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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Main Authors: Malgorzata Lichocka, Wojciech Rymaszewski, Karolina Morgiewicz, Izabela Barymow-Filoniuk, Aleksander Chlebowski, Miroslaw Sobczak, Marcus A. Samuel, Elmon Schmelzer, Magdalena Krzymowska, Jacek Hennig
Format: Article
Language:English
Published: BMC 2018-09-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1405-3
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spelling 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
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