光果甘草二体雄蕊的发育及其适应意义

doi:10.3724/SP.J.1258.2013.00066

摘要/Abstract

摘要：

甘草属(Glycyrrhiza)植物具“9 + 1”二体雄蕊, 其中9枚合生雄蕊的上部花丝分离, 分离的花丝在发育过程中存在由早期长、短交错的二组排列方式转变为后期以雄蕊管最长的1枚雄蕊为中心向两边渐次缩短的倒“V”形排列。为了解这种雄蕊发育动态、分化现象及发育成熟后的适应意义, 该文以光果甘草(G. glabra)为实验材料, 比较了雄蕊发育过程中的形态变化、成熟花粉的理化性质及在传粉中的作用。结果显示: 雄蕊发育早期长、短两组雄蕊在花药大小与形状上存在分化, 但后期伴随着花丝的快速生长与花粉的成熟、散出, 花药大小与形状趋于一致; 花粉组织化学成分及授粉成功率无差异, 但成熟花粉的数量和花粉活力存在差异; 去雄处理虽然使访花者在一天内的两个访花高峰期的访花频次降低, 但结实率高于自然对照, 说明以异交为主的花去除雄蕊后, 降低了雌、雄蕊间的功能干扰, 提高了传粉昆虫的授粉率; 发育早期长、短交错排列的二组雄蕊到成熟期时发生的倒“V”形排列的转变, 使不同数量与活性的花粉分布在花内不同空间, 最大化接触访花者, 实现了资源节约, 提高了雄蕊的雄性适合度, 即在有限的空间内用最节约的雄性资源投入、使传粉空间与传粉几率最大化的方式, 来提高雄性功能。

关键词: 排列方式, 雄性功能, 传粉, 资源分配, 雄蕊发育

Abstract:

Aims The stamens of Glycyrrhiza species are diadelphous, with nine staminal filaments united at the base as a staminal sheath and separated in the upper portion of the staminal sheath. The arrayal shape of the nine stamens changes from two rows at an early stage to an inverted “V”-shaped arrangement at a later stage. Our objectives were to (1) describe development of the stamens in G. glabra (from the bud stage to full bloom) to determine differences in shape development, timing and position of stamens and (2) determine the functional role of long- and short-level stamens in the pollination processes and its adaptive significance.
Methods The development of stamens (measurement of the filament, anther, and style lengths at five developmental stages) and variability of timing and position of stamens were observed under a dissecting microscope. Scanning electron microscopy recorded pollen morphology. The vitality, quantity and chemical composition of pollen were counted and detected. In addition, the number of seeds following each pollination treatment and the pollinator behavior of insects on different stamen removal treatments were compared to examine differentiation of long- and short-level stamens.
Important findings There were differences between the long- and short-level stamens in filament length, anther size and shape early in development, but the differences disappeared when filaments elongated and mature pollen was released. The numbers of pollen grains and pollen vitality between the long- and short-level stamens were different later in development. However, no significant differences were observed in chemical composition of pollen and seed sets among different treatments. Emasculation of the long- and short-level stamens induced reductions in the visiting frequency, but the seed sets of emasculation were higher than without emasculation, which indicates that emasculation reduces the interference between stamens and stigma and improves the pollination rate. The arrayal shape of stamens changed from two rows early in time to an inverted “V”-shaped arrangement at a later stage and resulted in different quantity and vitality of pollen. This indicates that the flower of G. glabra uses fewer male resources to obtain the highest pollination efficiency and to improve male functionality.

Key words: arrangement, male function, pollination, resource allocation, stamen development

田润炜,陆嘉惠,李学禹,余营,谢良碧,秦忠立. 光果甘草二体雄蕊的发育及其适应意义. 植物生态学报, 2013, 37(7): 641-649. DOI: 10.3724/SP.J.1258.2013.00066

TIAN Run-Wei,LU Jia-Hui,LI Xue-Yu,YU Ying,XIE Liang-Bi,QIN Zhong-Li. Diadelphous stamens in Glycyrrhiza glabra: their development and adaptive significance. Chinese Journal of Plant Ecology, 2013, 37(7): 641-649. DOI: 10.3724/SP.J.1258.2013.00066

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链接本文: https://www.plant-ecology.com/CN/10.3724/SP.J.1258.2013.00066

https://www.plant-ecology.com/CN/Y2013/V37/I7/641

图/表 7

图1 光果甘草花发育的不同时期。A, 雄蕊发育的5个不同时期。B, 未散粉雄蕊。C, 未散粉雄蕊剥离展平后的形态(L, 长雄蕊; S, 短雄蕊; 1, 长雄蕊; 2、3, 短雄蕊)。D, 散粉后雄蕊(1, 长雄蕊; 2、3, 短雄蕊)。E, 已散粉雄蕊剥离展平后的形态(1, 长雄蕊; 2、3, 短雄蕊)。

