Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge

In pollen and pollen tubes, immotile sperm cells are enclosed by an inner vegetative plasma membrane (IVPM), a single endomembrane originating from the vegetative-cell plasma membrane. It is widely believed that sperm cells must be removed from the IVPM prior to gamete associations and fusions; howe...

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Main Authors: Naoya Sugi, Rie Izumi, Shun Tomomi, Daichi Susaki, Tetsu Kinoshita, Daisuke Maruyama
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1116289/full
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author Naoya Sugi
Rie Izumi
Shun Tomomi
Daichi Susaki
Tetsu Kinoshita
Daisuke Maruyama
author_facet Naoya Sugi
Rie Izumi
Shun Tomomi
Daichi Susaki
Tetsu Kinoshita
Daisuke Maruyama
author_sort Naoya Sugi
collection DOAJ
description In pollen and pollen tubes, immotile sperm cells are enclosed by an inner vegetative plasma membrane (IVPM), a single endomembrane originating from the vegetative-cell plasma membrane. It is widely believed that sperm cells must be removed from the IVPM prior to gamete associations and fusions; however, details of the timing and morphological changes upon IVPM dissociation remain elusive. Here, we report a rapid IVPM breakdown immediately before double fertilization in Arabidopsis thaliana. The IVPM was stably observed in coiling pollen tubes when pollen tube discharge was prevented using lorelei mutant ovules. In contrast, a semi-in vivo fertilization assay in wild-type ovules demonstrated fragmented IVPM around sperm nuclei 1 min after pollen tube discharge. These observations revealed the dynamic alteration of released sperm cells and provided new insights into double fertilization in flowering plants. With a summary of recent findings on IVPM lipid composition, we discussed the possible physiological signals controlling IVPM breakdown.
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spelling doaj.art-1d59d0bcec104d02bd4f3d1d76b1d7a92023-01-26T07:57:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-01-011410.3389/fpls.2023.11162891116289Removal of the endoplasma membrane upon sperm cell activation after pollen tube dischargeNaoya SugiRie IzumiShun TomomiDaichi SusakiTetsu KinoshitaDaisuke MaruyamaIn pollen and pollen tubes, immotile sperm cells are enclosed by an inner vegetative plasma membrane (IVPM), a single endomembrane originating from the vegetative-cell plasma membrane. It is widely believed that sperm cells must be removed from the IVPM prior to gamete associations and fusions; however, details of the timing and morphological changes upon IVPM dissociation remain elusive. Here, we report a rapid IVPM breakdown immediately before double fertilization in Arabidopsis thaliana. The IVPM was stably observed in coiling pollen tubes when pollen tube discharge was prevented using lorelei mutant ovules. In contrast, a semi-in vivo fertilization assay in wild-type ovules demonstrated fragmented IVPM around sperm nuclei 1 min after pollen tube discharge. These observations revealed the dynamic alteration of released sperm cells and provided new insights into double fertilization in flowering plants. With a summary of recent findings on IVPM lipid composition, we discussed the possible physiological signals controlling IVPM breakdown.https://www.frontiersin.org/articles/10.3389/fpls.2023.1116289/fullpollen tubesperm cellvegetative nucleusmale germ unit (MGU)double fertilization
spellingShingle Naoya Sugi
Rie Izumi
Shun Tomomi
Daichi Susaki
Tetsu Kinoshita
Daisuke Maruyama
Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
Frontiers in Plant Science
pollen tube
sperm cell
vegetative nucleus
male germ unit (MGU)
double fertilization
title Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
title_full Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
title_fullStr Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
title_full_unstemmed Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
title_short Removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
title_sort removal of the endoplasma membrane upon sperm cell activation after pollen tube discharge
topic pollen tube
sperm cell
vegetative nucleus
male germ unit (MGU)
double fertilization
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1116289/full
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AT rieizumi removaloftheendoplasmamembraneuponspermcellactivationafterpollentubedischarge
AT shuntomomi removaloftheendoplasmamembraneuponspermcellactivationafterpollentubedischarge
AT daichisusaki removaloftheendoplasmamembraneuponspermcellactivationafterpollentubedischarge
AT tetsukinoshita removaloftheendoplasmamembraneuponspermcellactivationafterpollentubedischarge
AT daisukemaruyama removaloftheendoplasmamembraneuponspermcellactivationafterpollentubedischarge