Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation
Abstract 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...
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doaj-fe06075838704659ab788f8fb859cb262020-11-25T02:41:59ZengBMCBMC Plant Biology1471-22292018-09-0118111510.1186/s12870-018-1405-3Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formationMalgorzata Lichocka0Wojciech Rymaszewski1Karolina Morgiewicz2Izabela Barymow-Filoniuk3Aleksander Chlebowski4Miroslaw Sobczak5Marcus A. Samuel6Elmon Schmelzer7Magdalena Krzymowska8Jacek Hennig9Institute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesDepartment of Botany, Warsaw University of Life Sciences (SGGW)Department of Biological Sciences, University of CalgaryMax-Planck Institute for Plant Breeding ResearchInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesAbstract 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.http://link.springer.com/article/10.1186/s12870-018-1405-3ArabidopsisAccessionAnnexinPollen grainSeedEmbryo |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Malgorzata Lichocka Wojciech Rymaszewski Karolina Morgiewicz Izabela Barymow-Filoniuk Aleksander Chlebowski Miroslaw Sobczak Marcus A. Samuel Elmon Schmelzer Magdalena Krzymowska Jacek Hennig |
spellingShingle |
Malgorzata Lichocka Wojciech Rymaszewski Karolina Morgiewicz Izabela Barymow-Filoniuk Aleksander Chlebowski Miroslaw Sobczak Marcus A. Samuel Elmon Schmelzer Magdalena Krzymowska Jacek Hennig Nucleus- and plastid-targeted annexin 5 promotes reproductive development in Arabidopsis and is essential for pollen and embryo formation BMC Plant Biology Arabidopsis Accession Annexin Pollen grain Seed Embryo |
author_facet |
Malgorzata Lichocka Wojciech Rymaszewski Karolina Morgiewicz Izabela Barymow-Filoniuk Aleksander Chlebowski Miroslaw Sobczak Marcus A. Samuel Elmon Schmelzer Magdalena Krzymowska Jacek Hennig |
author_sort |
Malgorzata Lichocka |
title |
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_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_sort |
nucleus- and plastid-targeted annexin 5 promotes reproductive development in arabidopsis and is essential for pollen and embryo formation |
publisher |
BMC |
series |
BMC Plant Biology |
issn |
1471-2229 |
publishDate |
2018-09-01 |
description |
Abstract 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. |
topic |
Arabidopsis Accession Annexin Pollen grain Seed Embryo |
url |
http://link.springer.com/article/10.1186/s12870-018-1405-3 |
work_keys_str_mv |
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