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Longitudinal slit formation and pollen dispersal in G. biloba. (a) Formation of longitudinal slit at the facing sides of both microsporangia. (b) The trapped and sunken sporangial wall at the longitudinal slit. (c) Longitudinal slit. (d) Longitudinal slit in detail. (e) The broken epidermis. (f) The opening of the tapeta. (g) Shrunken epidermis and opening longitudinal slit. (h) Microsporangium dehiscence. (i) Regulation of pollen release for microsporangium. (j) Regulation of pollen dispersal in male cones. D 0dyad; LS0longitudinal slit; Sg 0microsporangium; P 0pollen; SW 0sporangial wall; Th 0fibrous thickening. Scale bars 0200 mm (a,g); 100 mm (b,c); 50 mm (dÁf); 2 mm (h,i); 1 cm (j).
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Lu, Y., Wang, L., Wang, D., Wang, Y., Zhang, M., Jin, B. and Chen, P. 2011. Male cone morphogenesis, pollen development and pollen dispersal mechanism in Ginkgo biloba L. Can. J. Plant Sci. 91: 971-981. Ginkgo biloba L. is one of the oldest gymnosperms. Male cone morphogenesis, pollen development and dispersal are important for successful pollinati...
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... slit formation occurred at the early stage of meiotic division (Fig. 7a). At first, the sporangial wall kept expanding, except at the sides facing both microsporangia (Fig. 7b). Subsequently, these cells were trapped and sank, which resulted in formation of the longitudinal slit by the end of the microspore period (Fig. 7c, d). During the different pollen dispersal stages, the endothecium cell walls ...
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... slit formation occurred at the early stage of meiotic division (Fig. 7a). At first, the sporangial wall kept expanding, except at the sides facing both microsporangia (Fig. 7b). Subsequently, these cells were trapped and sank, which resulted in formation of the longitudinal slit by the end of the microspore period (Fig. 7c, d). During the different pollen dispersal stages, the endothecium cell walls thickened and the epidermis rapidly dehydrated, leading to an increase in the cohesive force within the cells, ...
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... slit formation occurred at the early stage of meiotic division (Fig. 7a). At first, the sporangial wall kept expanding, except at the sides facing both microsporangia (Fig. 7b). Subsequently, these cells were trapped and sank, which resulted in formation of the longitudinal slit by the end of the microspore period (Fig. 7c, d). During the different pollen dispersal stages, the endothecium cell walls thickened and the epidermis rapidly dehydrated, leading to an increase in the cohesive force within the cells, concentrated mainly on the longitudinal slit. The epidermis and endothecium within the longitudinal slit broke first (Fig. 7e) and then the tapeta ...
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... the end of the microspore period (Fig. 7c, d). During the different pollen dispersal stages, the endothecium cell walls thickened and the epidermis rapidly dehydrated, leading to an increase in the cohesive force within the cells, concentrated mainly on the longitudinal slit. The epidermis and endothecium within the longitudinal slit broke first (Fig. 7e) and then the tapeta opened, owing to further dehydration of the cells (Fig. 7f). Finally, the sporangial wall bent outwards along the longitudinal slit (Fig. 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones ...
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... stages, the endothecium cell walls thickened and the epidermis rapidly dehydrated, leading to an increase in the cohesive force within the cells, concentrated mainly on the longitudinal slit. The epidermis and endothecium within the longitudinal slit broke first (Fig. 7e) and then the tapeta opened, owing to further dehydration of the cells (Fig. 7f). Finally, the sporangial wall bent outwards along the longitudinal slit (Fig. 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones and trees. For one microsporangium, the slit dehisced from the middle part to ...
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... leading to an increase in the cohesive force within the cells, concentrated mainly on the longitudinal slit. The epidermis and endothecium within the longitudinal slit broke first (Fig. 7e) and then the tapeta opened, owing to further dehydration of the cells (Fig. 7f). Finally, the sporangial wall bent outwards along the longitudinal slit (Fig. 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones and trees. For one microsporangium, the slit dehisced from the middle part to the ends (Fig. 7i). The dehiscence took place from bottom to top for individual ...
