Abstract
Main conclusion
The pistillate flowers of Lithocarpus dealbatus show two pollen tube (PT) arresting sites (the style-joining and micropyle) within the pistil during the postpollination-prezygotic stage. The PT, arrested at the pre-ovule stage, enhanced PT competition allowing the most compatible PTs to enter the ovary to ensure the highest fertilization success.
Abstract
During the shift from animal pollination to wind pollination, plants require a series of changes in reproductive traits. The mode of pollination is striking labile in Fagaceae. Lithocarpus is insect pollinated and is closely related to wind-pollinated Quercus. Little is known about the sexual reproduction of Lithocarpus. This study aimed to reveal the sexual reproduction of Lithocarpus dealbatus and to explore the evolutionary pattern of the key sexual reproduction traits to better understand their possible role in labile pollination. We found that after pollination, L. dealbatus PTs grew slowly in the style reaching style-joining in mid-January of the second year; then PT growth was arrested at style-joining for four months. Only two to three PTs resumed growth in mid-May to reach the micropyle, where PT growth ceased for one month before one PT resumed growth and passed through the micropyle to the embryo sac. Fagaceae showed a generalized mating system. Vast pollen production, small-sized pollen grains, long stigmatic receptive time, and reduced perianth were compatible with beetle pollination syndrome, representing the plesiomorphic status in Fagaceae. A large stigmatic surface and dry pollen grains linked to wind pollination might be independently derived several times in fagaceous lineages. Beetle pollination syndrome can cope with the uncertainty of pollinators to ensure conspecific pollen capture, which represents pre-adaptation status and has a selective advantage when conditions change, favouring wind pollination. The arrest of the PT at style-joining is a unique mechanism in later derived fagaceous lineages to enhance PT competition and promote outcrossing.
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Data availability
The data generated and/or analysed during this study are available from the corresponding author on reasonable request.
Abbreviations
- ASR:
-
Ancestral state reconstruction
- OI:
-
Outer integument
- OP:
-
Ovule primordia
- PT:
-
Pollen tube
- TT:
-
Transmission tissue
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Acknowledgements
We are grateful to Asian Elephant Yunnan Field Scientific Observation and Research Station, Yunnan Asian Elephant Field Scientific Observation and Research Station of the Ministry of Education, and Baima Snow Mountain Complex Ecosystem Vertical Transect Field Observation and Research Station for their help on the field work; Qun Sui and Sui Wan (Yunnan University) and Wen Shao (Chenshan Botanical Garden) for the help on the microtome-based experiments; Chun-Ya Wu, Jian-Jun Yang, Yong-Ling Qiu and Yin-Mei Xu (Yunnan University) for their help on data analyses; Xian-Zhi Guo (Yunnan University) for helping on the sampling. Special thanks to the Kunming Botanical Garden for granted our collection application and kindly assisted our study in the garden.
Funding
This work was supported by the National Natural Science Foundation of China (grant. no. 31972858), the Fund of Yunnan Key Laboratory for Integrative Conservation of Plant Species with Extremely Small Populations (PSESP2021F01), and the Fund of Key Laboratory for Silviculture and Forest Resources Development of Yunnan Province, Yunnan, Academy of Forestry and Grassland (KFJJ21-05), and the Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (Y4ZK111B01).
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425_2023_4178_MOESM1_ESM.tif
Supplementary file1 Fig. S1 Stigma morphological changes during the flowering time. a On 17 July 2021, the stigmatic surface turned brown and began to receipt pollen grains. b On 30 July 2021, the stigmatic surface gradually changed from brown to black. c On 18 August 2021, the stigma was senescent. d–f Enlarged views of a–c, respectively (The black arrows show the stigma). Scale bars = 2 mm (a–c), 1 mm (d–f) (TIF 2488 KB)
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Supplementary file2 Fig. S2 The diagram on the style length measurement of the pistillate flower in the Fagales using Lithocarpus dealbatus (a), and Castanea mollissima (b), as examples. O, ovule; Ov, ovary; OW, ovary wall; Sc, seed scar; Se, septum; Sg, stigma; St, style. Scale bars = 200 μm (a), 500 μm (b) (TIF 770 KB)
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Supplementary file3 Fig. S3 Phenology of Lithocarpus dealbatus. a 21 March 2021, buds breaking and pistillate flowers (PFs) of the previous year remain unchanged. b 9 April 2021, the fast growth of young twigs and inflorescence of the previous year resumed growth. c 11 June 2021, fast development of young inflorescences (In) on twigs and pistillate flowers (PFs) of the 2nd year. d 26 June 2021, the dense erect inflorescence on twigs, including androgynous and staminate inflorescences. The black arrow shows the staminate flowers (SFs), and the white arrows show the pistillate flowers (PFs). e 23 July 2021, inflorescences at the full-bloom stage, showing the pistillate flower dichasium and the staminate flower dichasium. f 24 September 2021, mature infructescence formed from inflorescence development of the previous year, showing mature fruit (F) and the aborted pistillate flowers (or young fruits) (AF). Scale bars = 1 cm (a–f) (TIF 5082 KB)
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Supplementary file4 Fig. S4 Lithocarpus dealbatus tree at the full bloom stage (20 July 2021), showing vast inflorescences production on the canopy (TIF 9198 KB)
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Supplementary file5 Fig. S5 Ancestral state reconstructions of four reproductive traits in the Fagales. a PT pathway to the embryo sac. b Self-incompatibility type (GSI, gametophytic self-incompatibility; SSI, sporophytic self-incompatibility). c Floral system. d Stigma type. e Development of OP during pollination period (TIF 559 KB)
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Yao, K., Deng, M., Lin, L. et al. The fertilization process in Lithocarpus dealbatus (Fagaceae) and its implication on the sexual reproduction evolution of Fagales. Planta 258, 23 (2023). https://doi.org/10.1007/s00425-023-04178-0
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DOI: https://doi.org/10.1007/s00425-023-04178-0