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The difference between the first and last two categories is significant. A — C Boxes show medians and the interquartile range, and error bars show the full range excluding outliers. D The percentage of noncollapsed seeds of the indicated genotypes. E The percentage of germinated seeds of the indicated genotypes. The kyp suvh5 suvh6 triple mutant is nearly completely depleted of H3K9me2 Stroud et al. In contrast, there was no enrichment for down-regulated genes 9. Up-regulated TE-associated genes were preferentially expressed in the chalazal region of the endosperm Fig.

Gain of H3K9me2 at TEs coincides with increased expression of neighboring genes. B Cluster analysis of up-regulated TE-associated genes based on their expression in embryos and the endosperm during heart and cotyledon stages of seed development. Each row represents a gene, and each column represents a tissue type.

Red and green indicate tissues in which a particular gene is highly expressed or repressed, respectively. Data were normalized to PP2A. Data show results from biological triplicates.

S9C , suggesting an antagonistic relationship between both marks. This interpretation is consistent with previous reports revealing inhibition of the RdDM pathway by heterochromatin with its hallmark, H3K9me2 Schoft et al. The boxes show medians and the interquartile range, and the error bars show the full range excluding outliers. The difference between group 1 and group 5 is significant.

D The percentage of noncollapsed seeds derived from the indicated crosses. E The percentage of germinated seeds derived from the indicated crosses. All differences are significant. Genotypes are specified in A. S10 , which argues against this possibility. Consistent with the reported inhibition of the RdDM pathway by heterochromatin Schoft et al. Reduced CHH methylation correlated with increased expression of neighboring genes, in agreement with the observation that DNA-methylated TEs exert a repressive effect on neighboring genes Hollister and Gaut ; Wang et al.

Histone H1 condenses chromatin and inhibits nucleosome mobility and transcription in vitro Robinson and Rhodes , suggesting that transcriptional inhibition by H3K9me2- and H1-mediated chromatin condensation are functionally connected. Activity of DRD1 has been suggested to be inhibited by heterochromatic nucleosomes Zemach et al. Our data bear striking similarities to hybrid lethality between Drosophila melanogaster and Drosophila simulans caused by the heterochromatin-interacting proteins hybrid male rescue Hmr and lethal hybrid rescue Lhr.

Both proteins form a heterochromatic complex with heterochromatin protein 1a, and, while mutants in both genes are viable, their combination in F1 hybrid males is lethal Brideau et al.

Hmr and Lhr are not ubiquitous heterochromatin proteins but localize to a specific subfraction of repeat elements Satyaki et al. Furthermore, Hmr and Lhr are dosage-sensitive Barbash et al.

TEs coevolve with mechanisms suppressing their activity; therefore, hybridizations of species differing in TE load are expected to cause incompatibilities as a consequence of unleashed TE activity Blumenstiel ; Castillo and Moyle This idea has been well established in Drosophila by studies revealing that intraspecific crosses result in hybrid dysgenesis as a consequence of increased transcription and transposition of specific TEs in dysgenic germlines Malone et al.

Similarly, hybridizations of A. Nevertheless, our data show that differences in dosage or function of chromatin regulators in parental species can also cause off-target effects in hybrids that are not associated with increased TE expression but rather affect neighboring gene expression. A similar effect has been reported in Drosophila hybrids, where Lhr and Hmr cause increased expression of genes located in pericentromeric heterochromatin, while their functional role in the parental species is likely to repress repeat elements Satyaki et al.

There are striking similarities between interploidy and interspecies hybrid seed defects, indicative of a common mechanistic basis Josefsson et al. Interploidy hybridizations disrupt the balance of two maternal genomes to one paternal genome in the endosperm, resulting in unbalanced contributions of imprinted genes such as ADM , AHL10 , and SUVH9.

Strikingly, chromatin regulators are overrepresented among PEGs identified in plants Gehring et al. Chromatin regulatory genes are inherently dosage-sensitive Henikoff ; Reuter and Spierer , which possibly makes them prone to become controlled by imprinting mechanisms. Gametic histones are rapidly exchanged after fertilization Ingouff et al.

In conclusion, our study reveals that interploidy hybridizations cause deregulated expression of imprinted dosage-sensitive chromatin regulators targeting TEs, adding strong support to the hypothesis that genetic conflict between TEs and host fitness drive the evolution of hybrid incompatibility. If not otherwise indicated, ahl was used for all experiments.

The suvh mutant in Col background was obtained from Judith Bender, and osd introgressed into the Col background and osd in L er background d’Erfurth et al.

The adm-1 and adm-2 mutants were described previously Kradolfer et al. For complementation experiments using different promoters, the adm-1 mutant was used, while the adm-2 mutant was used for ChIP-seq chromatin immunoprecipitation [ChIP] combined with high-throughput sequencing and bisulfite sequencing experiments. For crosses, designated female partners were emasculated, and the pistils were hand-pollinated at 2 d after emasculation. TAP experiments were performed with mg of total protein extract following published procedures Van Leene et al.

