Dead Element Replicating: Degenerate R2 Element Replication and rDNA Genomic Turnover in the Bacillus rossius Stick Insect (Insecta: Phasmida)

Martoni, Francesco; Eickbush, Danna G.; Scavariello, Claudia; Luchetti, Andrea; Mantovani, Barbara

doi:10.1371/journal.pone.0121831

Cited by 5 publications

(7 citation statements)

References 36 publications

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“…This apparent absence of homogenisation is indicative of extremely high mutation rates and/or considerable periods of time since the arrays last homogenised. Such variability contrasts with the situation in some animals where pseudogenes (transposon-inserted) seem to undergo at least partial homogenisation (Eickbush et al 1997 ; Glass et al 2008 ; Martoni et al 2015 ). The high homogeneity of 18S reads in D. lowei (Fig.…”

Section: Discussionmentioning

confidence: 85%

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb

Wang

Becher

et al. 2015

Chromosoma

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In all eukaryotes, the highly repeated 35S ribosomal DNA (rDNA) sequences encoding 18S-5.8S-26S ribosomal RNA (rRNA) typically show high levels of intragenomic uniformity due to homogenisation processes, leading to concerted evolution of 35S rDNA repeats. Here, we compared 35S rDNA divergence in several seed plants using next generation sequencing and a range of molecular and cytogenetic approaches. Most species showed similar 35S rDNA homogeneity indicating concerted evolution. However, Cycas revoluta exhibits an extraordinary diversity of rDNA repeats (nucleotide sequence divergence of different copies averaging 12 %), influencing both the coding and non-coding rDNA regions nearly equally. In contrast, its rRNA transcriptome was highly homogeneous suggesting that only a minority of genes (<20 %) encode functional rRNA. The most common SNPs were C > T substitutions located in symmetrical CG and CHG contexts which were also highly methylated. Both functional genes and pseudogenes appear to cluster on chromosomes. The extraordinary high levels of 35S rDNA diversity in C. revoluta, and probably other species of cycads, indicate that the frequency of repeat homogenisation has been much lower in this lineage, compared with all other land plant lineages studied. This has led to the accumulation of methylation-driven mutations and pseudogenisation. Potentially, the reduced homology between paralogs prevented their elimination by homologous recombination, resulting in long-term retention of rDNA pseudogenes in the genome.Electronic supplementary materialThe online version of this article (doi:10.1007/s00412-015-0556-3) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 85%

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb

Wang

Becher

et al. 2015

Chromosoma

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“…As far as R2 is concerned, we showed that the B. rossius genome hosts a functional (R2Br fun ) and a closely related, degenerate (R2Br deg ) element (Bonandin et al, 2014). Both elements actively replicate, but while R2Br fun showed a canonical pattern of a functional R2, R2Br deg copies are exclusively full length, that is, they have no associated 5 -end deletions, and lost the ability to fold into the ribozyme necessary for R2 RNA maturation, suggesting they replicate via 28S rDNA unequal recombination (Martoni et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Obligatory parthenogenesis and TE load: Bacillus stick insects and the R2 non‐LTR retrotransposon

et al. 2016

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Transposable elements (TEs) are selfish genetic elements whose self-replication is contrasted by the host genome. In this context, host reproductive strategies are predicted to impact on both TEs load and activity. The presence and insertion distribution of the non-LTR retrotransposon R2 was here studied in populations of the strictly bisexual Bacillus grandii maretimi and of the obligatory parthenogenetic Bacillus atticus atticus. Furthermore, data were also obtained from the offspring of selected B. a. atticus females. At the population level, the gonochoric B. g. maretimi showed a significantly higher R2 load than the obligatory parthenogenetic B. a. atticus. The comparison with bisexual and unisexual Bacillus rossius populations showed that their values were higher than those recorded for B. a. atticus and similar, or even higher, than those of B. g. maretimi. Consistently, an R2 load reduction is scored in B. a. atticus offspring even if with a great variance. On the whole, data here produced indicate that in the obligatory unisexual B. a. atticus R2 is active and that mechanisms of molecular turnover are effective. Furthermore, progeny analyses show that, at variance of the facultative parthenogenetic B. rossius, the R2 activity is held at a lower rate. Modeling parental-offspring inheritance, suggests that in B. a. atticus recombination plays a major role in eliminating insertions rather than selection, as previously suggested for unisexual B. rossius progeny, even if in both cases a high variance is observed. In addition to this, mechanisms of R2 silencing or chances of clonal selection cannot be ruled out.