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... mainly on the longitudinal slit. The epidermis and endothecium within the longitudinal slit broke first (Fig. 7e) and then the tapeta opened, owing to further dehydration of the cells (Fig. 7f). Finally, the sporangial wall bent outwards along the longitudinal slit (Fig. 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones and trees. For one microsporangium, the slit dehisced from the middle part to the ends (Fig. 7i). The dehiscence took place from bottom to top for individual male cones (Fig. 7j), and the male cones opened from exterior to interior ...
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... 7f). Finally, the sporangial wall bent outwards along the longitudinal slit (Fig. 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones and trees. For one microsporangium, the slit dehisced from the middle part to the ends (Fig. 7i). The dehiscence took place from bottom to top for individual male cones (Fig. 7j), and the male cones opened from exterior to interior for an entire ...
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... 7g) and the microsporangium dehisced to ballistic pollen dispersal (Fig. 7h). Moreover, we investigated the regulation of pollen dispersal in individual microsporangia, male cones and trees. For one microsporangium, the slit dehisced from the middle part to the ends (Fig. 7i). The dehiscence took place from bottom to top for individual male cones (Fig. 7j), and the male cones opened from exterior to interior for an entire ...
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Ginkgo biloba L. is a dioecious anemophilous species. Its female flower is a naked ovule which catches and identifies drifting pollens in the air during pollination and has specific structures to facilitate pollen entrance into the ovule and to store them. As a consequence, the ovule structures have important effects on pollination efficiency and r...
Citations
... The simplest and most intuitive method to distinguish the sexes of plants is based on their morphological characteristics. Previous studies reported the differences between the two sexes of ginkgo in their reproductive organs (cones) [5,6], vegetative organs [3,7], and phenology [8,9]. However, ginkgo trees have juvenile periods lasting two decades in which they produce no cones. ...
Ginkgo biloba L. is a rare dioecious species that is valued for its diverse applications and is cultivated globally. This study aimed to develop a rapid and effective method for determining the sex of a Ginkgo biloba. Green and yellow leaves representing annual growth stages were scanned with a hyperspectral imager, and classification models for RGB images, spectral features, and a fusion of spectral and image features were established. Initially, a ResNet101 model classified the RGB dataset using the proportional scaling–background expansion preprocessing method, achieving an accuracy of 90.27%. Further, machine learning algorithms like support vector machine (SVM), linear discriminant analysis (LDA), and subspace discriminant analysis (SDA) were applied. Optimal results were achieved with SVM and SDA in the green leaf stage and LDA in the yellow leaf stage, with prediction accuracies of 87.35% and 98.85%, respectively. To fully utilize the optimal model, a two-stage Period-Predetermined (PP) method was proposed, and a fusion dataset was built using the spectral and image features. The overall accuracy for the prediction set was as high as 96.30%. This is the first study to establish a standard technique framework for Ginkgo sex classification using hyperspectral imaging, offering an efficient tool for industrial and ecological applications and the potential for classifying other dioecious plants.
... March while in northern populations it is often delayed to mid-April (Lu et al., 2011;Wang et al., 2013). After a week, the green male cones tend to droop, perpendicular to the fan-shaped leaves above (Lu et al., 2011). ...
... March while in northern populations it is often delayed to mid-April (Lu et al., 2011;Wang et al., 2013). After a week, the green male cones tend to droop, perpendicular to the fan-shaped leaves above (Lu et al., 2011). By mid-April, the main axis elongates and separates the microsporophylls, then male cones turn yellow and begin to shed pollen (Lu et al., 2011). ...
... After a week, the green male cones tend to droop, perpendicular to the fan-shaped leaves above (Lu et al., 2011). By mid-April, the main axis elongates and separates the microsporophylls, then male cones turn yellow and begin to shed pollen (Lu et al., 2011). A large amount of pollen grains disperse within 7 days (Gao et al., 2001;Lu et al., 2011). ...
This account presents information on all aspects of the biology of Ginkgo biloba L. (Ginkgo, Maidenhair tree) that are relevant to understanding its ecological characteristics. The main topics are presented within the standard framework of the International Biological Flora: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, reproductive and seed characters, herbivores and disease, history, conservation and global heterogeneity.