Fig. 1 Different flowering stages of Glycyrrhiza glabra. A, Stamens on five different developmental stages. B, No loose powder stamens. C, Peel and flattened form of no loose powder stamens (L, longer stamens; S, shorter stamens; 1, longer stamens; 2, 3, shorter stamens). D, Loose powder stamens (1, longer stamens; 2, 3, shorter stamens). E, Peel and flattened form of loose powder stamens (1, longer stamens; 2, 3, shorter stamens).

表1 光果甘草长、短雄蕊特征参数(mm) (平均值±标准偏差)

Table 1 Longer and shorter stamens’ attributes of Glycyrrhiza glabra (mm) (mean ± SD)

雄蕊特征 Stamen attributes		花药宽度 Anther width	花药长度 Anther length	雄蕊长度 Stamen length
第1时期 Stage 1	长雄蕊 Longer stamen	0.39 ± 0.02	0.74 ± 0.05	2.16 ± 0.12
	短雄蕊 Shorter stamen	0.35 ± 0.02	0.49 ± 0.02	1.52 ± 0.12
	t检验 t-test	4.18^*	14.12	11.95^**
第2时期 Stage 2	长雄蕊 Longer stamen	0.45 ± 0.03	0.81 ± 0.08	2.66 ± 0.24
	短雄蕊 Shorter stamen	0.41 ± 0.03	0.52 ± 0.03	1.99 ± 0.21
	t检验 t-test	3.70^**	10.80^**	6.53^**
第3时期 Stage 3	长雄蕊 Longer stamen	0.46 ± 0.03	0.74 ± 0.10	3.90 ± 0.41
	短雄蕊 Shorter stamen	0.41 ± 0.03	0.55 ± 0.06	3.23 ± 0.43
	t检验 t-test	3.79^**	5.08^**	3.55^**
第4时期 Stage 4	长雄蕊 Longer stamen	0.22 ± 0.03	0.40 ± 0.04	5.23 ± 0.47
	短雄蕊 Shorter stamen	0.21 ± 0.02	0.32 ± 0.05	4.87 ± 0.53
	t检验 t-test	0.59	4.23^**	1.63
第5时期 Stage 5	长雄蕊 Longer stamen	0.21 ± 0.03	0.39 ± 0.05	5.48 ± 0.46
	短雄蕊 Shorter stamen	0.19 ± 0.02	0.31 ± 0.04	5.44 ± 0.33
	t检验 t-test	1.04	4.37^**	0.25

图2 光果甘草长/短雄蕊花粉电镜扫描及组织化学检测图。A, B, 长、短雄蕊花粉赤道面。C, D, 长、短雄蕊花粉表面纹饰。E, F, 长、短雄蕊花粉I2-KI染色。G, H, 长、短雄蕊花粉苏丹III染色Sudan III。

Fig. 2 Morphology of pollen grains in longer/shorter stamen under scanning electron microscopy and histochemical staining of Glycyrrhiza glabra. A, B, Equatorial view of pollen grains from longer and shorter stamens. C, D, Surface ornamentation of pollen grains from longer and shorter stamens. E, F, I2-KI staining of longer and shorter stamens pollen grains. G, H, Sudan III staining of longer and shorter stamens pollen grains.

图3 光果甘草花发育不同时期与开花当天花粉活力的变化(平均值±标准偏差)。A, 花发育不同时期花粉活力的变化(1, 2, 3 …, 5为花发育的5个不同时期; 6, 开花第2天; 7, 开花第3天)。B, 开花当天花粉活力变化。

Fig. 3 Changes of pollen viability of Glycyrrhiza glabra in different developmental stages of flower and on the first day of anthesis (mean ± SD). A, Viability of pollen in different developmental stages of flower (1-5, five developmental stages of flower; 6, second day of anthesis; 7, third day of anthesis). B, Viability of pollen on the first day of anthesis.

