Cargando…
Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis
The female gametophytes of angiosperms contain cells with distinct functions, such as those that enable reproduction via pollen tube attraction and fertilization. Although the female gametophyte undergoes unique developmental processes, such as several rounds of nuclear division without cell plate f...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7997040/ https://www.ncbi.nlm.nih.gov/pubmed/33770073 http://dx.doi.org/10.1371/journal.pbio.3001123 |
_version_ | 1783670237418225664 |
---|---|
author | Susaki, Daichi Suzuki, Takamasa Maruyama, Daisuke Ueda, Minako Higashiyama, Tetsuya Kurihara, Daisuke |
author_facet | Susaki, Daichi Suzuki, Takamasa Maruyama, Daisuke Ueda, Minako Higashiyama, Tetsuya Kurihara, Daisuke |
author_sort | Susaki, Daichi |
collection | PubMed |
description | The female gametophytes of angiosperms contain cells with distinct functions, such as those that enable reproduction via pollen tube attraction and fertilization. Although the female gametophyte undergoes unique developmental processes, such as several rounds of nuclear division without cell plate formation and final cellularization, it remains unknown when and how the cell fate is determined during development. Here, we visualized the living dynamics of female gametophyte development and performed transcriptome analysis of individual cell types to assess the cell fate specifications in Arabidopsis thaliana. We recorded time lapses of the nuclear dynamics and cell plate formation from the 1-nucleate stage to the 7-cell stage after cellularization using an in vitro ovule culture system. The movies showed that the nuclear division occurred along the micropylar–chalazal (distal–proximal) axis. During cellularization, the polar nuclei migrated while associating with the forming edge of the cell plate, and then, migrated toward each other to fuse linearly. We also tracked the gene expression dynamics and identified that the expression of MYB98pro::GFP–MYB98, a synergid-specific marker, was initiated just after cellularization in the synergid, egg, and central cells and was then restricted to the synergid cells. This indicated that cell fates are determined immediately after cellularization. Transcriptome analysis of the female gametophyte cells of the wild-type and myb98 mutant revealed that the myb98 synergid cells had egg cell–like gene expression profiles. Although in myb98, egg cell–specific gene expression was properly initiated in the egg cells only after cellularization, but subsequently expressed ectopically in one of the 2 synergid cells. These results, together with the various initiation timings of the egg cell–specific genes, suggest complex regulation of the individual gametophyte cells, such as cellularization-triggered fate initiation, MYB98-dependent fate maintenance, cell morphogenesis, and organelle positioning. Our system of live-cell imaging and cell type–specific gene expression analysis provides insights into the dynamics and mechanisms of cell fate specifications in the development of female gametophytes in plants. |
format | Online Article Text |
id | pubmed-7997040 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-79970402021-04-06 Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis Susaki, Daichi Suzuki, Takamasa Maruyama, Daisuke Ueda, Minako Higashiyama, Tetsuya Kurihara, Daisuke PLoS Biol Research Article The female gametophytes of angiosperms contain cells with distinct functions, such as those that enable reproduction via pollen tube attraction and fertilization. Although the female gametophyte undergoes unique developmental processes, such as several rounds of nuclear division without cell plate formation and final cellularization, it remains unknown when and how the cell fate is determined during development. Here, we visualized the living dynamics of female gametophyte development and performed transcriptome analysis of individual cell types to assess the cell fate specifications in Arabidopsis thaliana. We recorded time lapses of the nuclear dynamics and cell plate formation from the 1-nucleate stage to the 7-cell stage after cellularization using an in vitro ovule culture system. The movies showed that the nuclear division occurred along the micropylar–chalazal (distal–proximal) axis. During cellularization, the polar nuclei migrated while associating with the forming edge of the cell plate, and then, migrated toward each other to fuse linearly. We also tracked the gene expression dynamics and identified that the expression of MYB98pro::GFP–MYB98, a synergid-specific marker, was initiated just after cellularization in the synergid, egg, and central cells and was then restricted to the synergid cells. This indicated that cell fates are determined immediately after cellularization. Transcriptome analysis of the female gametophyte cells of the wild-type and myb98 mutant revealed that the myb98 synergid cells had egg cell–like gene expression profiles. Although in myb98, egg cell–specific gene expression was properly initiated in the egg cells only after cellularization, but subsequently expressed ectopically in one of the 2 synergid cells. These results, together with the various initiation timings of the egg cell–specific genes, suggest complex regulation of the individual gametophyte cells, such as cellularization-triggered fate initiation, MYB98-dependent fate maintenance, cell morphogenesis, and organelle positioning. Our system of live-cell imaging and cell type–specific gene expression analysis provides insights into the dynamics and mechanisms of cell fate specifications in the development of female gametophytes in plants. Public Library of Science 2021-03-26 /pmc/articles/PMC7997040/ /pubmed/33770073 http://dx.doi.org/10.1371/journal.pbio.3001123 Text en © 2021 Susaki et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Susaki, Daichi Suzuki, Takamasa Maruyama, Daisuke Ueda, Minako Higashiyama, Tetsuya Kurihara, Daisuke Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title | Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title_full | Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title_fullStr | Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title_full_unstemmed | Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title_short | Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis |
title_sort | dynamics of the cell fate specifications during female gametophyte development in arabidopsis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7997040/ https://www.ncbi.nlm.nih.gov/pubmed/33770073 http://dx.doi.org/10.1371/journal.pbio.3001123 |
work_keys_str_mv | AT susakidaichi dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis AT suzukitakamasa dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis AT maruyamadaisuke dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis AT uedaminako dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis AT higashiyamatetsuya dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis AT kuriharadaisuke dynamicsofthecellfatespecificationsduringfemalegametophytedevelopmentinarabidopsis |