Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort
The nuclear lamina (NL) is a complex network of nuclear lamins and lamina-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of NL. Plant genomes do not encode any homologs of these in...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-05-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.670306/full |
| _version_ | 1818672240419405824 |
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| author | Nan Wang Nan Wang Ezgi Süheyla Karaaslan Natalie Faiss Kenneth Wayne Berendzen Chang Liu Chang Liu |
| author_facet | Nan Wang Nan Wang Ezgi Süheyla Karaaslan Natalie Faiss Kenneth Wayne Berendzen Chang Liu Chang Liu |
| author_sort | Nan Wang |
| collection | DOAJ |
| description | The nuclear lamina (NL) is a complex network of nuclear lamins and lamina-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of NL. Plant genomes do not encode any homologs of these intermediate filaments, yet plant nuclei contain lamina-like structures that are present in their nuclei. In Arabidopsis thaliana, CROWDED NUCLEI (CRWN), which are required for maintaining structural integrity of the nucleus and specific perinuclear chromatin anchoring, are strong candidates for plant lamin proteins. Recent studies revealed additional roles of Arabidopsis Nuclear Matrix Constituent Proteins (NMCPs) in modulating plants’ response to pathogen and abiotic stresses. However, detailed analyses of Arabidopsis NMCP activities are challenging due to the presence of multiple homologs and their functional redundancy. In this study, we investigated the sole NMCP gene in the liverwort Marchantia polymorpha (MpNMCP). We found that MpNMCP proteins preferentially were localized to the nuclear periphery. Using CRISPR/Cas9 techniques, we generated an MpNMCP loss-of-function mutant, which displayed reduced growth rate and curly thallus lobes. At an organelle level, MpNMCP mutants did not show any alteration in nuclear morphology. Transcriptome analyses indicated that MpNMCP was involved in regulating biotic and abiotic stress responses. Additionally, a highly repetitive genomic region on the male sex chromosome, which was preferentially tethered at the nuclear periphery in wild-type thalli, decondensed in the MpNMCP mutants and located in the nuclear interior. This perinuclear chromatin anchoring, however, was not directly controlled by MpNMCP. Altogether, our results unveiled that NMCP in plants have conserved functions in modulating stress responses. |
| first_indexed | 2024-12-17T07:36:45Z |
| format | Article |
| id | doaj.art-2798f9ef279d40c6ba4945da09b24a61 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-17T07:36:45Z |
| publishDate | 2021-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-2798f9ef279d40c6ba4945da09b24a612022-12-21T21:58:17ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-05-011210.3389/fpls.2021.670306670306Characterization of a Plant Nuclear Matrix Constituent Protein in LiverwortNan Wang0Nan Wang1Ezgi Süheyla Karaaslan2Natalie Faiss3Kenneth Wayne Berendzen4Chang Liu5Chang Liu6Center for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyInstitute of Biology, University of Hohenheim, Stuttgart, GermanyCenter for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyCenter for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyCenter for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyCenter for Plant Molecular Biology (ZMBP), University of Tübingen, Tübingen, GermanyInstitute of Biology, University of Hohenheim, Stuttgart, GermanyThe nuclear lamina (NL) is a complex network of nuclear lamins and lamina-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of NL. Plant genomes do not encode any homologs of these intermediate filaments, yet plant nuclei contain lamina-like structures that are present in their nuclei. In Arabidopsis thaliana, CROWDED NUCLEI (CRWN), which are required for maintaining structural integrity of the nucleus and specific perinuclear chromatin anchoring, are strong candidates for plant lamin proteins. Recent studies revealed additional roles of Arabidopsis Nuclear Matrix Constituent Proteins (NMCPs) in modulating plants’ response to pathogen and abiotic stresses. However, detailed analyses of Arabidopsis NMCP activities are challenging due to the presence of multiple homologs and their functional redundancy. In this study, we investigated the sole NMCP gene in the liverwort Marchantia polymorpha (MpNMCP). We found that MpNMCP proteins preferentially were localized to the nuclear periphery. Using CRISPR/Cas9 techniques, we generated an MpNMCP loss-of-function mutant, which displayed reduced growth rate and curly thallus lobes. At an organelle level, MpNMCP mutants did not show any alteration in nuclear morphology. Transcriptome analyses indicated that MpNMCP was involved in regulating biotic and abiotic stress responses. Additionally, a highly repetitive genomic region on the male sex chromosome, which was preferentially tethered at the nuclear periphery in wild-type thalli, decondensed in the MpNMCP mutants and located in the nuclear interior. This perinuclear chromatin anchoring, however, was not directly controlled by MpNMCP. Altogether, our results unveiled that NMCP in plants have conserved functions in modulating stress responses.https://www.frontiersin.org/articles/10.3389/fpls.2021.670306/fullMarchantiaNMCPnuclear peripherynuclear laminanuclear envelope |
| spellingShingle | Nan Wang Nan Wang Ezgi Süheyla Karaaslan Natalie Faiss Kenneth Wayne Berendzen Chang Liu Chang Liu Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort Frontiers in Plant Science Marchantia NMCP nuclear periphery nuclear lamina nuclear envelope |
| title | Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort |
| title_full | Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort |
| title_fullStr | Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort |
| title_full_unstemmed | Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort |
| title_short | Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort |
| title_sort | characterization of a plant nuclear matrix constituent protein in liverwort |
| topic | Marchantia NMCP nuclear periphery nuclear lamina nuclear envelope |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.670306/full |
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