Development of Quercus acutissima (Fagaceae) pollen tubes inside pistils during the sexual reproduction process

Deng, Min; Yao, Grace; Shi, Chengcheng; Wen, Shifeng; Li, Qiansheng

doi:10.1007/s00425-022-03937-9

Cited by 14 publications

(6 citation statements)

References 59 publications

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“…The cargo of these secretory vesicles is unknown, but candidate cargo could be plasma membrane aquaporins, which could facilitate water transfer (Safavian & Goring, 2013; Windari et al, 2021) from the stigmatic papilla to the pollen grain for hydration and cell‐wall modifying enzymes for stigmatic papillar cell‐wall loosening and pollen tube penetration (Elleman & Dickinson, 1996; Samuel et al, 2009). In 2‐year fruiting Quercus ( Q. acutissima , Q. rubra , Q. suber L., Q. velutina ), pollen germinates instantly after pollination to penetrate the stigmatic surface to the stylar transmitting tissue (Cecich, 1997; Deng et al, 2022). Then, the pollen tube is arrested and overwinters at the style‐joining site until the formation of the rudimentary ovule and embryo sac maturation in the next spring (Boavida et al, 2001; Borgardt & Nixson, 2003; Cecich, 1997; Deng et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…In 2‐year fruiting Quercus ( Q. acutissima , Q. rubra , Q. suber L., Q. velutina ), pollen germinates instantly after pollination to penetrate the stigmatic surface to the stylar transmitting tissue (Cecich, 1997; Deng et al, 2022). Then, the pollen tube is arrested and overwinters at the style‐joining site until the formation of the rudimentary ovule and embryo sac maturation in the next spring (Boavida et al, 2001; Borgardt & Nixson, 2003; Cecich, 1997; Deng et al, 2022). Intermittent and delayed activation of SEC5A in the pistillate flowers of L. edulis with a sharp expression peak after winter (Figure 6c) implies female‐side regulation for the delivery of secretory vesicles to provide the resources, probably cell‐wall modifying enzymes or signalling molecules, necessary for the resumption of pollen tube growth to fertilize the ovule after a prolonged post‐pollination period.…”

Section: Discussionmentioning

confidence: 99%

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Seasonal gene expression signatures of delayed fertilization in Fagaceae

et al. 2023

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In the family Fagaceae, fertilization is delayed by several weeks to 1 year after pollination, leading to 1‐ or 2‐year fruiting species depending on whether fruiting occurs in the same or the next year after flowering. To investigate physiological responses underlying the regulation of delayed fertilization, we monitored seasonal changes in genome‐wide gene expression in tissues including leaves and buds over 2 years under natural conditions in one‐ (Quercus glauca) and 2‐year fruiting species (Lithocarpus edulis). Genes associated with metabolic changes in response to winter cold, photosynthesis and cell proliferation, which are essential for survival and growth, showed highly conserved seasonal expression profiles between species. However, seasonal expression profiles diverged between species in genes associated with pollination, an important process contributing to the origin and maintenance of the reproductive barrier between plant species. By comparing seasonal progression of ovule development and gene expression in pistillate flowers, we revealed that ovules started developing after winter in the 2‐year fruiting species, which could be linked to the activation of genes involved in fertilization and female gametophyte development after winter. These findings suggest that the 2‐year fruiting species may have evolved a requirement of winter cold to prevent fertilization before winter and facilitate fertilization and embryo development in the following spring when temperature rises. This study offers new possibilities to explore the evolution of reproductive strategies in Fagaceae.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Seasonal gene expression signatures of delayed fertilization in Fagaceae

et al. 2023

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“…The cargo of these secretory vesicles is unknown, but candidate cargo could be plasma membrane aquaporins, which could facilitate water transfer (Safavian & Goring, 2013; Windari et al, 2021) from the stigmatic papilla to the pollen grain for hydration and cell-wall modifying enzymes for stigmatic papillar cell wall loosening and pollen tube penetration (Elleman & Dickinson, 1996; Samuel et al, 2009). In two-year fruiting Quercus ( Q. acutissima , Q. rubra , Q. suber L. , Q. velutina ) pollen germinates instantly after pollination to penetrate the stigmatic surface to the stylar transmitting tissue (Cecich, 1997; Deng et al, 2022). Then, the pollen tube is arrested and overwinters at the style-joining site until the formation of the rudimentary ovule and embryo sac maturation in the next spring (Cecich, 1997; Deng et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…In two-year fruiting Quercus ( Q. acutissima , Q. rubra , Q. suber L. , Q. velutina ) pollen germinates instantly after pollination to penetrate the stigmatic surface to the stylar transmitting tissue (Cecich, 1997; Deng et al, 2022). Then, the pollen tube is arrested and overwinters at the style-joining site until the formation of the rudimentary ovule and embryo sac maturation in the next spring (Cecich, 1997; Deng et al, 2022). Intermittent and delayed activation of SEC5A in the pistillate flowers of L. edulis with a sharp expression peak after winter (Fig.…”

Section: Discussionmentioning

confidence: 99%

Seasonal gene-expression signatures of delayed fertilization in Fagaceae

Satake

Ohta

Takeda-Kamiya

et al. 2023

Preprint

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In the family Fagaceae, fertilization is delayed by several weeks to one year after pollination, leading to one- or two-year fruiting species depending on whether fruiting occurs in the same or the next year after flowering. To investigate physiological responses underlying the regulation of delayed fertilization, we monitored seasonal changes in genome-wide gene expression in tissues including leaves and buds over two years under natural conditions in one- (Quercus glauca) and two-year fruiting species (Lithocarpus edulis). Genes associated with the responses to cold stress, photosynthesis, and cell proliferation, which are essential for survival and growth, showed highly conserved seasonal expression profiles regardless of species. However, seasonal expression profiles diverged between the one- and two-year fruiting species in genes associated with pollination, an important process contributing to the origin and maintenance of the reproductive barrier between plant species. By comparing seasonal progression of ovule development and gene expression in pistillate flowers, we revealed that ovules started developing after winter in the two-year fruiting species, which could be linked to the activation of genes involved in fertilization and female gametophyte development after winter. These findings suggest that the two-year fruiting species may have evolved a requirement of winter cold to prevent fertilization before winter and facilitate fertilization and embryo development in the following spring when temperature rises. This study offers new possibilities to explore the evolution of reproductive strategies in Fagaceae.

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“…There is certainly potential for complex interactions between potential parents in the reproductive cycle of Pinus , where pollination and fertilization are separated by a full year, and the male gametophyte undergoes most of its development lying on the ovule in the developing female cone (Gifford & Foster, 1989). Similar delayed‐fertilization systems are found in some angiosperms, where they have been posited to allow increased interactions between the ovulate plant and the microgametophyte, thus allowing the ovulate parent to select favorable pollen for fertilization (Deng et al ., 2022). Furthermore, abiotic stresses can affect specific stages of the reproductive process, altering the spectrum of offspring produced (Williams et al ., 2001).…”

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confidence: 99%