A domesticated <i>Harbinger</i> transposase forms a complex with HDA6 and promotes histone H3 deacetylation at genes but not TEs in <i>Arabidopsis</i>

Zhou, Xishi; He, Junna; Velanis, Christos N.; Zhu, Yufan; He, Yuhan; Tang, Kai; Zhu, Mingku; Graser, Lisa; Leau, Erica de; Wang, Xingang; Zhang, Lingrui; Tao, W. Andy; Goodrich, Justin; Zhu, Jian‐Kang; Zhang, Cui‐Jun

doi:10.1111/jipb.13108

Cited by 18 publications

(34 citation statements)

References 59 publications

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“…Since their discovery, beyond their neutral or negative effects, multiple works have demonstrated the propensity of TEs to be positively recruited by host genomes as new regulatory and coding sequences [ 5 , 52 , 53 ]. Harbinger transposons are not exceptions to this, as multiple cases of Harbinger -derived genes have been reported in various organisms [ 16 , 18 , 24 , 54 , 55 , 56 , 57 , 58 ]. The ability of Harbinger transposons to form new genes may be linked to the presence of two ORFs encoding proteins with useful and different molecular properties that can interact together [ 24 ].…”

Section: Discussionmentioning

confidence: 99%

Diversity of Harbinger-like Transposons in Teleost Fish Genomes

Etchegaray

Dechaud

Barbier

et al. 2022

Animals

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Harbinger elements are DNA transposons that are widespread from plants to vertebrates but absent from mammalian genomes. Among vertebrates, teleost fish are the clade presenting not only the largest number of species but also the highest diversity of transposable elements, both quantitatively and qualitatively, making them a very attractive group to investigate the evolution of mobile sequences. We studied Harbinger DNA transposons and the distantly related ISL2EU elements in fish, focusing on representative teleost species compared to the spotted gar, the coelacanth, the elephant shark and the amphioxus. We observed high variability in the genomic composition of Harbinger-like sequences in teleost fish, as they covered 0.002–0.14% of the genome, when present. While Harbinger transposons might have been present in a common ancestor of all the fish species studied here, with secondary loss in elephant shark, our results suggests that ISL2EU elements were gained by horizontal transfer at the base of teleost fish 200–300 million years ago, and that there was secondary loss in a common ancestor of pufferfishes and stickleback. Harbinger transposons code for a transposase and a Myb-like protein. We reconstructed and compared molecular phylogenies of both proteins to get insights into the evolution of Harbinger transposons in fish. Transposase and Myb-like protein phylogenies showed global congruent evolution, indicating unique origin of the association between both genes and suggesting rare recombination between transposon sublineages. Finally, we report one case of Harbinger horizontal transfer between divergent fish species and the transcriptional activity of both Harbinger and ISL2EU transposons in teleost fish. There was male-biased expression in the gonads of the medaka fish.

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Section: Discussionmentioning

confidence: 99%

Diversity of Harbinger-like Transposons in Teleost Fish Genomes

Etchegaray

Dechaud

Barbier

et al. 2022

Animals

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“…Harbinger DNA transposons have given rise to multiple novel genes in divergent organisms: at least six in vertebrates, nine in Arabidopsis and seven in Drosophila ( Kapitonov and Jurka 2004 ; Casola et al 2007 ; Sinzelle et al 2008 ; Liang et al 2015 ; Duan et al 2017 ; Velanis et al 2020 ; Zhou et al 2021 ). Hence, it seems that these elements have high propensity to be recruited as new genes.…”

Section: Discussionmentioning

confidence: 99%

“…MSANTD3 has been suggested to work as a transcription factor that binds to DNA, where it can recruit the Polycomb Repressive Complex 2 to regulate neuronal differentiation in P19 mouse cells ( Gou 2014 ). Outside of vertebrates, other genes derived from Harbinger transposons have been identified in Arabidopsis ( Liang et al 2015 ; Duan et al 2017 ; Velanis et al 2020 ; Zhou et al 2021 ). ALP1 (Antagonist of Like Heterochromatin Protein 1), its paralog HHP1 (HDA6-associated Harbinger transposon-derived Protein 1) and HDP1 ( Harbinger transposon-derived protein 1) are derived from transposases, while ALP2 (Antagonist of Like Heterochromatin Protein 2), HDP2 ( Harbinger transposon-Derived Protein 2), SANT1 , SANT2 , SANT3 , and SANT4 have been formed from Harbinger Myb-like genes.…”