Globally, Ginkgo survives a wide range of mean annual temperature (−3.3 to 23.3°C) and annual precipitation (34–3925 mm) conditions, according to a meta‐analysis. It prefers a warm, humid, open‐canopy and a well‐drained environment. The species shows strong tolerance to drought, freezing, fire, air pollution, heavy metals and low‐level salt, whereas it is intolerant to long‐time shade and waterlogging. Six Ginkgo trees even survived the atom bomb in Hiroshima, Japan, during World War II.
Ginkgo is susceptible to few diseases. Those occurring in nursery seedlings and juvenile trees involve stem rot and leaf blight. The former is caused by Macrophomina phaseoli, which could lead to a mortality rate of 5%–12% (up to 31.8%) for seedlings. This disease can be mitigated by a 4‐h shading treatment and applying organic fertilisers. The pathogens inducing leaf blight include Alternaria alternata, Colletotrichum gloeosporioides and Pestalotia ginkgo, which may infect 100% juvenile trees in some regions. The application of 45% carbendazim or 50% Tuzet can effectively prevent leaf blight.
Ginkgo biloba is one of the world’s most distinctive trees with an important position in plant evolution and human society. It is a tall deciduous dioecious tree native to China. Refugial populations were identified in three glacial refugia located in eastern, southern and south‐western China, respectively, with a patchy distribution pattern and a small population size. It typically grows along flood‐disturbed streamsides in warm‐temperate deciduous (and evergreen mixed) broadleaved forests. Ginkgo may have been introduced repeatedly out of China since the sixth century. It has been planted as a landscape tree world‐wide, except in Antarctica. Ginkgo is also of great value for edible nuts, herbal medicine, religion and art. It is a natural and cultural symbol of China.
... First, the homology of tapetum-like structures across all land plants is far from clear. Typical tapetum structures are found in all vascular land plants-ferns, lycophytes and seed plants-which are wellsupported by past studies exploring morphological and genetic similarities (Duncan, 1940;Aya et al., 2011;Lu et al., 2011;Johri & Srivastava, 2001;Koi et al., 2016) (Fig. 9d). Tapetumlike structures also are reported in mosses even though they are difficult to recognize (Pacini et al., 1985;Wallace et al., 2015), whereas the interpretation of the sporangial structures in hornworts and liverworts require further studies (Johri & Srivastava, 2001;Villarreal et al., 2017;Yamaoka et al., 2018) (Fig. 9d). ...
... In M. truncatula, EAN1 has a tandem duplicate, EAN2, which showed much lower expression in anthers than EAN1 (Fig. 7b), indicating the possible functional divergence between EAN1 and EAN2. Such a scenario is similar to that observed in tomato, in which, although a tandem duplication led to two subfamily II genes MALE STERILE 32 (MS32) (Solyc01g081100) and Solyc01g081090, single mutations of the MS32 induced abnormal tapetum development and (Lu et al., 2011), Azolla filiculoides (Duncan, 1940;Nayak & Singh, 1989) and Selaginella moellendorffii (Schulz et al., 2010;Aya et al., 2011), the male antheridia of hornwort Anthoceros sp. (Johri & Srivastava, 2013;Villarreal et al., 2017), moss Physcomitrella patens (Landberg et al., 2013;Sanchez-Vera et al., 2017), liverwort Marchantia polymorpha (Koi et al., 2016;Yamaoka et al., 2018) and charophyte Chara braunii (Nishiyama et al., 2018), and the male gamete of chlorophyte Chlamydomonas reinhardtii (Johri & Srivastava, 2001). ...
Male sterility is an important tool for plant breeding and hybrid seed production. Male‐sterile mutants are largely due to an abnormal development of either the sporophytic or gametophytic anther tissues. Tapetum, a key sporophytic tissue, provides nutrients for pollen development, and its delayed degeneration induces pollen abortion. Numerous bHLH proteins have been documented to participate in the degeneration of the tapetum in angiosperms, but relatively little attention has been given to the evolution of the involved developmental pathways across the phylogeny of land plants.
