Widespread imprinting of transposable elements and young genes in the maize endosperm

Fertilization and seed development is a critical time in the plant life cycle, and coordinated development of the embryo and endosperm are required to produce a viable seed. In the endosperm, some genes show imprinted expression where transcripts are derived primarily from one parental genome. Imprinted gene expression has been observed across many flowering plant species, though only a small proportion of genes are imprinted. Understanding the rate of turnover for gain or loss of imprinted expression has been complicated by the reliance on single nucleotide polymorphisms between alleles to enable testing for imprinting. Here, we develop a method to use whole genome assemblies of multiple genotypes to assess for imprinting of both shared and variable portions of the genome using data from reciprocal crosses. This reveals widespread maternal expression of genes and transposable elements with presence-absence variation within maize and across species. Most maternally expressed features are expressed primarily in the endosperm, suggesting that maternal de-repression in the central cell facilitates expression. Furthermore, maternally expressed TEs are enriched for maternal expression of the nearest gene. Read alignments over maternal TE-gene pairs indicate fused transcripts, suggesting that variable TEs contribute imprinted expression of nearby genes.

[1]  Mary Gehring,et al.  Identification and Comparison of Imprinted Genes Across Plant Species. , 2020, Methods in molecular biology.

[2]  Nathan M. Springer,et al.  Dynamic Patterns of Transcript Abundance of Transposable Element Families in Maize , 2019, G3: Genes, Genomes, Genetics.

[3]  C. Köhler,et al.  The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons , 2019, bioRxiv.

[4]  Nathan M. Springer,et al.  Dynamic Patterns of Gene Expression Additivity and Regulatory Variation throughout Maize Development. , 2019, Molecular plant.

[5]  Alex B. Brohammer,et al.  Transposable elements contribute to dynamic genome content in maize , 2019, bioRxiv.

[6]  Christine G. Elsik,et al.  MaizeGDB 2018: the maize multi-genome genetics and genomics database , 2018, Nucleic Acids Res..

[7]  Daniel L. Vera,et al.  The maize W22 genome provides a foundation for functional genomics and transposon biology , 2018, Nature Genetics.

[8]  U. Grossniklaus,et al.  Consistent Reanalysis of Genome-wide Imprinting Studies in Plants Using Generalized Linear Models Increases Concordance across Datasets , 2017, bioRxiv.

[9]  Michael D. Nodine,et al.  Widespread Contamination of Arabidopsis Embryo and Endosperm Transcriptome Data Sets[OPEN] , 2017, Plant Cell.

[10]  Kevin L. Schneider,et al.  Improved maize reference genome with single-molecule technologies , 2017, Nature.

[11]  D. Zilberman,et al.  DNA demethylation is initiated in the central cells of Arabidopsis and rice , 2016, Proceedings of the National Academy of Sciences.

[12]  Kevin L. Childs,et al.  Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize[OPEN] , 2016, Plant Cell.

[13]  B. Laenen,et al.  Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae , 2016, Plant Cell.

[14]  C. Köhler,et al.  Parental epigenetic asymmetry of PRC2‐mediated histone modifications in the Arabidopsis endosperm , 2016, The EMBO journal.

[15]  R. Sekhon,et al.  An Expanded Maize Gene Expression Atlas based on RNA Sequencing and its Use to Explore Root Development , 2016, The plant genome.

[16]  Bao Liu,et al.  Genome-wide screen of genes imprinted in sorghum endosperm, and the roles of allelic differential cytosine methylation. , 2016, The Plant journal : for cell and molecular biology.

[17]  Jack Gardiner,et al.  MaizeGDB: The Maize Genetics and Genomics Database. , 2016, Methods in molecular biology.

[18]  James C. Schnable,et al.  Genome evolution in maize: from genomes back to genes. , 2015, Annual review of plant biology.

[19]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[20]  Paul Theodor Pyl,et al.  HTSeq—a Python framework to work with high-throughput sequencing data , 2014, bioRxiv.

[21]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[22]  D. Haig,et al.  Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting , 2013, Heredity.

[23]  G. Bell,et al.  Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting , 2014, eLife.

[24]  W. Jin,et al.  Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize , 2014, Genome research.

[25]  M. A. Pedraza,et al.  Insights into the Maize Pan-Genome and Pan-Transcriptome[W][OPEN] , 2014, Plant Cell.

[26]  Nathan M. Springer,et al.  Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species , 2013, Proceedings of the National Academy of Sciences.

[27]  D. Zilberman,et al.  Active DNA Demethylation in Plant Companion Cells Reinforces Transposon Methylation in Gametes , 2012, Science.

[28]  D. Haig Retroviruses and the Placenta , 2012, Current Biology.

[29]  Lin Fang,et al.  Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes , 2011, Nature Biotechnology.

[30]  Patrick S. Schnable,et al.  Parent-of-Origin Effects on Gene Expression and DNA Methylation in the Maize Endosperm[W] , 2011, Plant Cell.

[31]  Ming Luo,et al.  A Genome-Wide Survey of Imprinted Genes in Rice Seeds Reveals Imprinting Primarily Occurs in the Endosperm , 2011, PLoS genetics.

[32]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[33]  Robert L. Fischer,et al.  Regulation of imprinted gene expression in Arabidopsis endosperm , 2011, Proceedings of the National Academy of Sciences.

[34]  L. Hennig,et al.  H3K27me3 Profiling of the Endosperm Implies Exclusion of Polycomb Group Protein Targeting by DNA Methylation , 2010, PLoS genetics.

[35]  Patrick S. Schnable,et al.  Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content , 2009, PLoS genetics.

[36]  Steven Henikoff,et al.  Extensive Demethylation of Repetitive Elements During Seed Development Underlies Gene Imprinting , 2009, Science.

[37]  B. Dilkes,et al.  A Differential Dosage Hypothesis for Parental Effects in Seed Development , 2004, The Plant Cell Online.

[38]  W. Peacock,et al.  Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Kermicle Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. , 1970, Genetics.