High-frequency recombination between members of an LTR retrotransposon family during transposition bursts

Sánchez, Diego H.; Gaubert, Hervé; Drost, Hajk-Georg; Zabet, Nicolae Radu; Paszkowski, Jerzy

doi:10.1038/s41467-017-01374-x

Cited by 44 publications

(54 citation statements)

References 27 publications

(35 reference statements)

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“…Because completely unrestrained and fully activated LTR retrotransposons typically generate copious life‐cycle intermediates in the form of extrachromosomal DNA (Mirouze et al ., ; Ito et al ., ), we wondered if this was also the case for MESSI . We performed tissue‐specific PCR‐free DNA‐seq and counted reads mapping to the target TEs, potentially revealing not only extrachromosomal DNA but also putative new chromosomal copies (Sanchez et al ., ). However, tomato shoot apical meristems did not show an increased number of DNA‐seq reads mapping to the very young transcriptionally activated MESSI (Fig.…”

Section: Resultsmentioning

confidence: 97%

“…To the best of our knowledge, no operative antisilencing factors have been described for LTR retrotransposons, but mounting evidence suggests that several plant retrotransposon families could override certain layers of epigenetic suppression. For instance, inductive environmental conditions activated ONSEN/COPIA78 of A. thaliana and Tnt1 of tobacco despite TGS recognition and targeting (Ito et al ., ; Hernandez‐Pinzon et al ., ; Sanchez et al ., ). Other plant retrotransposons such as RIDER of tomato, OGRE of pea, SARE A of soybean and BARE1 of barley appeared transcriptionally unrestricted – and certainly translationally competent at least in the last case – across most wild‐type tissues where the epigenetic machinery is intact (Neumann et al ., ; Jiang et al ., ; Du et al ., ; Jaaskelainen et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…DNA‐seq was mapped with B owtie 2 (Langmead & Salzberg, ), using parameter sets –very‐sensitive ‐X 1000 –non‐deterministic. Reads mapping over MESSI were prefiltered to diminish ambiguous mapping (first mapped to a masked genome recovering unmapped reads, then remapping these to specific sequences; Sanchez et al ., ), and were subsequently counted with BED tools intersect. Open‐source software such as SAM tools (Li et al ., ), P icard ( http://picard.sourceforge.net.)…”

Section: Methodsmentioning

confidence: 99%

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Evidence of developmental escape from transcriptional gene silencing in MESSI retrotransposons

2019

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Summary Transposable elements (TEs) are ubiquitous genomic features. ‘Copy‐and‐paste’ long‐terminal‐repeat (LTR) retrotransposons have been particularly successful during evolution of the plant kingdom, representing a substantial proportion of genomes. For survival in copious numbers, these TEs may have evolved replicative mobilization strategies that circumvented hosts’ epigenetic silencing. Stressful circumstances are known to trigger the majority of known mobilizing plant retrotransposons, leading to the idea that most are activated by environmental signals. However, previous research revealed that plant developmental programs include steps of silencing relaxation, suggesting that developmental signals may also be of importance for thriving parasitic elements. Here, we uncover an unusual family of giant LTR retrotransposons from the Solanum clade, named MESSI, with transcriptional competence in shoot apical meristems of tomato. Despite being recognized and targeted by the host epigenetic surveillance, this family is activated in specific meristematic areas fundamental for plant shoot development, which are involved in meristem formation and maintenance. Our work provides initial evidence that some retrotransposons may evolve developmentally associated escape strategies to overcome transcriptional gene silencing in vegetative tissues contributing to the host's next generation. This implies that not only environmental but also developmental signals could be exploited by selfish elements for survival within the plant kingdom.

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Section: Resultsmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

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Evidence of developmental escape from transcriptional gene silencing in MESSI retrotransposons

2019

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“…We consider these values as conservative estimates, and likely underestimations, as they do not account for the high rate of repeated DNA divergence. Repeats may have escaped their detection by accumulation of mutations over time, recombination, diversification, reshuffling, and decay (Ma et al, 2004, Wollrab et al, 2012, Elliott and Gregory, 2015, Sanchez et al, 2017, Bourque et al, 2018. From the extracted repeat dataset, we identified and characterised seven Chenopodium satDNAs and the 5S rRNA genes.…”

