雄全异株流苏树的花部特征及繁育系统研究
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摘要
雄全异株是自然界罕见的繁育系统。通过野外观察和人工授粉实验对雄全异株植物流苏树传粉生物学特征及繁育系统进行研究。结果表明:流苏树的雄花与两性花的雄蕊发育过程基本一致,均能产生功能花粉粒。两性花的两个心皮原基愈合分化形成雌蕊,雄花的两个心皮原基愈合后形成一个空室并停止发育至整体退化。雌蕊先熟,柱头可授期长,花粉在花药开裂后具有活力,室温下,活力维持在10%以上约2周。流苏树靠风和昆虫(主要是蓟马和食蚜蝇)传粉。控制授粉30 d后,自然对照结实率为34.36%;两性花不存在无融合生殖现象,自交亲和,但自发自交的结实率仅10.70%;人工授粉下杂交结实率显著高于自交(同株异花);有性生殖受到传粉者限制;是混合交配系统。证实流苏树是木犀科又一功能性的雄全异株,其依靠雄株增加异交花粉的数量和质量,避免自交衰退;同时两性花的自交亲和保障生殖成功。流苏树雄花的雌蕊退化,从另一个角度证明木犀科的雄全异株是两性株向雌雄异株进化的过渡状态。
Androdioecy is a rare reproductive strategy in plants. Comprehensive studies on the flowering dynamics,pollinators,morphology,and structure of flowers,breeding systems,and controlled pollination were performed in four populations of the Chinese fringe tree,Chionanthus retusus. This species is typically androdioecious in morphology,with male and hermaphroditic individuals coexisting in the same population. Results showed that the development of the stamens of male and hermaphrodite flowers was similar,and could produce functional 2-cell pollen grains. Two carpel primordia appeared inside the stamens of males and hermaphrodites at the initial pistil stage. Subsequently,these two carpels fused with each other and differentiated into the ovary and stigma in hermaphroditic flowers. However,in males,a cavity was formed after the fusion of two carpels,and it stopped growing further and eventually degenerated. This species was protogynous,and the stigma was receptive throughout anthesis. Pollen grains were viable after anther dehiscence and the viability was maintained at ﹥ 10% for about 2 weeks at room temperature of 20-25℃. C. retusus is a wind-and insectpollinated species, and the main pollinating insects belonged to Thripidae and Syrphidae. The results of controlled experiments 30 days after pollination showed that C. retusus could bear fruit under natural conditions with fruit setpercentage of 34.36%. The hermaphroditic flowers were self-compatible,and the fruit set percentage under autogamy was very low,i. e.,only 10. 70%. No apomixis was observed. In artificial pollination,the fruit set percentage with crosspollination( xenogamy with pollen from male or hermaphroditic flower) was significantly higher than that with selfpollination( geitonogamy)( P < 0. 05). Sexual reproduction of this species was limited by the pollinators. It was demonstrated that C. retusus presented a mixed mating system,because it can produce fruit under any type of pollination tested. In terms of functional gamete production from both males and hermaphrodites,C. retusus represents a novel case of functional androdioecy in the family Oleaceae. The maintenance mechanism of androdioecy of this species could be as follows: males increase the quantity and quality of pollen, which can avoid inbreeding depression, and the selfcompatibility of hermaphrodites might ensure reproductive success. Based on the presence of pistillodes in male flowers,and the results of previous studies,androdioecy might be a transition from hermaphroditism to dioecy in Oleaceae.
Androdioecy is a rare reproductive strategy in plants. Comprehensive studies on the flowering dynamics,pollinators,morphology,and structure of flowers,breeding systems,and controlled pollination were performed in four populations of the Chinese fringe tree,Chionanthus retusus. This species is typically androdioecious in morphology,with male and hermaphroditic individuals coexisting in the same population. Results showed that the development of the stamens of male and hermaphrodite flowers was similar,and could produce functional 2-cell pollen grains. Two carpel primordia appeared inside the stamens of males and hermaphrodites at the initial pistil stage. Subsequently,these two carpels fused with each other and differentiated into the ovary and stigma in hermaphroditic flowers. However,in males,a cavity was formed after the fusion of two carpels,and it stopped growing further and eventually degenerated. This species was protogynous,and the stigma was receptive throughout anthesis. Pollen grains were viable after anther dehiscence and the viability was maintained at ﹥ 10% for about 2 weeks at room temperature of 20-25℃. C. retusus is a wind-and insectpollinated species, and the main pollinating insects belonged to Thripidae and Syrphidae. The results of controlled experiments 30 days after pollination showed that C. retusus could bear fruit under natural conditions with fruit setpercentage of 34.36%. The hermaphroditic flowers were self-compatible,and the fruit set percentage under autogamy was very low,i. e.,only 10. 70%. No apomixis was observed. In artificial pollination,the fruit set percentage with crosspollination( xenogamy with pollen from male or hermaphroditic flower) was significantly higher than that with selfpollination( geitonogamy)( P < 0. 05). Sexual reproduction of this species was limited by the pollinators. It was demonstrated that C. retusus presented a mixed mating system,because it can produce fruit under any type of pollination tested. In terms of functional gamete production from both males and hermaphrodites,C. retusus represents a novel case of functional androdioecy in the family Oleaceae. The maintenance mechanism of androdioecy of this species could be as follows: males increase the quantity and quality of pollen, which can avoid inbreeding depression, and the selfcompatibility of hermaphrodites might ensure reproductive success. Based on the presence of pistillodes in male flowers,and the results of previous studies,androdioecy might be a transition from hermaphroditism to dioecy in Oleaceae.