表2 光果甘草人工授粉试验结果

Table 2 Results of artifical pollination experiments in Glycyrrhiza glabra

处理 Treatment	处理花朵数(结实花朵数) No. of treatment flowers (fruit flowers)	结实率 Seed set (%)
对照 Control	72 (31)	43.06 ± 0.50^b
长雄蕊花药花粉自交 Experimentally selfed by pollen of longer stamen	34 (1)	2.94 ± 0.17^a
短雄蕊花药花粉自交 Experimentally selfed by pollen of shorter stamen	36 (0)	0.00 ± 0.00^a
两种雄蕊花药花粉混合自交 Experimentally selfed by two styles of stamen pollen of mixture	52 (1)	1.92 ± 0.14^a
长雄蕊花药花粉异交 Experimentally out-crossed by pollen of longer stamen	30 (3)	10.00 ± 0.31^a
短雄蕊花药花粉异交 Experimentally out-crossed by pollen of shorter stamen	35 (4)	11.43 ± 0.32^a
两种雄蕊花药花粉混合异交 Experimentally out-crossed by two styles of stamen pollen of mixture	34 (18)	52.94 ± 0.51^b

图4 昆虫访花频次。不同字母表示此时段不同处理间差异显著。

Fig. 4 Visiting frequency of insect pollinators. Different letters indicate significant difference of this period in different treatments.

表3 不同处理下光果甘草的结实率

Table 3 Seed sets of Glycyrrhiza glabra under different treatments

处理 Treatment	处理花朵数 No. of treatment flowers	结实数 No. of seed	结实率 Seed set (%)
去长雄蕊 Removing longer stamen	40	22	55.00 ± 0.51^ab
去短雄蕊 Removing shorter stamen	42	30	71.43 ± 0.46^a
去全部雄蕊 Removing all of stamens	42	30	71.43 ± 0.46^a
对照 Control	72	31	43.06 ± 0.50^b

