Cargando…
Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation
BACKGROUND: Pollen development is a strictly controlled post-meiotic process during which microspores differentiate into microgametophytes and profound structural and functional changes occur in organelles. Annexin 5 is a calcium- and lipid-binding protein that is highly expressed in pollen grains a...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2018
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6127919/ https://www.ncbi.nlm.nih.gov/pubmed/30189843 http://dx.doi.org/10.1186/s12870-018-1405-3 |
_version_ | 1783353556777041920 |
---|---|
author | Lichocka, Malgorzata Rymaszewski, Wojciech Morgiewicz, Karolina Barymow-Filoniuk, Izabela Chlebowski, Aleksander Sobczak, Miroslaw Samuel, Marcus A. Schmelzer, Elmon Krzymowska, Magdalena Hennig, Jacek |
author_facet | Lichocka, Malgorzata Rymaszewski, Wojciech Morgiewicz, Karolina Barymow-Filoniuk, Izabela Chlebowski, Aleksander Sobczak, Miroslaw Samuel, Marcus A. Schmelzer, Elmon Krzymowska, Magdalena Hennig, Jacek |
author_sort | Lichocka, Malgorzata |
collection | PubMed |
description | BACKGROUND: Pollen development is a strictly controlled post-meiotic process during which microspores differentiate into microgametophytes and profound structural and functional changes occur in organelles. Annexin 5 is a calcium- and lipid-binding protein that is highly expressed in pollen grains and regulates pollen development and physiology. To gain further insights into the role of ANN5 in Arabidopsis development, we performed detailed phenotypic characterization of Arabidopsis plants with modified ANN5 levels. In addition, interaction partners and subcellular localization of ANN5 were analyzed to investigate potential functions of ANN5 at cellular level. RESULTS: Here, we report that RNAi-mediated suppression of ANN5 results in formation of smaller pollen grains, enhanced pollen lethality, and delayed pollen tube growth. ANN5 RNAi knockdown plants also displayed aberrant development during the transition from the vegetative to generative phase and during embryogenesis, reflected by delayed bolting time and reduced embryo size, respectively. At the subcellular level, ANN5 was delivered to the nucleus, nucleolus, and cytoplasm, and was frequently localized in plastid nucleoids, suggesting a likely role in interorganellar communication. Furthermore, ANN5-YFP co-immunoprecipitated with RABE1b, a putative GTPase, and interaction in planta was confirmed in plastidial nucleoids using FLIM-FRET analysis. CONCLUSIONS: Our findings let us to propose that ANN5 influences basal cell homeostasis via modulation of plastid activity during pollen maturation. We hypothesize that the role of ANN5 is to orchestrate the plastidial and nuclear genome activities via protein-protein interactions however not only in maturing pollen but also during the transition from the vegetative to the generative growth and seed development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1405-3) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6127919 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-61279192018-09-10 Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation Lichocka, Malgorzata Rymaszewski, Wojciech Morgiewicz, Karolina Barymow-Filoniuk, Izabela Chlebowski, Aleksander Sobczak, Miroslaw Samuel, Marcus A. Schmelzer, Elmon Krzymowska, Magdalena Hennig, Jacek BMC Plant Biol Research Article BACKGROUND: Pollen development is a strictly controlled post-meiotic process during which microspores differentiate into microgametophytes and profound structural and functional changes occur in organelles. Annexin 5 is a calcium- and lipid-binding protein that is highly expressed in pollen grains and regulates pollen development and physiology. To gain further insights into the role of ANN5 in Arabidopsis development, we performed detailed phenotypic characterization of Arabidopsis plants with modified ANN5 levels. In addition, interaction partners and subcellular localization of ANN5 were analyzed to investigate potential functions of ANN5 at cellular level. RESULTS: Here, we report that RNAi-mediated suppression of ANN5 results in formation of smaller pollen grains, enhanced pollen lethality, and delayed pollen tube growth. ANN5 RNAi knockdown plants also displayed aberrant development during the transition from the vegetative to generative phase and during embryogenesis, reflected by delayed bolting time and reduced embryo size, respectively. At the subcellular level, ANN5 was delivered to the nucleus, nucleolus, and cytoplasm, and was frequently localized in plastid nucleoids, suggesting a likely role in interorganellar communication. Furthermore, ANN5-YFP co-immunoprecipitated with RABE1b, a putative GTPase, and interaction in planta was confirmed in plastidial nucleoids using FLIM-FRET analysis. CONCLUSIONS: Our findings let us to propose that ANN5 influences basal cell homeostasis via modulation of plastid activity during pollen maturation. We hypothesize that the role of ANN5 is to orchestrate the plastidial and nuclear genome activities via protein-protein interactions however not only in maturing pollen but also during the transition from the vegetative to the generative growth and seed development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1405-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-06 /pmc/articles/PMC6127919/ /pubmed/30189843 http://dx.doi.org/10.1186/s12870-018-1405-3 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Lichocka, Malgorzata Rymaszewski, Wojciech Morgiewicz, Karolina Barymow-Filoniuk, Izabela Chlebowski, Aleksander Sobczak, Miroslaw Samuel, Marcus A. Schmelzer, Elmon Krzymowska, Magdalena Hennig, Jacek Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title | Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title_full | Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title_fullStr | Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title_full_unstemmed | Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title_short | Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation |
title_sort | nucleus- and plastid-targeted annexin 5 promotes reproductive development in arabidopsis and is essential for pollen and embryo formation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6127919/ https://www.ncbi.nlm.nih.gov/pubmed/30189843 http://dx.doi.org/10.1186/s12870-018-1405-3 |
work_keys_str_mv | AT lichockamalgorzata nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT rymaszewskiwojciech nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT morgiewiczkarolina nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT barymowfiloniukizabela nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT chlebowskialeksander nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT sobczakmiroslaw nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT samuelmarcusa nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT schmelzerelmon nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT krzymowskamagdalena nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation AT hennigjacek nucleusandplastidtargetedannexin5promotesreproductivedevelopmentinarabidopsisandisessentialforpollenandembryoformation |