Section: Next-and Third-generation Sequence Reads Give An Overview Onmentioning

confidence: 99%

Satellite DNA landscapes after allotetraploidisation of quinoa (Chenopodium quinoa) reveal unique A and B subgenomes

Heitkam

Weber

Walter

et al. 2019

Preprint

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Key words: Chenopodium quinoa, polyploidy, tandem repeat, satellite DNA, 5S rDNA, fluorescent in situ hybridisation (FISH), single molecule real-time (SMRT) reads Word count: 7,901 (total without abstract, references and figure legends), divided into 754 (introduction), 3,578 (results), 2,181 (discussion), 1,164 (experimental procedures) SUMMARY If two related plant species hybridise, their genomes are combined within a single nucleus, thereby forming an allotetraploid. How the emerging plant balances two co-evolved genomes is still a matter of ongoing research. Here, we focus on satellite DNA (satDNA), the fastest turn-over sequence class in eukaryotes, aiming to trace its emergence, amplification and loss during plant speciation and allopolyploidisation. As a model, we used Chenopodium quinoa Willd. (quinoa), an allopolyploid crop with 2n=4x=36 chromosomes. Quinoa originated by hybridisation of an unknown female American Chenopodium diploid (AA genome) with an unknown male Old World diploid species (BB genome), dating back 3.3 to 6.3 million years.Applying short read clustering to quinoa (AABB), C. pallidicaule (AA), and C. suecicum (BB) whole genome shotgun sequences, we classified their repetitive fractions, and identified and characterised seven satDNA families, together with the 5S rDNA model repeat. We show unequal satDNA amplification (two families) and exclusive occurrence (four families) in the AA and BB diploids by read mapping as well as Southern, genomic and fluorescent in situ hybridisation. As C. pallidicaule harbours a unique satDNA profile, we are able to exclude it as quinoa's parental species. Using quinoa long reads and scaffolds, we detected only limited evidence of interlocus homogenisation of satDNA after allopolyploidisation, but were able to exclude dispersal of 5S rRNA genes between subgenomes. Our results exemplify the complex route of tandem repeat evolution through Chenopodium speciation and allopolyploidisation, and may provide sequence targets for the identification of quinoa's progenitors.

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“…This is because selfers reduce the spread of TEs between individuals, and, compared to outcrossers, more efficiently purge insertions with deleterious recessive effects (Morgan 2001; Wright et al 2008; Wright and Schoen 1999). Outcrossing may also increase the activity and genetic diversity of LTRs during transposition burst cycles (Sanchez et al 2017). Expectations of these models parallel those concerning genetic load in homosporous ferns (Hedrick 1987), and TEs, if deleterious, may comprise a large component of genetic load.…”

Section: Dissussionmentioning

confidence: 99%

Nuclear Genome Size is Positively Correlated with Mean LTR Insertion Date in Fern and Lycophyte Genomes

Baniaga

Barker

2019

Preprint

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Nuclear genome size is highly variable in vascular plants. The composition of long terminal repeat retrotransposons (LTRs) is a chief mechanism of long term change in the amount of nuclear DNA. Compared to flowering plants, little is known about LTR dynamics in ferns and lycophytes. Drawing upon the availability of recently sequenced fern and lycophyte genomes we investigated these dynamics and placed them in the context of vascular plants. We found that similar to seed plants, mean LTR insertion dates were strongly correlated with haploid nuclear genome size. Fern and lycophyte species with small genomes such as those of the heterosporous Selaginella and members of the Salviniaceae had recent mean LTR insertion dates, whereas species with large genomes such as homosporous ferns had old mean LTR insertion dates intermediate between angiosperms and gymnosperms. This pattern holds despite methylation and life history differences in ferns and lycophytes compared to seed plants, and our results are consistent with other patterns of structural variation in fern and lycophyte genomes.

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High-frequency recombination between members of an LTR retrotransposon family during transposition bursts

Cited by 44 publications

References 27 publications

Evidence of developmental escape from transcriptional gene silencing in MESSI retrotransposons

Evidence of developmental escape from transcriptional gene silencing in MESSI retrotransposons

Satellite DNA landscapes after allotetraploidisation of quinoa (Chenopodium quinoa) reveal unique A and B subgenomes

Nuclear Genome Size is Positively Correlated with Mean LTR Insertion Date in Fern and Lycophyte Genomes

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