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

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.

SUBMITTER: Reinders J

PROVIDER: S-EPMC3790068 | biostudies-literature | 2013 Sep

REPOSITORIES: biostudies-literature

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

Reinders Jon J Mirouze Marie M Nicolet Joël J Paszkowski Jerzy J

EMBO reports 20130709 9

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 ...[more]

PMID: 23835507

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Project description:BACKGROUND: Epigenetic regulation of gene dosage by genomic imprinting of some autosomal genes facilitates normal reproductive development in both mammals and flowering plants. While many imprinted genes have been identified and intensively studied in mammals, smaller numbers have been characterized in flowering plants, mostly in Arabidopsis thaliana. Identification of additional imprinted loci in flowering plants by genome-wide screening for parent-of-origin specific uniparental expression in seed tissues will facilitate our understanding of the origins and functions of imprinted genes in flowering plants. RESULTS: cDNA-AFLP can detect allele-specific expression that is parent-of-origin dependent for expressed genes in which restriction site polymorphisms exist in the transcripts derived from each allele. Using a genome-wide cDNA-AFLP screen surveying allele-specific expression of 4500 transcript-derived fragments, we report the identification of 52 maternally expressed genes (MEGs) displaying parent-of-origin dependent expression patterns in Arabidopsis siliques containing F1 hybrid seeds (3, 4 and 5 days after pollination). We identified these MEGs by developing a bioinformatics tool (GenFrag) which can directly determine the identities of transcript-derived fragments from (i) their size and (ii) which selective nucleotides were added to the primers used to generate them. Hence, GenFrag facilitates increased throughput for genome-wide cDNA-AFLP fragment analyses. The 52 MEGs we identified were further filtered for high expression levels in the endosperm relative to the seed coat to identify the candidate genes most likely representing novel imprinted genes expressed in the endosperm of Arabidopsis thaliana. Expression in seed tissues of the three top-ranked candidate genes, ATCDC48, PDE120 and MS5-like, was confirmed by Laser-Capture Microdissection and qRT-PCR analysis. Maternal-specific expression of these genes in Arabidopsis thaliana F1 seeds was confirmed via allele-specific transcript analysis across a range of different accessions. Differentially methylated regions were identified adjacent to ATCDC48 and PDE120, which may represent candidate imprinting control regions. Finally, we demonstrate that expression levels of these three genes in vegetative tissues are MET1-dependent, while their uniparental maternal expression in the seed is not dependent on MET1. CONCLUSIONS: Using a cDNA-AFLP transcriptome profiling approach, we have identified three genes, ATCDC48, PDE120 and MS5-like which represent novel maternally expressed imprinted genes in the Arabidopsis thaliana seed. The extent of overlap between our cDNA-AFLP screen for maternally expressed imprinted genes, and other screens for imprinted and endosperm-expressed genes is discussed.

Dataset Information

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

Publications

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

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