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“…This element shows a complete ORF of 2739 bp encoding a protein of 912 amino acids. Interestingly, in a 5′ end sequence survey carried out in B. rossius 34 , an incomplete element was retrieved (R2Br del ), showing 99% of similarity with R2Bgm del and sharing the same internal deletion. The R2Br del fragment encompasses the whole 5′ UTR and the first 1293 bp of the ORF; the protein sequence obtained from that part of the ORF is 430 amino acids long, and the RT domain was only partially covered.…”

Section: Resultsmentioning

confidence: 99%

“…Subsequent comparisons involved presently isolated elements ( B. atticus : R2Ba; B. g. grandii : R2Bgg A and R2Bgg B ; B. g. benazzii : R2Bgb; B. g. maretimi : R2Bgm and R2Bgm del Fig. 1 ) together with previously identified ones ( B. rossius : R2Br fun , R2Br deg and R2Br del 32 34 ).…”

Section: Resultsmentioning

confidence: 99%

“…We recently analyzed R2 in stick insects of the genus Bacillus , addressing the evolutionary dynamics of their insertions in different reproductive strategies 32 33 , as well as the coevolution of multiple lineages in the genome of B. rossius 34 . In order to have a full picture of R2 evolution in the Bacillus species complex, we isolated and characterized R2 from the obligatory parthenogenetic B. atticus and the strictly gonochoric B. grandii .…”

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confidence: 99%

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Hybridogenesis and a potential case of R2 non-LTR retrotransposon horizontal transmission in Bacillus stick insects (Insecta Phasmida)

Scavariello

Luchetti

Martoni

et al. 2017

Sci Rep

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Horizontal transfer (HT) is an event in which the genetic material is transferred from one species to another, even if distantly related, and it has been demonstrated as a possible essential part of the lifecycle of transposable elements (TEs). However, previous studies on the non-LTR R2 retrotransposon, a metazoan-wide distributed element, indicated its vertical transmission since the Radiata-Bilateria split. Here we present the first possible instances of R2 HT in stick insects of the genus Bacillus (Phasmida). Six R2 elements were characterized in the strictly bisexual subspecies B. grandii grandii, B. grandii benazzii and B. grandii maretimi and in the obligatory parthenogenetic taxon B. atticus. These elements were compared with those previously retrieved in the facultative parthenogenetic species B. rossius. Phylogenetic inconsistencies between element and host taxa, and age versus divergence analyses agree and support at least two HT events. These HT events can be explained by taking into consideration the complex Bacillus reproductive biology, which includes also hybridogenesis, gynogenesis and androgenesis. Through these non-canonical reproductive modes, R2 elements may have been transferred between Bacillus genomes. Our data suggest, therefore, a possible role of hybridization for TEs survival and the consequent reshaping of involved genomes.

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Dead Element Replicating: Degenerate R2 Element Replication and rDNA Genomic Turnover in the Bacillus rossius Stick Insect (Insecta: Phasmida)

Cited by 5 publications

References 36 publications

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb

Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb

Obligatory parthenogenesis and TE load: Bacillus stick insects and the R2 non‐LTR retrotransposon

Hybridogenesis and a potential case of R2 non-LTR retrotransposon horizontal transmission in Bacillus stick insects (Insecta Phasmida)

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