Section: Discussionmentioning

confidence: 99%

The Neurodevelopmental Gene MSANTD2 Belongs to a Gene Family Formed by Recurrent Molecular Domestication of Harbinger Transposons at the Base of Vertebrates

Etchegaray

Baas

Naville

et al. 2022

Molecular Biology and Evolution

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The formation of new genes is a major source of organism evolutionary innovation. Beyond their mutational effects, transposable elements can be co-opted by host genomes to form different types of sequences including novel genes, through a mechanism named molecular domestication.We report the formation of four genes through molecular domestication of Harbinger transposons, three in a common ancestor of jawed vertebrates about 500 million years ago and one in sarcopterygians approx. 430 million years ago. Additionally, one processed pseudogene arose approx. 60 million years ago in simians. In zebrafish, Harbinger-derived genes are expressed during early development but also in adult tissues, and predominantly co-expressed in male brain. In human, expression was detected in multiple organs, with major expression in the brain particularly during fetal development. We used CRISPR/Cas9 with direct gene knock-out in the F0 generation and the morpholino antisense oligonucleotide knock-down technique to study in zebrafish the function of one of these genes called MSANTD2, which has been suggested to be associated to neuro-developmental diseases such as autism spectrum disorders and schizophrenia in human. MSANTD2 inactivation led to developmental delays including tail and nervous system malformation at one day post fertilization. Affected embryos showed dead cell accumulation, major anatomical defects characterized by impaired brain ventricle formation and alterations in expression of some characteristic genes involved in vertebrate nervous system development. Hence, the characterization of MSANTD2 and other Harbinger-derived genes might contribute to a better understanding of the genetic innovations having driven the early evolution of the vertebrate nervous system.

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“…An interaction was also described with the SWItch/Sucrose Non-Fermentable (SWI/SNF) chromatin-remodeling complex (CRC) subunit SWI3B to repress a subset of TEs [ 74 ]. Although these former interactors could not be confirmed, recent HDA6 affinity purification followed by mass spectrometry (AP-MS) analyses highlighted the co-existence of several HDA6 complexes [ 75 , 76 ]. It remains unclear as to what is the composition of the HDA6 complex specifically involved in TE silencing.…”

Section: A Plethora Of Sophisticated Epigenetic Pathways Dampen Tesmentioning

confidence: 99%

“…Finally, the co-opted transposase HDA6-associated Harbinger transposon-derived protein 1 (HHP1) was recently identified as a new HDA6 partner, forming a complex together with the four Harbinger-derived SANT-domain-containing proteins SANT1, SANT2, SANT3 and SANT4, and the MBD1, MBD2 and MBD4 [ 76 ]. Then, split luciferase assays suggested that HHP1 and MBD1 would act as bridges between HDA6 and the SANTs.…”

Section: Exaptation Of Te Coding Regionsmentioning

confidence: 99%

The Evolutionary Volte-Face of Transposable Elements: From Harmful Jumping Genes to Major Drivers of Genetic Innovation

Nicolau

Picault

Moissiard

2021

Cells

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Transposable elements (TEs) are self-replicating DNA elements that constitute major fractions of eukaryote genomes. Their ability to transpose can modify the genome structure with potentially deleterious effects. To repress TE activity, host cells have developed numerous strategies, including epigenetic pathways, such as DNA methylation or histone modifications. Although TE neo-insertions are mostly deleterious or neutral, they can become advantageous for the host under specific circumstances. The phenomenon leading to the appropriation of TE-derived sequences by the host is known as TE exaptation or co-option. TE exaptation can be of different natures, through the production of coding or non-coding DNA sequences with ultimately an adaptive benefit for the host. In this review, we first give new insights into the silencing pathways controlling TE activity. We then discuss a model to explain how, under specific environmental conditions, TEs are unleashed, leading to a TE burst and neo-insertions, with potential benefits for the host. Finally, we review our current knowledge of coding and non-coding TE exaptation by providing several examples in various organisms and describing a method to identify TE co-option events.

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A domesticated Harbinger transposase forms a complex with HDA6 and promotes histone H3 deacetylation at genes but not TEs in Arabidopsis

Cited by 18 publications

References 59 publications

Diversity of Harbinger-like Transposons in Teleost Fish Genomes

Diversity of Harbinger-like Transposons in Teleost Fish Genomes

The Neurodevelopmental Gene MSANTD2 Belongs to a Gene Family Formed by Recurrent Molecular Domestication of Harbinger Transposons at the Base of Vertebrates

The Evolutionary Volte-Face of Transposable Elements: From Harmful Jumping Genes to Major Drivers of Genetic Innovation

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