A combination of cellular, molecular, biochemical and evolutionary analyses was used to investigate the male fertility control in Medicago truncatula.
We characterized the male‐sterile mutant empty anther1 (ean1) and identified EAN1 as a tapetum‐specific bHLH transcription factor necessary for tapetum degeneration. Our study uncovered an evolutionarily conserved recruitment of bHLH subfamily II and III(a + c)1 in the regulation of tapetum degeneration. EAN1 belongs to the subfamily II and specifically forms heterodimers with the subfamily III(a + c)1 members, which suggests a heterodimerization mechanism conserved in angiosperms.
Our work suggested that the pathway of two tapetal‐bHLH subfamilies is conserved in all land plants, and likely was established before the divergence of the spore‐producing land plants.
... Ginkgo biloba L. is commonly described as a 'living fossil'; it is dioecious with anemophilous pollination (Labandeira 2010; Lu et al. 2011a;Jin et al. 2012c). The shape of dry pollen after dispersal is a bilaterally symmetrical boat with monosulcate and smooth ornamentation (Lu et al. 2011a). ...
... Ginkgo biloba L. is commonly described as a 'living fossil'; it is dioecious with anemophilous pollination (Labandeira 2010; Lu et al. 2011a;Jin et al. 2012c). The shape of dry pollen after dispersal is a bilaterally symmetrical boat with monosulcate and smooth ornamentation (Lu et al. 2011a). After hydration with the pollination drop, the pollen converts into a round shape (Tekleva et al. 2007), and the pollen grains enter into the pollen chamber to cause pollen tube germination (Lu et al. 2009;Wang et al. 2010). ...
... The pollen wall plays a key role in pollination and pollen germination (Pacini and Hesse 2005;Tekleva and Krassilov 2009). In Ginkgo, the pollen wall is constituted by intine, endexine and ectexine (Tekleva et al. 2007;Lu et al. 2011a). The ectexine is characterised by a thick solid tectum, distinct foot layer and infratectum of columellalike elements or large granules (Tekleva et al. 2007). ...
Key message
The morphology, structure, element distribution and motion of pollen grains in Ginkgo biloba are beneficial for pollination and germination in the pollination drop.
Abstract
The morphology and structure of pollen grains are important for pollination, and hence reproductive success in gymnosperms. To examine the role of pollen structures associated with pollination and germination in Ginkgo biloba L., scanning and transmission electron microscopy were used to observe ultrastructure features of pollen. Compared with pollen grains before dispersal, the aperture area was sunken, spinules on the pollen surface disappeared, and the tectum and intine were thickened during pollen dispersal. However, after pollen hydration, the aperture area and spinules recovered and the thickness of tectum and intine were similar to those of pollen before dispersal, suggesting that G. biloba pollen grains could facilitate pollination and germination through changing their microstructure. In addition, calcium was mainly distributed in the intine. Calcium levels decreased significantly after ethylene glycol tetraacetic acid treatment, resulting in a low germination rate compared with untreated pollen. These results indicate that calcium could play an important role in pollen germination. Importantly, the use of both in vivo and in vitro pollen experiments revealed that after the pollen grains landed on the ovule, they hydrated and swelled on the surface of the pollination drop. This was accompanied by air bubble release at the exposed part of the aperture area. The viable Ginkgo pollen could get into the ovule easier than less-viable pollen. These results showed that the effectiveness of hydration and sinking as a selection mechanism is a result of the ability of G. biloba to exclude less-viable pollen grains and preferentially concentrate on viable pollen inside ovules.
... Intermediate cytokinesis, on the other hand, has been described in detail only in Magnolia ( Farr, 1918 ;Sampson, 1969a , b ;Brown and Lemmon, 1992 ;Nadot et al., 2008 ). For a comparison, either simultaneous or successive cytokinesis was reported for microsporogenesis in gymnosperm species other than cycads ( Maheshwari, 1935 ;Moitra and Bhatnagar, 1982 ;Anderson and Owens, 2000 ;Lü et al., 2003 ;Zhang et al., 2008 ;Lu et al., 2011 ). Currently, only limited information is available on the process of microsporogenesis in several cycads, but the cytokinetic process seems to be similar to the intermediate type ( Singh, 1978 ;Audran, 1981 ;Zhang et al., 2012 ). ...
