Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage
Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess frequently results in extensive endosperm proliferation without cellularization and seed abortion. We previously showed that loss of the RNA polymerase I...
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| Format: | Article |
| Language: | English |
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American Society of Plant Biologists (ASPB)
2020
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| Online Access: | https://hdl.handle.net/1721.1/126073 |
| _version_ | 1811085414363037696 |
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| author | Satyaki, Prasad R.V. Gehring, Mary |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Satyaki, Prasad R.V. Gehring, Mary |
| author_sort | Satyaki, Prasad R.V. |
| collection | MIT |
| description | Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess frequently results in extensive endosperm proliferation without cellularization and seed abortion. We previously showed that loss of the RNA polymerase IV gene NUCLEAR RNA POLYMERASE D1 (NRPD1) in tetraploid fathers represses seed abortion in paternal excess crosses. Here, we show genetically that RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is sufficient to determine the viability of paternal excess Arabidopsis (Arabidopsis thaliana) seeds. We compared transcriptomes, DNA methylation, and small RNAs from the endosperm of seeds from balanced crosses (diploid × diploid) and lethal (diploid × tetraploid) and viable paternal excess crosses (diploid × tetraploid nrpd1). Endosperms from both lethal and viable paternal excess seeds share widespread transcriptional and DNA methylation changes at genes and transposable elements. Interploidy seed abortion is thus unlikely to be caused by transposable elements or imprinted gene misregulation, and its repression by the loss of paternal RdDM is associated with only modest gene expression changes. Finally, using allele-specific transcription data, we present evidence for a transcriptional buffering system that increases the expression of maternal alleles and represses paternal alleles in response to excess paternal genomic dosage. These findings prompt reconsideration of models for dosage sensitivity in endosperm. |
| first_indexed | 2024-09-23T13:09:13Z |
| format | Article |
| id | mit-1721.1/126073 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T13:09:13Z |
| publishDate | 2020 |
| publisher | American Society of Plant Biologists (ASPB) |
| record_format | dspace |
| spelling | mit-1721.1/1260732022-10-01T13:23:14Z Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage Satyaki, Prasad R.V. Gehring, Mary Massachusetts Institute of Technology. Department of Biology Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess frequently results in extensive endosperm proliferation without cellularization and seed abortion. We previously showed that loss of the RNA polymerase IV gene NUCLEAR RNA POLYMERASE D1 (NRPD1) in tetraploid fathers represses seed abortion in paternal excess crosses. Here, we show genetically that RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is sufficient to determine the viability of paternal excess Arabidopsis (Arabidopsis thaliana) seeds. We compared transcriptomes, DNA methylation, and small RNAs from the endosperm of seeds from balanced crosses (diploid × diploid) and lethal (diploid × tetraploid) and viable paternal excess crosses (diploid × tetraploid nrpd1). Endosperms from both lethal and viable paternal excess seeds share widespread transcriptional and DNA methylation changes at genes and transposable elements. Interploidy seed abortion is thus unlikely to be caused by transposable elements or imprinted gene misregulation, and its repression by the loss of paternal RdDM is associated with only modest gene expression changes. Finally, using allele-specific transcription data, we present evidence for a transcriptional buffering system that increases the expression of maternal alleles and represses paternal alleles in response to excess paternal genomic dosage. These findings prompt reconsideration of models for dosage sensitivity in endosperm. National Science Foundation Division of Molecular and Cellular Biosciences (Grant 1453459) 2020-07-07T18:36:56Z 2020-07-07T18:36:56Z 2019-07 2019-12-05T14:29:02Z Article http://purl.org/eprint/type/JournalArticle 1040-4651 1532-298X https://hdl.handle.net/1721.1/126073 Satyaki, Prasad R. V. and Mary Gehring. "Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage." Plant Cell 31, 7 (July 2019): 1563-1578 © 2019 American Society of Plant Biologists en http://dx.doi.org/10.1105/tpc.19.00047 Plant Cell Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf American Society of Plant Biologists (ASPB) bioRxiv |
| spellingShingle | Satyaki, Prasad R.V. Gehring, Mary Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title | Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title_full | Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title_fullStr | Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title_full_unstemmed | Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title_short | Paternally Acting Canonical RNA-Directed DNA Methylation Pathway Genes Sensitize Arabidopsis Endosperm to Paternal Genome Dosage |
| title_sort | paternally acting canonical rna directed dna methylation pathway genes sensitize arabidopsis endosperm to paternal genome dosage |
| url | https://hdl.handle.net/1721.1/126073 |
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