参考文献 29

[1]	Albert S, Joshi A, Patel C (2009). Heteranthery in four tree species of Cassia. Journal of Economic and Taxonomic Botany, 33, 285-288.
[2]	Barrett SCH (2002). Sexual interference of the floral kind. Heredity, 88, 154-159. DOI URL PMID
[3]	Barrett SCH (2003). Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philosophical Transactions of the Royal Society B: Biological Sciences, 358, 991-1004.
[4]	Barrett SCH (2010). Darwin’s legacy: the forms, function and sexual diversity of flowers. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 351-368.
[5]	Dai C, Galloway LF (2011). Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species? Functional Ecology, 25, 271-278.
[6]	Darwin C (1877). The Different Forms of Flowers on Plants of the Same Species. John Murray, London.
[7]	de Almeida NM, de Castro CC, de Lima Leite AV, Novo RR, Machado IC (2013). Enantiostyly in Chamaecrista ramosa (Fabaceae-Caesalpinioideae): floral morphology, pollen transfer dynamics and breeding system. Plant Biology, 15, 369-375. DOI URL PMID
[8]	de Freitas Mansano V, de Souza AL (2005). A new Swartzia (Leguminosae: Papilionoideae: Swartzieae) species with trimorphic stamens from Amazonian Brazil. Botanical Journal of the Linnean Society, 147, 235-238.
[9]	Foerste AF (1888). Notes on structures adapted to cross-fertilization. Botanical Gazette, 13, 151-156.
[10]	Forbes HO (1882). Two kinds of stamens with different functions in the same flower. Nature, 26, 386.
[11]	Kliber A, Eckert CG (2004). Sequential decline in allocation among flowers within inflorescences: proximate mechanisms and adaptive significance. Ecology, 85, 1675-1687.
[12]	Liao YH (2011). A Study on Breeding System of Two Drug glycyrrhiza. Master degree dissertation, Shihezi University, Shihezi, Xinjiang. 6-29. (in Chinese with English abstract)
	[ 廖云海 (2011). 两种药用甘草繁育系统的研究. 硕士论文, 石河子大学, 新疆石河子. 6-29.]
[13]	Liao YH, Lu JH, Zhang JZ, Liu J, Li XY (2010). A preliminary study on the characteristics of reproductive biology of Glycyrrhiza glabra L. Acta Botanica Boreali-Occidentalia Sinica, 30, 939-943. (in Chinese with English abstract)
	[ 廖云海, 陆嘉惠, 张继昭, 刘静, 李学禹 (2010). 光果甘草生殖生物学特性的初步研究. 西北植物学报, 30, 939-943.]
[14]	Liu SM (1996). Study on flowering behaviour and crossbreeding technique of alfafa. Grassland of China, (2), 7-11. (in Chinese with English abstract)
	[ 刘淑明 (1996). 苜蓿的开花习性及其杂交技术的研究. 中国草地, (2), 7-10.]
[15]	Luo ZL, Zhang DX (2005). A review of heteranthery in flowering plants. Journal of Tropical and Subtropical Botany, 13, 536-542. (in Chinese with English abstract)
	[ 罗中莱, 张奠湘 (2005). 异型雄蕊的研究进展. 热带亚热带植物学报, 13, 536-542.]
[16]	Luo ZL, Zhang DX, Renner SS (2008). Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin’s division-of-labour hypothesis. Functional Ecology, 22, 794-800.
[17]	Medrano M, Guitián P, Guitián J (2000). Patterns of fruit and seed set within inflorescences of Pancratium maritimum (Amaryllidaceae): nonuniform pollination, resource limitation, or architectural effects? American Journal of Botany, 87, 493-501. URL PMID
[18]	Morgan MT, Schoen DJ (1997). The role of theory in an emerging new plant reproductive biology. Trends in Ecology and Evolution, 12, 231-234. DOI URL PMID
[19]	Muchhala N, Brown Z, Armbruster WS, Potts MD (2010). Competition drives specialization in pollination systems through costs to male fitness. The American Naturalist, 176, 732-743. DOI URL PMID
[20]	Proctor MCF, Yeo P, Lack A (1996). The Natural History of Pollination. Harper Collins Publishers, London. 294-295.
[21]	Ren MX (2009). Intrafloral stamen differentiations and their adaptive significances. Chinese Journal of Plant Ecology, 33, 222-236. (in Chinese with English abstract)
	[ 任明迅 (2009). 花内雄蕊分化及其适应意义. 植物生态学报, 33, 222-236.]
[22]	Ren MX (2010). Stamen movements in hermaphroditic flowers: diversity and adaptive significance. Chinese Journal of Plant Ecology, 34, 867-875. (in Chinese with English abstract)
	[ 任明迅 (2010). 两性花的雄蕊运动: 多样性和适应意义. 植物生态学报, 34, 867-875.]
[23]	Ren MX, Jiang XH, Zhang DY (2012). Some important questions in plant reproductive ecology. Biodiversity Science, 20, 241-249. (in Chinese with English abstract)
	[ 任明迅, 姜新华, 张大勇 (2012). 植物繁殖生态学的若干重要问题. 生物多样性, 20, 241-249.]
[24]	Tian RW, Lu JH, Xie LB, Qin ZL, Li XY (2012). Effect of flowering mode and pollination on reproductive success and the relationship between Glycyrrhiza glabra L. and Glycyrrhiza uralensis Fisch. Acta Botanica Boreali-Occidentalia Sinica, 32, 2004-2008. (in Chinese with English abstract)
	[ 田润炜, 陆嘉惠, 谢良碧, 秦忠立, 李学禹 (2012). 光果甘草与乌拉尔甘草开花与传粉方式对生殖及种间关系的影响. 西北植物学报, 32, 2004-2008.]
[25]	Torres MW, Aximoff IA, Ferreira MHS, Guerra TJ (2007). Aspects of floral biology of buzz pollinated Senna cana (Leguminosae: Caesalpinioideae) in a rupestrian field in Mucugê, BA. http://www.seb-ecologia.org.br/viiiceb/pdf/1575.pdf. Cited: Jan. 2013.
[26]	Wang XJ, Zhang LC, Zhao ZG (2010). The pattern of seed reproduction and its response to resources in Pedicularis semitorta individuals. Acta Prataculturae Sinica, 19, 236-242. (in Chinese with English abstract)
	[ 王晓娟, 张龙冲, 赵志刚 (2010). 半扭卷马先蒿个体内的种子生产模式及其对资源的响应. 草业学报, 19, 236-242.]
[27]	Weigend M, Ackermann M, Henning T (2010). Reloading the revolver-male fitness as a simple explanation for complex reward partitioning in Nasa macrothyrsa (Loasaceae, Cornales). Biological Journal of the Linnean Society, 100, 124-131.
[28]	Wu GF, Feng ZJ, Ma WL, Zhou XJ, Lang KC, Hu RL, Wang CZ, Li RG (1992). Botany 2nd edn. China Higher Education Press, Beijing. 272. (in Chinese)
	[ 吴国芳, 冯志坚, 马炜梁, 周秀佳, 郎奎昌, 胡人亮, 王策箴, 李茹光 (1992). 植物学.第二版. 高等教育出版社, 北京. 272.]
[29]	Zhang DY (2004). Plant Life-History Evolution and Reproductive Ecology. Science Press, Beijing. (in Chinese)
	[ 张大勇 (2004). 植物生活史进化与繁殖生态学. 科学出版社, 北京.]