292 publications

References 57 publications

On the Origin and Evolution of Drosophila New Genes during Spermatogenesis

On the Origin and Evolution of Drosophila New Genes during Spermatogenesis

Maternal H3K36 and H3K27 HMTs protect germline immortality via regulation of the transcription factor LIN-15B

X chromosomes show relaxed selection and complete somatic dosage compensation acrossTimemastick insect species

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