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

Abstract

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.

Blue light irradiation induces pollen tube rupture in various flowering plants

“…Double fertilization in Arabidopsis is completed within 10 min after pollen tube burst (Hamamura et al, 2011). Subsequent IVPM breakdown and GCS1/HAP2 relocation must occur swiftly before gamete fusion (Sugi et al, 2023; Sprunck et al, 2012; Wang et al, 2022). To observe these events under a microscope, the development of a new technique for controlling pollen tube discharge timing and position was eagerly anticipated.…”

“…After pollen tube burst, double fertilization is completed within 10 min (Hamamura et al, 2011). Swift removal of the inner vegetative plasma membrane (IVPM) and relocation of GENERATIVE CELL SPECIFIC 1 (GCS1)/HAPLESS 2 (HAP2) must be achieved before gamete fusion following pollen tube burst (Sugi et al, 2023, Sprunck et al, 2012, Wang et al, 2022). Analyzing these membrane dynamics poses a significant challenge due to the need for observations in seconds or milliseconds.…”

Heat stress at the bicellular stage inhibits sperm cell development and transport into pollen tubes

“…In angiosperms including maize ( Zea mays ), sperm cells have lost their motility and are transported as a passive cargo through the pollen tube toward the ovule for double fertilization ( Zhou and Dresselhaus 2019 ). After pollen germination, sperm cells move as a male germ unit (MGU) attached to the nucleus of the vegetative cell before being delivered in the receptive synergid cell and separated ( Dumas et al 1985 ; Dresselhaus et al 2016 ; Sprunck 2020 ; Sugi et al 2023 ). Sperm cell transport and delivery requires a well-organized and dynamic cytoskeleton system ( Cheung et al 2008 ; Sharma et al 2021 ).…”

Heat stress at the bicellular stage inhibits sperm cell development and their transport into pollen tubes

“…In angiosperms including maize, sperm cells have lost their motility and are transported as a passive cargo through the pollen tube towards the ovule for double fertilization (Zhou and Dresselhaus, 2019). After pollen germination, sperm cells move as a male germ unit (MGU) attached to the nucleus of the vegetative cell before being delivered in the receptive synergid cell and separated (Dumas et al, 1985; Dresselhaus et al, 2016; Sprunck, 2020; Sugi et al, 2023). Sperm cell transport and delivery requires a well-organized and dynamic cytoskeleton system (Cheung et al, 2008; Sharma et al, 2021).…”