Environmentally-Induced Transgenerational Epigenetic Inheritance: Implication of PIWI Interacting RNAs

Casier, Karine; Boivin, Antoine; Carré, Clément; Teysset, Laure

doi:10.3390/cells8091108

Cited by 29 publications

(24 citation statements)

References 189 publications

(220 reference statements)

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“…The maternally-transmitted piRNA pool deposited in the oocyte launches piRNA processing in the progeny, leading to transposon suppression in Drosophila [40]. Maternal inheritance of transgenic piRNAs was reported to be crucial for the paramutation of a homologous initially inactive transgene [18,46]. The latter transgenic model is based on the T1 transgene cluster bearing tandem repeats of P-lac-w transgenes located in the heterochromatin of a rearranged chromosome 2R [47].…”

Section: Discussionmentioning

confidence: 99%

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

Komarov

Akulenko

Brasset

et al. 2020

Cells

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Transgenes containing a fragment of the I retrotransposon represent a powerful model of piRNA cluster de novo formation in the Drosophila germline. We revealed that the same transgenes located at different genomic loci form piRNA clusters with various capacity of small RNA production. Transgenic piRNA clusters are not established in piRNA pathway mutants. However, in the wild-type context, the endogenous ancestral I-related piRNAs heterochromatinize and convert the I-containing transgenes into piRNA-producing loci. Here, we address how the quantitative level of piRNAs influences the heterochromatinization and piRNA production. We show that a minimal amount of maternal piRNAs from ancestral I-elements is sufficient to form the transgenic piRNA clusters. Supplemental piRNAs stemming from active I-element copies do not stimulate additional chromatin changes or piRNA production from transgenes. Therefore, chromatin changes and piRNA production are initiated by a minimum threshold level of complementary piRNAs, suggesting a selective advantage of prompt cell response to the lowest level of piRNAs. It is noteworthy that the weak piRNA clusters do not transform into strong ones after being targeted by abundant I-specific piRNAs, indicating the importance of the genomic context for piRNA cluster establishment. Analysis of ovarian transcription profiles suggests that regions facilitating convergent transcription favor the formation of transgenic piRNA clusters.

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Section: Discussionmentioning

confidence: 99%

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

Komarov

Akulenko

Brasset

et al. 2020

Cells

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“…It is also possible that parental environment can establish epigenetic states that influence multiple generations (Heard and Martienssen 2014). Environmentally-induced trans-generational epigenetic inheritance is an emerging field (Casier et al 2019, Pang et al 2019. The scientific understanding of myriad mechanisms, especially the role of reproductive small RNAs in trans-generational inheritance of male fertility and sterility, is at a nascent stage.…”

Section: Discussionmentioning

confidence: 99%

Environment-conditioned male fertility of HD-ZIP IV transcription factor mutantocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers

Yadava

Tamim

Zhang

et al. 2020

Preprint

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AbstractEnvironment-conditioned genic male sterility is a key strategy used to produce hybrid seeds efficiently in many crops, with the exception of maize. The underlying molecular mechanisms of environment-conditioned sterility are poorly understood. Here, we report a derivative line of the male sterile outer cell layer 4 (ocl4) mutant of maize, in which fertility was restored and perpetuated over several generations, under warm growing conditions. Conditionally fertile ocl4 anthers exhibit the anatomical abnormality of a partially duplicated endothecial layer, just like their sterile counterparts. We profiled the dynamics of phased, small interfering RNAs (phasiRNAs) during pre-meiotic development in fully sterile and various grades of semi-fertile ocl4 anthers. We found that the biogenesis of 21-nt phasiRNAs is largely dependent on Ocl4 at three key steps: (1) production of PHAS precursor transcripts, (2) expression of miR2118 that modulates precursor processing, and (3) accumulation of 21-nt phasiRNAs. We propose that 21-nt reproductive phasiRNAs buffer development under unfavorable environmental conditions and are dispensable under favorable conditions.

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“…Currently many questions about paramutations remain to be answered: i) are paramutations important for silencing novel TE invasions or mostly for maintaining silencing of a TE, ii) which fraction of the TE insertions could potentially be converted into piRNA producing loci iii) are paramutated loci stably inherited over generations and iv) what is the role of the environment in paramutations (e.g. Casier et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

piRNA clusters need a minimum size to control transposable element invasions

Kofler¹

2019

Preprint

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piRNA clusters are thought to repress transposable element activity in mammals and invertebrates. Here we show that a simple population genetics model reveals a constraint on the size of piRNA clusters: the total size of the piRNA clusters of an organism ought to exceed 0.2% of a genome. Larger piRNA clusters accounting for up to 3% of the genome may be necessary when populations are small, transposition rates are high and TE insertions recessive. If piRNA clusters are too small the load of deleterious TE insertions accumulating during a TE invasion may drive populations extinct before an effective piRNA based defence against the TE can be established. Our finding is solely based on three well supported assumptions: i) TEs multiply withing genomes, ii) TEs are mostly deleterious and iii) piRNA clusters act as transposons traps, where a single insertion in a cluster silences all TE copies in trans. Interestingly, piRNA clusters of some species meet our minimum size requirements while clusters of other species don't. Species with small piRNA clusters, such as humans and mice, may experience severe fitness reductions during invasions of novel TEs, possibly even threatening the persistence of some populations. This work also raises the important question of how piRNA clusters evolve. We propose that the size of piRNA clusters may be at an equilibrium between evolutionary forces that act to expand and contract piRNA clusters.

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Environmentally-Induced Transgenerational Epigenetic Inheritance: Implication of PIWI Interacting RNAs

Cited by 29 publications

References 189 publications

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

Epigenetic Requirements for Triggering Heterochromatinization and Piwi-Interacting RNA Production from Transgenes in the Drosophila Germline

Environment-conditioned male fertility of HD-ZIP IV transcription factor mutantocl4: impact on 21-nt phasiRNA accumulation in pre-meiotic maize anthers

piRNA clusters need a minimum size to control transposable element invasions

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