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Transpositional shuffling and quality control in male germ cells to enhance evolution of complex organisms.

Werner A, Piatek MJ, Mattick JS - Ann. N. Y. Acad. Sci. (2014)

Bottom Line: This reduces the ability of such organisms to explore evolutionary space, and, consequently, strategies that mitigate this problem likely have a strategic advantage.Cells that fail the genomic quality test are excluded from further development, eventually resulting in a positively selected mature sperm population.We suggest that these processes, enhanced variability and stringent molecular quality control, compensate for the apparent reduced potential of complex animals to adapt and evolve.

View Article: PubMed Central - PubMed

Affiliation: RNA Biology Group, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle, United Kingdom.

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Schematic representation of spermatogenesis. The timing of developmental processes relevant to transposon derepression and resilencing are indicated in the lower panels. Accordingly, TEs undergo a first round of derepression during fetal germ cell differentiation that triggers piRNA expression and de novo DNA remethylation. This course of events is thought to be specific for animals, because piRNAs are only found in the animal kingdom. In mammals, a second round of TE derepression initiates at the mitotic phase as a consequence of either active or passive genome-wide demethylation. The relaxation of repressive chromatin marks enables transposition but also triggers a wave of transcription that promotes sense/antisense RNA expression and the synthesis of pachytene piRNAs. We propose that the majority of the transcripts are stored in the chromatoid body (indicated in round and elongated spermatids). siRNA (and piRNA)–Argonaute complexes (RISCs) search for their complementary target RNAs in the chromatoid body (CB) if the corresponding transcript is present; if the target RNA is not found in the CB, the RISCs enter the nucleus to interfere with the maturation process of the spermatid.
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Figure 1: Schematic representation of spermatogenesis. The timing of developmental processes relevant to transposon derepression and resilencing are indicated in the lower panels. Accordingly, TEs undergo a first round of derepression during fetal germ cell differentiation that triggers piRNA expression and de novo DNA remethylation. This course of events is thought to be specific for animals, because piRNAs are only found in the animal kingdom. In mammals, a second round of TE derepression initiates at the mitotic phase as a consequence of either active or passive genome-wide demethylation. The relaxation of repressive chromatin marks enables transposition but also triggers a wave of transcription that promotes sense/antisense RNA expression and the synthesis of pachytene piRNAs. We propose that the majority of the transcripts are stored in the chromatoid body (indicated in round and elongated spermatids). siRNA (and piRNA)–Argonaute complexes (RISCs) search for their complementary target RNAs in the chromatoid body (CB) if the corresponding transcript is present; if the target RNA is not found in the CB, the RISCs enter the nucleus to interfere with the maturation process of the spermatid.

Mentions: The scenario that mutational variation and initial selection and quality control have been transferred in substantial part from the zygote to the sperm fits with the known temporal events in spermatogenesis, including DNA demethylation, the activation of transposition, its subsequent suppression by Piwi-interacting RNA (piRNA)–mediated pathways, the genome-wide wave of transcription that is followed by chromatin compaction, and large-scale apoptosis of immature sperm cells.2–4 We propose that these processes represent stages of a developmental program to enable the mobilization of transposable elements (TEs), which, through quasi-random insertion, promote variation in the genome. The transcriptional burst in the meiotic phase of spermatogenesis that produces the most complex transcriptome of all tissue, including the brain,5 represents the next important event in the proposed developmental program. Accordingly, the germ line–specific program6 enables pervasive transcription as the prerequisite for genomic quality screening to reduce the deleterious side effects of transposon insertions and recombination errors (Figs. 1 and 2). Intriguingly, the proposed stringent quality-control mechanism also helps to explain how complex organisms, humans in particular, can thrive in a highly mutagenic environment.7


Transpositional shuffling and quality control in male germ cells to enhance evolution of complex organisms.

Werner A, Piatek MJ, Mattick JS - Ann. N. Y. Acad. Sci. (2014)

Schematic representation of spermatogenesis. The timing of developmental processes relevant to transposon derepression and resilencing are indicated in the lower panels. Accordingly, TEs undergo a first round of derepression during fetal germ cell differentiation that triggers piRNA expression and de novo DNA remethylation. This course of events is thought to be specific for animals, because piRNAs are only found in the animal kingdom. In mammals, a second round of TE derepression initiates at the mitotic phase as a consequence of either active or passive genome-wide demethylation. The relaxation of repressive chromatin marks enables transposition but also triggers a wave of transcription that promotes sense/antisense RNA expression and the synthesis of pachytene piRNAs. We propose that the majority of the transcripts are stored in the chromatoid body (indicated in round and elongated spermatids). siRNA (and piRNA)–Argonaute complexes (RISCs) search for their complementary target RNAs in the chromatoid body (CB) if the corresponding transcript is present; if the target RNA is not found in the CB, the RISCs enter the nucleus to interfere with the maturation process of the spermatid.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390386&req=5

Figure 1: Schematic representation of spermatogenesis. The timing of developmental processes relevant to transposon derepression and resilencing are indicated in the lower panels. Accordingly, TEs undergo a first round of derepression during fetal germ cell differentiation that triggers piRNA expression and de novo DNA remethylation. This course of events is thought to be specific for animals, because piRNAs are only found in the animal kingdom. In mammals, a second round of TE derepression initiates at the mitotic phase as a consequence of either active or passive genome-wide demethylation. The relaxation of repressive chromatin marks enables transposition but also triggers a wave of transcription that promotes sense/antisense RNA expression and the synthesis of pachytene piRNAs. We propose that the majority of the transcripts are stored in the chromatoid body (indicated in round and elongated spermatids). siRNA (and piRNA)–Argonaute complexes (RISCs) search for their complementary target RNAs in the chromatoid body (CB) if the corresponding transcript is present; if the target RNA is not found in the CB, the RISCs enter the nucleus to interfere with the maturation process of the spermatid.
Mentions: The scenario that mutational variation and initial selection and quality control have been transferred in substantial part from the zygote to the sperm fits with the known temporal events in spermatogenesis, including DNA demethylation, the activation of transposition, its subsequent suppression by Piwi-interacting RNA (piRNA)–mediated pathways, the genome-wide wave of transcription that is followed by chromatin compaction, and large-scale apoptosis of immature sperm cells.2–4 We propose that these processes represent stages of a developmental program to enable the mobilization of transposable elements (TEs), which, through quasi-random insertion, promote variation in the genome. The transcriptional burst in the meiotic phase of spermatogenesis that produces the most complex transcriptome of all tissue, including the brain,5 represents the next important event in the proposed developmental program. Accordingly, the germ line–specific program6 enables pervasive transcription as the prerequisite for genomic quality screening to reduce the deleterious side effects of transposon insertions and recombination errors (Figs. 1 and 2). Intriguingly, the proposed stringent quality-control mechanism also helps to explain how complex organisms, humans in particular, can thrive in a highly mutagenic environment.7

Bottom Line: This reduces the ability of such organisms to explore evolutionary space, and, consequently, strategies that mitigate this problem likely have a strategic advantage.Cells that fail the genomic quality test are excluded from further development, eventually resulting in a positively selected mature sperm population.We suggest that these processes, enhanced variability and stringent molecular quality control, compensate for the apparent reduced potential of complex animals to adapt and evolve.

View Article: PubMed Central - PubMed

Affiliation: RNA Biology Group, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle, United Kingdom.

Show MeSH
Related in: MedlinePlus