... In the majority of seed plants, wall stub formation is closely coupled with cell plate formation in both simultaneous cytokinesis and successive cytokinesis ( Fig. 10C ). As a comparison, in Ginkgo biloba , cytokinesis in microsporogenesis appears to be simultaneous without ACWIs ( Brown and Lemmon, 2005 ;Lu et al., 2011 ). ...
... Spatial and temporal control of the callose deposition -Callose deposition is a common event during meiosis in plants ( Singh, 1978 ;Johri, 1984 ;Bhatia and Malik, 1996 ;Lü et al., 2003 ;Lu et al., 2011 ;Zhang et al., 2012 ). In M. communis , two callose rings form at the sites where future cell plates will join the parental cell wall in advance of the mini-phragmoplast-based process of cell plate formation in the interior of the cell. ...
PREMISE OF THE STUDY: Spatiotemporal features of microsporogenesis may provide important clues about the evolution of microsporogenesis in seed plants. One cellular feature that attracts special attention is advance cell wall ingrowths (ACWIs) at future cytokinetic sites in microsporocytes since they have been found only in species of an ancient lineage of angiosperms, Magnolia , and in much less detail, of an ancient lineage of gymnosperms, cycads. Further investigation into microsporogenesis in a cycad species may yield knowledge critical to understanding the establishment of ACWIs as an important feature for comparative studies of microsporogenesis in seed plants.
METHODS: Bright-fi eld and epifl uorescence microscopy, confocal laser scanning microscopy, and transmission electron microscopy were used to investigate the microsporogenic process in Macrozamia communis , a species in the Zamiaceae family of cycads.
KEY RESULTS: In prophase-II microsporocytes in M. communis , ACWIs form as a callose ring between the newly formed nuclei and are not accompanied by cytokinetic apparatuses such as mini-phragmoplasts, wide tubules, or wide tubular networks. Shortly after the second nuclear division, new ACWIs, albeit thinner than the previous ACWIs, form between the newly formed nuclei. Subsequent cell plate formation in the planes of the ACWIs typically results in tetragonal tetrads.
CONCLUSIONS: Cytokinesis at the cell periphery is initiated earlier than cell plate formation in the cell interior in microsporogenesis in M. communis. The cellular features uncovered in M. communis may serve as useful reference features for comparative studies of microsporogenesis in plants.
... The shape of sporangia was oval, elongate-elliptical and boat-shaped and in our study some were also almost round (Liu et al. 2006). The microsporangia walls exhibit shrinkage of the epidermis, fibrous thickening of the endothecium and enzymatic dissolution of the tapetum during pollen dispersal, which contributes to sporangia opening (Keijzer 1987;Abid and Qaiser 2004;Lu et al. 2011). ...
Metasequoia glyptostroboides, a famous relic species of conifer that survived in China, has been successfully planted in large numbers across the world. However, limited information on male cone development in the species is available. In this study, we observed the morphological and anatomical changes that occur during male cone development in M. glyptostroboides using semi-thin sections and scanning electron microscopy. The male cones were borne oppositely on one-year-old twigs that were mainly located around the outer and sunlit parts of crown. Male cones were initiated from early September and shed pollen in the following February. Each cone consisted of spirally arranged microsporophylls subtended by decussate sterile scales, and each microsporophyll commonly consisted of three microsporangia and a phylloclade. The microsporangial wall was composed of an epidermis, endothecium, and tapetum. In mid-February, the endothecium and tapetum layers disintegrated, and in the epidermal layer the cell walls were thickened with inner protrusions. Subsequently, dehiscence of the microsporangia occurred through rupturing of the microsporangial wall along the dehiscence line. These results suggest that the structure, morphology, architecture and arrangement of male cones of M. glyptostroboides are mainly associated with the production, protection and dispersal of pollen for optimization of wind pollination.
