Germ granules and the control of mRNA translation

Sengupta, Madhu S.; Boag, Peter R.

doi:10.1002/iub.1039

Cited by 30 publications

(39 citation statements)

References 63 publications

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“…Interestingly, in the case of germ plasm, transcription factors are unlikely to have been key players in the mechanisms of evolutionary change for a number of reasons. First, regulation of germ line determinants is largely post-transcriptional (Arkov and Ramos, 2010; Richter and Lasko, 2011; Sengupta and Boag, 2012; Nousch and Eckmann, 2013). Second, germ plasm transcript function relies on their subcellular localisation (often mediated via signals in their 3′UTRs) rather than their presence or absence (Rangan et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Evidence against a germ plasm in the milkweed bugOncopeltus fasciatus, a hemimetabolous insect

2013

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SummaryPrimordial germ cell (PGC) formation in holometabolous insects like Drosophila melanogaster relies on maternally synthesised germ cell determinants that are asymmetrically localised to the oocyte posterior cortex. Embryonic nuclei that inherit this “germ plasm” acquire PGC fate. In contrast, historical studies of basally branching insects (Hemimetabola) suggest that a maternal requirement for germ line genes in PGC specification may be a derived character confined principally to Holometabola. However, there have been remarkably few investigations of germ line gene expression and function in hemimetabolous insects. Here we characterise PGC formation in the milkweed bug Oncopeltus fasciatus, a member of the sister group to Holometabola, thus providing an important evolutionary comparison to members of this clade. We examine the transcript distribution of orthologues of 19 Drosophila germ cell and/or germ plasm marker genes, and show that none of them localise asymmetrically within Oncopeltus oocytes or early embryos. Using multiple molecular and cytological criteria, we provide evidence that PGCs form after cellularisation at the site of gastrulation. Functional studies of vasa and tudor reveal that these genes are not required for germ cell formation, but that vasa is required in adult males for spermatogenesis. Taken together, our results provide evidence that Oncopeltus germ cells may form in the absence of germ plasm, consistent with the hypothesis that germ plasm is a derived strategy of germ cell specification in insects.

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Section: Discussionmentioning

confidence: 99%

Evidence against a germ plasm in the milkweed bugOncopeltus fasciatus, a hemimetabolous insect

2013

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“…In the adult germline, they act to maintain totipotency by repressing somatic cell fate via an unknown mechanism. Most P-granule-associated proteins identified to date contain RNA-binding domains or are known regulators of translation, suggesting that P granules act post-transcriptionally to maintain germline pluripotency [reviewed by Sengupta and Boag (2012)]. When P granules are impaired in the adult germline, germ cells lose pluripotency, and a fraction initiate somatic reprogramming (Updike et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

Campbell

Updike

2015

Development

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Germ granules (P granules) in C. elegans are required for fertility and function to maintain germ cell identity and pluripotency. Sterility in the absence of P granules is often accompanied by the misexpression of soma-specific proteins and the initiation of somatic differentiation in germ cells. To investigate whether this is caused by the accumulation of somatic transcripts, we performed mRNA-seq on dissected germlines with and without P granules. Strikingly, we found that somatic transcripts do not increase in the young adult germline when P granules are impaired. Instead, we found that impairing P granules causes sperm-specific mRNAs to become highly overexpressed. This includes the accumulation of major sperm protein (MSP) transcripts in germ cells, a phenotype that is suppressed by feminization of the germline. A core component of P granules, the endo-siRNA-binding Argonaute protein CSR-1, has recently been ascribed with the ability to license transcripts for germline expression. However, impairing CSR-1 has very little effect on the accumulation of its mRNA targets. Instead, we found that CSR-1 functions with P granules to prevent MSP and sperm-specific mRNAs from being transcribed in the hermaphrodite germline. These findings suggest that P granules protect germline integrity through two different mechanisms, by (1) preventing the inappropriate expression of somatic proteins at the level of translational regulation, and by (2) functioning with CSR-1 to limit the domain of sperm-specific expression at the level of transcription.

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“…The exact function of RNP granules is not entirely understood, but they are likely key players in the posttranscriptional regulation of gene expression throughout the eukaryotic kingdom with functions in mRNA degradation, storage, sorting, and transport. Animal germ granules play an essential role during early development, a time, when transcription is absent and cells rely entirely on maternal mRNAs . They are likely to regulate translational repression, activation, and transport of maternal mRNAs in a timed and spatial way to enable accurate early embryogenesis.…”

Section: Introductionmentioning

confidence: 99%

RNA in development: how ribonucleoprotein granules regulate the life cycles of pathogenic protozoa

Krämer

2013

WIREs RNA

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Ribonucleoprotein (RNP) granules are important posttranscriptional regulators of messenger RNA (mRNA) fate. Several types of RNP granules specifically regulate gene expression during development of multicellular organisms and are commonly referred to as germ granules. The function of germ granules is not entirely understood and probably diverse, but it is generally agreed that one main function is posttranscriptional regulation of gene expression during early development, when transcription is silent. One example is the translational repression of maternally derived mRNAs in oocytes. Here, I hope to show that the need for regulation of gene expression by RNP granules is not restricted to animal development, but plays an equally important role during the development of pathogenic protozoa. Apicomplexa and Trypanosomatidae have complex life cycles with frequent host changes. The need to quickly adapt gene expression to a new environment as well as the ability to suppress translation to survive latencies is critical for successful completion of life cycles. Posttranscriptional gene regulation is not necessarily simpler in protozoa. Apicomplexa surprise with the presence of micro RNA (miRNAs) and upstream open reading frames (µORFs). Trypanosomes have an unusually large repertoire of different RNP granule types. A better understanding of RNP granules in protozoa may help to gain insight into the evolutionary origin of RNP granules: Trypanosomes for example have two types of granules with interesting similarities to animal germ granules.

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Germ granules and the control of mRNA translation

Cited by 30 publications

References 63 publications

Evidence against a germ plasm in the milkweed bugOncopeltus fasciatus, a hemimetabolous insect

Evidence against a germ plasm in the milkweed bugOncopeltus fasciatus, a hemimetabolous insect

CSR-1 and P granules suppress sperm-specific transcription in theC. elegansgermline

RNA in development: how ribonucleoprotein granules regulate the life cycles of pathogenic protozoa

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