Protein interactors were identified by mass spectrometry using an LTQ Orbitrap Velos mass spectrometer. Proteins with at least two matched high-confidence peptides were retained.

Background proteins were filtered out based on the frequency of the occurrence of the copurified proteins in a large data set containing TAP experiments using different baits Van Leene et al. Suspensions of A. At 48 h after infiltration, water-mounted sections of leaf tissue were examined by confocal microscopy Zeiss, LSM The YFP channel was excited with a nm laser, and the emission signal was collected in a wavelength window between and nm.

Seeds from five siliques were collected for each cross and frozen together with 1. The samples were ground in a Silamat S5 Ivoclar Vivadent three times for 7 sec. All experiments were performed in two biological replicates. The osd mutant was introgressed from Nossen into Col d’Erfurth et al. We therefore mapped reads of spiked-in L er material to chromosome 5 to calculate contamination.

Experiments were performed in two biological replicates. Endosperm ChIP-seq libraries were generated using the Microplex library preparation kit Diagenode following the manufacturer’s protocol with 1 ng of starting material. Mapped reads were deduplicated and extended to the estimated average length of the genomic fragments bp. Coverage was estimated and normalized to 10 million reads. These data were standardized and normalized for comparative purposes across samples with a z -score Cheadle et al.

The 4-DAP bisulfite-treated samples were sequenced in bp paired-end mode. After assessing the quality Supplemental Table S7 and trimming, each read was split in two bp-long fragments. Splitting the reads and mapping them in single-end mode improved the mapping efficiency substantially in relation to other tested options. Duplicated reads aligning to the same genomic position were eliminated before calculating methylation levels.

Cytosine methylation was visualized separately for CG, CHG, and CHH cytosine contexts, with bedGraph files representing average methylation values in bp bins across the genome. The bisulfite conversion rate for each library was calculated based on the methylation status of cytosines in the CHH context from reads mapping to the chloroplast genome.

The data of 6-DAP bisulfite-treated samples have been published previously Schatlowski et al. RNA sequencing data used in this study have been published previously Wolff et al. We thank Markus Kuhlmann for providing seeds of the suvh2 suvh9 double mutant, Raphael Mercier for kindly providing seeds of osd1 , and Judith Bender for sharing seeds of the suvh triple mutant.

Supplemental material is available for this article. Article published online ahead of print. Genes Dev. Author information Article notes Copyright and License information Disclaimer. Corresponding author: es. Received Mar 24; Accepted Jun Abstract Hybrid seed lethality as a consequence of interspecies or interploidy hybridizations is a major mechanism of reproductive isolation in plants.

Keywords: hybrid incompatibility, heterochromatin, imprinted genes, endosperm, transposable elements, polyploidy. Open in a separate window. Figure 1. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. BiFC assays Suspensions of A. Library preparation and sequencing Endosperm ChIP-seq libraries were generated using the Microplex library preparation kit Diagenode following the manufacturer’s protocol with 1 ng of starting material.

Supplementary Material Supplemental Material: Click here to view. Footnotes Supplemental material is available for this article. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci : — Mammalian genomic imprinting.

Cold Spring Harb Perspect Biol 3 : a Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Dosage-dependent gene regulation in multicellular eukaryotes: implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev Biol : — Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet 27 : 23— Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants.

Am Nat : — Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science : — The endosperm in seed development. Bot Rev : — Early disruption of maternal-zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. Plant Cell 25 : — PLoS Genet 8 : e Evolutionary implications of mechanistic models of TE-mediated hybrid incompatibility.

Int J Evol Biol : Analysis of microarray data using Z score transformation. J Mol Diagn 5 : 73— Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana.

Plant J 16 : — More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9 : — The DnaJ-related factor Mrj interacts with nuclear factor of activated T cells c3 and mediates transcriptional repression through class II histone deacetylase recruitment. Mol Cell Biol 25 : — Turning meiosis into mitosis. PLoS Biol 7 : e PLoS Biol 6 : e Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants.

Cell : — Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One 6 : e Plant Cell 26 : — Curr Biol 23 : R—R A ubiquitin promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies.

Plant J 64 : — Imprinting in the endosperm: a possible role in preventing wide hybridization. PLoS Genet 12 : e Endosperm cellularization defines an important developmental transition for embryo development. Development : — Position effects and variegation enhancers in an autosomal region of Drosophila melanogaster. Genetics 93 : — Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression.

Genome Res 19 : — Regulation of imprinted gene expression in Arabidopsis endosperm. Plant J 90 : — Curr Biol 17 : — Curr Biol 20 : — Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division.

Plant J 65 : — Acronym Attic. Samples in periodicals archive: 1 Checkpoint Learning User Bulletin June 22, This user bulletin reviews software changes made to the latest release of Checkpoint Learning. SER No. Affected Version No So, truncate. User Bulletin No. Isolation of total RNA from 1 g plant material or 1 x cells. SP1 User Bulletin. Although the administrators and moderators of Sophos User Bulletin Board will attempt to keep all objectionable messages off this forum, it is impossible for us to

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