Population genomics in the arboviral vector <i>Aedes aegypti</i> reveals the genomic architecture and evolution of endogenous viral elements

Crava, Cristina M.; Varghese, Finny S.; Pischedda, Elisa; Halbach, Rebecca; Palatini, Umberto; Marconcini, Michele; Gasmi, Laila; Redmond, Seth; Afrane, Yaw A.; Ayala, Diégo; Paupy, Christophe; Carballar-Lejarazú, Rebeca; Miesen, Pascal; Rij, Ronald P. van; Bonizzoni, Mariangela

doi:10.1111/mec.15798

Cited by 44 publications

(62 citation statements)

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“…aegypti, the pathway has been implicated in diverse processes ranging from antiviral defense See also Figure S6. (Miesen et al, 2015;Schnettler et al, 2013;Vodovar et al, 2012;Morazzani et al, 2012) and immune memory (Tassetto et al, 2019;Suzuki et al, 2020;Crava et al, 2021) to gene regulation (Girardi et al, 2017) and embryonic development (Halbach et al, 2020;Betting et al, 2020). However, knowledge of piRNA biogenesis and effector mechanisms in Ae.…”

Section: Discussionmentioning

confidence: 99%

“…For example, the vector mosquito Aedes aegypti expresses an expanded PIWI protein repertoire of seven members, several of which are expressed in somatic tissues, suggesting that the pathway has additional functions besides transposon silencing (Miesen et al, 2016;Campbell et al, 2008;Lewis et al, 2016). Indeed, the Aedes piRNA pathway has been implicated in noncanonical processes, such as antiviral defense (Morazzani et al, 2012;Miesen et al, 2015;Vodovar et al, 2012;Schnettler et al, 2013), endogenous viral element (EVE)-mediated immune memory (Tassetto et al, 2019;Suzuki et al, 2020;Crava et al, 2021), mRNA elimination during embryonic development (Halbach et al, 2020;Betting et al, 2020), and gene regulation (Girardi et al, 2017;Arensburger et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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PIWI proteomics identifies Atari and Pasilla as piRNA biogenesis factors in Aedes mosquitoes

et al. 2021

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As in most arthropods, the PIWI-interacting RNA (piRNA) pathway in the vector mosquito Aedes aegypti is active in diverse biological processes in both soma and germline. To gain insights into piRNA biogenesis and effector complexes, we mapped the interactomes of the somatic PIWI proteins Ago3, Piwi4, Piwi5, and Piwi6 and identify numerous specific interactors as well as cofactors associated with multiple PIWI proteins. We describe the Piwi5 interactor AAEL014965, the direct ortholog of the Drosophila splicing factor pasilla. We find that Ae. aegypti Pasilla encodes a nuclear isoform and a cytoplasmic isoform, the latter of which is required for efficient piRNA production. In addition, we characterize a splice variant of the Tudor protein AAEL008101/Atari that associates with Ago3 and forms a scaffold for PIWI proteins and target RNAs to promote ping-pong amplification of piRNAs. Our study provides a useful resource for follow-up studies of somatic piRNA biogenesis, mechanism, and function in Aedes mosquitoes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

PIWI proteomics identifies Atari and Pasilla as piRNA biogenesis factors in Aedes mosquitoes

et al. 2021

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“…propiR1 mapped to seven locations on chromosome 3 (Fig. 1G), five of which are inside piRNA clusters (Crava et al 2021) These seven sites displayed a high degree of sequence conservation covering the piRNA and a ~250 bp flanking sequence element (Fig. 1H).…”

Section: A Host-derived Pirna Associates With Piwi4 and Piwi5mentioning

confidence: 99%

A piRNA-lncRNA regulatory network initiates responder and trailer piRNA formation during mosquito embryonic development

Betting

Joosten

Halbach

et al. 2020

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PIWI-interacting (pi)RNAs are small silencing RNAs that are crucial for the defense against transposable elements in germline tissues of animals. In the mosquito Aedes aegypti, the piRNA pathway also contributes to gene regulation in somatic tissues, illustrating additional roles for piRNAs and PIWI proteins besides transposon repression. Here, we identify a highly abundant, endogenous piRNA (propiR1) that associates with both Piwi4 and Piwi5. PropiR1-mediated target silencing requires base pairing in the seed region with supplemental base pairing at the piRNA 3' end. Yet, propiR1 strongly represses a single target, the lncRNA AAEL027353 (lnc027353). Slicing of this target initiates the production of responder and trailer piRNAs from the 3' cleavage fragment. Expression of propiR1 commences early during embryonic development and mediates degradation of maternally provided lnc027353. Both propiR1 and its lncRNA target display a high degree of sequence conservation in the closely related Aedes albopictus, underscoring the importance of this regulatory network for mosquito development.

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“…Of the five unmapped sequences, two mapped either between or immediately next to the EVEs we characterised (Additional file 1 : Table S2). The remaining three unmapped sequences did not have strong similarity to the AaegL5 assembly, but could be identified in the previous assembly used and in some field samples [ 10 , 11 , 31 ]. While we used the BLASTN tool and others may have used TBLASTX [ 11 ], almost all viral integration events were still detected using both approaches.…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore, recent work in Ae. aegypti [ 10 ] identified sequences similar to those of Cell-fusing agent virus in a number of RNAseq replicates and in several DNA WGS libraries [ 31 ] in which the latter is unexpected, and suggests the presence of an EVE . We replicated this analysis and found fragments of this Cell-fusing agent virus sequence in some WGS libraries including three out of five generated by our laboratory, though not in AaegL5 raw reads.…”

Section: Discussionmentioning

confidence: 99%

Flavivirus integrations in Aedes aegypti are limited and highly conserved across samples from different geographic regions unlike integrations in Aedes albopictus

et al. 2021

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Mosquitoes of the genus Aedes are the main vectors of many viruses, e.g. dengue and Zika, which affect millions of people each year and for which there are limited treatment options. Understanding how Aedes mosquitoes tolerate high viral loads may lead to better disease control strategies. Elucidating endogenous viral elements (EVEs) within vector genomes may give exploitable biological insights. Previous studies have reported the presence of a large number of EVEs in Aedes genomes. Here we investigated if flavivirus EVEs are conserved across populations and different Aedes species by using ~ 500 whole genome sequence libraries from Aedes aegypti and Aedes albopictus, sourced from colonies and field mosquitoes across continents. We found that nearly all flavivirus EVEs in the Ae. aegypti reference genome originate from four separate putative viral integration events, and that they are highly conserved across geographically diverse samples. By contrast, flavivirus EVEs in the Ae. albopictus reference genome originate from up to nine distinct integration events and show low levels of conservation, even within samples from narrow geographical ranges. Our analysis suggests that flaviviruses integrated as long sequences and were subsequently fragmented and shuffled by transposable elements. Given that EVEs of Ae. aegypti and Ae. albopictus belong to different phylogenetic clades and have very differing levels of conservation, they may have different evolutionary origins and potentially different functional roles.

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Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements

Abstract: This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Cited by 44 publications

References 83 publications

PIWI proteomics identifies Atari and Pasilla as piRNA biogenesis factors in Aedes mosquitoes

PIWI proteomics identifies Atari and Pasilla as piRNA biogenesis factors in Aedes mosquitoes

A piRNA-lncRNA regulatory network initiates responder and trailer piRNA formation during mosquito embryonic development

Flavivirus integrations in Aedes aegypti are limited and highly conserved across samples from different geographic regions unlike integrations in Aedes albopictus

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