The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons
- Swedish University of Agricultural Sciences, Sweden
Abstract
MADS-box transcription factors (TFs) are ubiquitous in eukaryotic organisms and play major roles during plant development. Nevertheless, their function in seed development remains largely unknown. Here we show that the imprinted Arabidopsis thaliana MADS-box TF PHERES1 (PHE1) is a master regulator of paternally expressed imprinted genes, as well as of non-imprinted key regulators of endosperm development. PHE1 binding sites show distinct epigenetic modifications on maternal and paternal alleles, correlating with parental-specific transcriptional activity. Importantly, we show that the CArG-box-like DNA-binding motifs bound by PHE1 have been distributed by RC/Helitron transposable elements. Our data provide an example of molecular domestication of these elements, which by distributing PHE1 binding sites throughout the genome, have facilitated the recruitment of crucial endosperm regulators into a single transcriptional network.
Data availability
ChIP-seq data generated in this study is available at NCBI's Gene Expression Omnibus database (https://www.ncbi.nlm.nih.gov/geo/), under the accession number GSE129744.
-
Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endospermNCBI Gene Expression Omnibus, GSE66585.
-
Paternal easiRNAs establish the triploid block in ArabidopsisNCBI Gene Expression Omnibus, GSE84122.
-
DNA hypomethylation bypasses the interploidy hybridization barrier in ArabidopsisNCBI Gene Expression Omnibus, GSE53642.
-
Epigenetic signatures associated with paternally-expressed imprinted genes in the endospermNCBI Gene Expression Omnibus, GSE119915.
-
Expression data from Arabidopsis Seed Compartments at 5 discrete stages of developmentNCBI Gene Expression Omnibus, GSE12404.
Article and author information
Author details
Duarte D Figueiredo
Funding
Vetenskapsrådet
- Claudia Köhler
Knut och Alice Wallenbergs Stiftelse
- Claudia Köhler
Goran Gustafsson Foundation for Research in Natural Sciences and Medicine
- Claudia Köhler
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Batista et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 5,073
- views
-
- 811
- downloads
-
- 80
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons
eLife 8:e50541.
https://doi.org/10.7554/eLife.50541
Further reading
-
- Genetics and Genomics
- Neuroscience
The central complex (CX) plays a key role in many higher-order functions of the insect brain including navigation and activity regulation. Genetic tools for manipulating individual cell types, and knowledge of what neurotransmitters and neuromodulators they express, will be required to gain mechanistic understanding of how these functions are implemented. We generated and characterized split-GAL4 driver lines that express in individual or small subsets of about half of CX cell types. We surveyed neuropeptide and neuropeptide receptor expression in the central brain using fluorescent in situ hybridization. About half of the neuropeptides we examined were expressed in only a few cells, while the rest were expressed in dozens to hundreds of cells. Neuropeptide receptors were expressed more broadly and at lower levels. Using our GAL4 drivers to mark individual cell types, we found that 51 of the 85 CX cell types we examined expressed at least one neuropeptide and 21 expressed multiple neuropeptides. Surprisingly, all co-expressed a small molecule neurotransmitter. Finally, we used our driver lines to identify CX cell types whose activation affects sleep, and identified other central brain cell types that link the circadian clock to the CX. The well-characterized genetic tools and information on neuropeptide and neurotransmitter expression we provide should enhance studies of the CX.
-
- Evolutionary Biology
- Genetics and Genomics
Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in Drosophila melanogaster, we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with In(3 R)K favoring survival and In(3 L)Ok favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, In(3 L)Ok was also found to be less costly to the viability and/or longevity of males than females, whereas In(3 R)K was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism.
