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Parent-of-origin control of transgenerational retrotransposon proliferation in Arabidopsis - PubMed

Parent-of-origin control of transgenerational retrotransposon proliferation in Arabidopsis

Jon Reinders et al. EMBO Rep. 2013 Sep.

Abstract

Retrotransposons are ubiquitous mobile genetic elements constituting a major part of eukaryotic genomes. Yet, monitoring retrotransposition and subsequent copy number increases in multicellular eukaryotes is intrinsically difficult. By following the transgenerational accumulation of a newly activated retrotransposon EVADE (EVD) in Arabidopsis, we noticed fast expansion of activated elements transmitted through the paternal germ line but suppression when EVD-active copies are maternally inherited. This parent-of-origin effect on EVD proliferation was still observed when gametophytes carried mutations for key epigenetic regulators previously shown to restrict EVD mobility. Therefore, the main mechanism preventing active EVD proliferation seems to act through epigenetic control in sporophytic tissues in the mother plant. In consequence, once activated, this retrotransposon proliferates in plant populations owing to suppressed epigenetic control during paternal transmission. This parental gateway might contribute to the occasional bursts of retrotransposon mobilization deduced from the genome sequences of many plant species.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1

Parent-of-origin effects on the transmission of the active EVD within inter-accession crosses. (A) Crossing scheme to obtain epi12 and its F3 cross to the Ler accession. One plant from line 12 (epi12) of the epiRIL population at the F3 generation was crossed reciprocally (double arrow) with Ler to generate F1 and reciprocal F1 (rF1) hybrids. The use of Ler (L) or the epiRIL (e) parent is indicated (maternal/paternal) for each hybrid. The inferred EVD activity levels (EVD-silent or EVD-active) are indicated by white and black circles, respectively. (B) Southern blot detection of EVD ecDNA reveals pollen transmission of EVD. Undigested genomic DNA was probed for EVD. The presence of the ∼5-kb EVD ecDNA is indicated (black arrow). Individual epiRIL siblings were investigated, while the two F1 samples and the Ler parental control each comprised a bulked lot of eight individual plants. ecDNA, extrachromosomal DNA; Ler, Landsberg erecta.

Figure 2
Figure 2

Acceleration of EVD activity via pollen transmission within inter-accession crosses. (A) Crossing scheme between four epi12 F3 individuals (marked as A, B, C, D) crossed reciprocally (double arrow) to Ler parents to create populations A–D (see supplementary Fig S2B online for details). (B) Relative EVD DNA content observed in populations A–D at the F1 with the corresponding self-fertilized parental controls. The maternal and paternal contributions (as described in Fig 1) of each cross and sample size (n) are listed along the X axis below the graphs. The average relative EVD content levels (±s.e.m.) for each cross relative to the mid-parent level (set to 1 as midpoint of Col and Ler) are shown along the Y axis. The significance (P<0.05) of Student t-test comparisons of reciprocal crosses (F1 and rF1) for each population (horizontal bars) is indicated by asterisks. (C) Analyses of relative EVD DNA content in the epi12 x Ler F2 progenies of populations A and B. The maternal and paternal contribution and relative EVD DNA content for each population is shown as described in A. Significant differences between reciprocal crosses are shown as described in B. Ler, Landsberg erecta.

Figure 3
Figure 3

EVD transmission rates in EVD-active first-generation reciprocal backcross (BC1) populations. (A) Crossing scheme between one F3 generation epi12 individual (epi12.38, paternal parent) and ago5, kyp and nrpd2a mutants (as maternal parents) to create EVD-active backcross populations. Resultant F1 individuals selected as either EVD-active or EVD-silent (see supplementary Fig S3 online) was backcrossed reciprocally to the WT Col parent and the selected mutant parents (ago5, kyp and nrpd2a) to create the respective backcross populations. Shown here are the EVD-active populations; see supplementary Fig S4 online for EVD-silent population results. (B) Relative EVD DNA content levels (Y axis) shown for each entry (X axis) for the mutant populations: ago5 (upper panel), kyp (middle panel), and nrpd2a (lower panel). The parent-of-origin effect (active maternal, active paternal or active F1), sample size (n), and allelic origin at each respective epigenetic regulator for WT (M) and mutant (m) alleles are indicated with respect to parental contributions (maternal/paternal). Heterozygous F2 generation progeny (Het.) comprise both mM and Mm progeny. WT, wild type.

Figure 4
Figure 4

Initiation of EVD proliferation is controlled by parental sporophyte. (A) F1 plants met1 (±) nrpd2a (±) (mM nN) originating from a cross between met1 and nrpd2a parents were self-fertilized to produce segregating 1st and 2nd generation plants (1st and 2nd G, respectively). (B) Southern blot analysis of individual plants with SspI-digested DNA hybridized to an EVD-specific probe as previously reported [19]. (C) LTR-PCR showing EVD extrachromosomal forms diagnostic for EVD life cycle initiation in individual plants. Actin was a loading control and epi12 (F8) a positive control for EVD activity. LTR-PCR, long terminal repeat polymerase chain reaction; met1, methyltransferase 1.

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