Spatial and temporal regulation of parent-of-origin allelic expression in the endosperm

Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before i...

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Published inPlant physiology (Bethesda) Vol. 191; no. 2; pp. 986 - 1001
Main Authors van Ekelenburg, Yuri S, Hornslien, Karina S, Van Hautegem, Tom, Fendrych, Matyáš, Van Isterdael, Gert, Bjerkan, Katrine N, Miller, Jason R, Nowack, Moritz K, Grini, Paul E
Format Journal Article
LanguageEnglish
Published United States American Society of Plant Biologists 12.02.2023
Oxford University Press
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Abstract Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before it cellularizes and becomes a nutrient source for the growing embryo. Regional compartmentalization has been shown both in early and late endosperm development, and different transcriptional domains suggest divergent spatial and temporal regional functions. The analysis of the role of parent-of-origin allelic expression in the endosperm as a whole and the investigation of domain-specific functions have been hampered by the inaccessibility of the tissue for high-throughput transcriptome analyses and contamination from surrounding tissue. Here, we used fluorescence-activated nuclear sorting (FANS) of nuclear targeted GFP fluorescent genetic markers to capture parental-specific allelic expression from different developmental stages and specific endosperm domains. This approach allowed us to successfully identify differential genomic imprinting with temporal and spatial resolution. We used a systematic approach to report temporal regulation of imprinted genes in the endosperm, as well as region-specific imprinting in endosperm domains. Analysis of our data identified loci that are spatially differentially imprinted in one domain of the endosperm, while biparentally expressed in other domains. These findings suggest that the regulation of genomic imprinting is dynamic and challenge the canonical mechanisms for genomic imprinting.
AbstractList Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before it cellularizes and becomes a nutrient source for the growing embryo. Regional compartmentalization has been shown both in early and late endosperm development, and different transcriptional domains suggest divergent spatial and temporal regional functions. The analysis of the role of parent-of-origin allelic expression in the endosperm as a whole and the investigation of domain-specific functions have been hampered by the inaccessibility of the tissue for high-throughput transcriptome analyses and contamination from surrounding tissue. Here, we used fluorescence-activated nuclear sorting (FANS) of nuclear targeted GFP fluorescent genetic markers to capture parental-specific allelic expression from different developmental stages and specific endosperm domains. This approach allowed us to successfully identify differential genomic imprinting with temporal and spatial resolution. We used a systematic approach to report temporal regulation of imprinted genes in the endosperm, as well as region-specific imprinting in endosperm domains. Analysis of our data identified loci that are spatially differentially imprinted in one domain of the endosperm, while biparentally expressed in other domains. These findings suggest that the regulation of genomic imprinting is dynamic and challenge the canonical mechanisms for genomic imprinting.
Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before it cellularizes and becomes a nutrient source for the growing embryo. Regional compartmentalization has been shown both in early and late endosperm development, and different transcriptional domains suggest divergent spatial and temporal regional functions. The analysis of the role of parent-of-origin allelic expression in the endosperm as a whole and the investigation of domain-specific functions have been hampered by the inaccessibility of the tissue for high-throughput transcriptome analyses and contamination from surrounding tissue. Here, we used fluorescence-activated nuclear sorting (FANS) of nuclear targeted GFP fluorescent genetic markers to capture parental-specific allelic expression from different developmental stages and specific endosperm domains. This approach allowed us to successfully identify differential genomic imprinting with temporal and spatial resolution. We used a systematic approach to report temporal regulation of imprinted genes in the endosperm, as well as region-specific imprinting in endosperm domains. Analysis of our data identified loci that are spatially differentially imprinted in one domain of the endosperm, while biparentally expressed in other domains. These findings suggest that the regulation of genomic imprinting is dynamic and challenge the canonical mechanisms for genomic imprinting.Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before it cellularizes and becomes a nutrient source for the growing embryo. Regional compartmentalization has been shown both in early and late endosperm development, and different transcriptional domains suggest divergent spatial and temporal regional functions. The analysis of the role of parent-of-origin allelic expression in the endosperm as a whole and the investigation of domain-specific functions have been hampered by the inaccessibility of the tissue for high-throughput transcriptome analyses and contamination from surrounding tissue. Here, we used fluorescence-activated nuclear sorting (FANS) of nuclear targeted GFP fluorescent genetic markers to capture parental-specific allelic expression from different developmental stages and specific endosperm domains. This approach allowed us to successfully identify differential genomic imprinting with temporal and spatial resolution. We used a systematic approach to report temporal regulation of imprinted genes in the endosperm, as well as region-specific imprinting in endosperm domains. Analysis of our data identified loci that are spatially differentially imprinted in one domain of the endosperm, while biparentally expressed in other domains. These findings suggest that the regulation of genomic imprinting is dynamic and challenge the canonical mechanisms for genomic imprinting.
Author Bjerkan, Katrine N
Miller, Jason R
Hornslien, Karina S
van Ekelenburg, Yuri S
Grini, Paul E
Van Hautegem, Tom
Fendrych, Matyáš
Van Isterdael, Gert
Nowack, Moritz K
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Conflict of interest statement. The auhors declare no conflict of interest.
Present address: Department of Experimental Plant Biology, Charles University, Prague, Czech Republic.
P.E.G., J.R.M., and M.K.N. designed the research; Y.S.vE., T.vH., M.F., K.N.B., G.vI., M.N.K., and P.E.G. performed the experiments; Y.S.vE., K.S.H., T.vH., M.F., J.R.M., M.N.K., and P.E.G. analyzed and discussed the data; Y.S.vE., K.S.H., and P.E.G. wrote the article. All authors revised and approved the article.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plphys/pages/General-Instructions) is: Paul E. Grini.
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  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1019273108
– volume: 37
  start-page: 1
  year: 2009
  ident: 2023021208210802900_kiac520-B30
  article-title: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkn923
– volume: 142
  start-page: 1160
  year: 2006
  ident: 2023021208210802900_kiac520-B78
  article-title: Regulation of seed size by hypomethylation of maternal and paternal genomes
  publication-title: Plant Physiol
  doi: 10.1104/pp.106.088849
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Snippet Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such...
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SubjectTerms Alleles
DNA Methylation - genetics
Endosperm - genetics
Endosperm - metabolism
Epigenesis, Genetic
Gene Expression Regulation, Plant
Genomic Imprinting - genetics
Title Spatial and temporal regulation of parent-of-origin allelic expression in the endosperm
URI https://www.ncbi.nlm.nih.gov/pubmed/36437711
https://www.proquest.com/docview/2740906877
http://hdl.handle.net/10852/100629
https://pubmed.ncbi.nlm.nih.gov/PMC9922421
Volume 191
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