引文
[1]Dellaporta S L,Calderon-Urrea A.Sex determination in flowering plants.Plant Cell,1993,5(10):1241-1251.
[2]Anderson G J,Symon D E.Functional dioecy and andromonoecy in solanum.Evolution,1989,43(1):204-219.
[3]Schlessman M A,Lowry P P,Lloyd D G.Functional dioecism in the New Caledonian Endemic Polyscias pancheri(Araliaceae).Biotropica,1990,22(2):133-139.
[4]Cane J H.Reproductive role of sterile pollen in Saurauia(Actinidiaceae),a cryptically dioecious Neotropical tree.Biotropica,1993,25(4):493-495.
[5]Ishida K,Hiura T.Pollen fertility and flowering phenology in an androdioecious tree,Fraxinus lanuginosa(Oleaceae),in Hokkaido,Japan.International Journal of Plant Sciences,1998,159(6):941-947.
[6]Liston A,Rieseberg L H,Elias T S.Functional androdioecy in the flowering plant Datisca glomerata.Nature,1990,343(6259):641-642.
[7]Akimoto J,Fukuhara T,Kikuzawa K.Sex ratios and genetic variation in a functionally androdioecious species,Schizopepon bryoniaefolius(Cucurbitaceae).American Journal of Botany,1999,86(6):880-886.
[8]Vassiliadis C,Saumitou-Laprade P,Lepart J,Viard F.High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia.Evolution,2002,56(7):1362-1373.
[9]Nishide M,Saito K,Kato H,Sugawara T.Functional androdioecy in Morinda umbellata subsp.boninensis(Rubiaceae),endemic to the Bonin(Ogasawara)Islands.Apg Acta Phytotaxonomica Et Geobotanica,2009,60(2):61-70.
[10]Choudhury B I,Khan M L,Dayanandan S.Functional androdioecy in critically endangered Gymnocladus assamicus(Leguminosae)in the Eastern Himalayan Region of Northeast India.PLo S One,2014,9(2):e87287.
[11]Zhou X J,Ma L,Liu W Z.Functional androdioecy in the rare endemic tree Tapiscia sinensis.Botanical Journal of the Linnean Society,2016,180(4):504-514.
[12]张美珍,邱莲卿.中国植物志.北京:科学出版社,1992.
[13]Saeki I.Application of aerial survey for detecting a rare maple species and endangered wetland ecosystems.Forest Ecology and Management,2005,216(1/3):283-294.
[14]冯永峰.流苏树面临生存危机.光明日报,2013-04-03.
[15]刘迎彩,陈娟,孙开理,刘世东,齐晓青.流苏树播种育苗技术.现代农业科技,2012,(13):181-181,183-183.
[16]邓瑞雪,张创峰,刘普,段文录,尹卫平.流苏花黄酮类化学成分的分离鉴定.食品科学,2014,35(1):74-78.
[17]Kwak J H,Kang M W,Roh J H,Choi S U,Zee O P.Cytotoxic phenolic compounds from Chionanthus retusus.Archives of Pharmacal Research,2009,32(12):1681-1687.
[18]Choi K S,Kim Y H,Kim S O,Shin K O,Chung K H.Effect of intake of sponge gourd(Luffa cylindrica)seed oil and Yukdomok(Chionanthus retusa L.)seed oil on lipid levels of blood and organs of a mice.Food Science and Biotechnology,2013,22(3):757-763.
[19]Arias R S,Techen N,Rinehart T A,Olsen R T,Kirkbride J H,Scheffler B E.Development of Simple Sequence Repeat Markers for Chionanthus Retusus(Oleaceae)and Effective Discrimination of Closely Related Taxa.Hortscience,2011,46(1):23-29.
[20]Chien C T,Kuo-Huang L L,Shen Y C,Zhang R C,Chen S Y,Yang J C,Pharis R P.Storage behavior of Chionanthus retusus seed and asynchronous development of the radicle and shoot apex during germination in relation to germination inhibitors,including abscisic acid and four phenolic glucosides.Plant and Cell Physiology,2004,45(9):1158-1167.
[21]Soejima A,Maki M,Ueda K.Genetic variation in relic and isolated populations of Chionanthus retusus(Oleaceae)of Tsushima Island and the T8no region,Japan.Genes&Genetic Systems,1998,73(1):29-37.
[22]Song J H,Oak M K,Hong S P.Morphological traits in an androdioecious species,Chionanthus retusus(Oleaceae).Flora-Morphology,Distribution,Functional Ecology of Plants,2016,223:129-137.
[23]Dafni A.Pollination ecology:A Practical Approach.OXford:Oxford University Press,1993.
[24]马红.流苏开花及种苗特性的研究[D].泰安:山东农业大学,2007.
[25]Barrett S C H,Case A L,Peters G B.Gender modification and resource allocation in subdioecious Wurmbea dioica(Colchicaceae).Journal of Ecology,1998,87(1):123-137.
[26]Lloyd D G,Webb C J.Secondary sex characters in plants.The Botanical Review,1977,43(2):177-216.
[27]Shea M M,Dixon P M,Sharitz R R.Size differences,sex ratio,and spatial distribution of male and female water tupelo,Nyssa aquatica(Nyssaceae).American Journal of Botany,1993,80(1):26-30.
[28]El-Keblawy A,Freeman D C.Spatial segregation by gender of the subdioecious shrub Thymelaea hirsuta in the Egyptian Desert.International Journal of Plant Sciences,1999,160(2):341-350.
[29]Delph L F,Wolf D E.Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems.New Phytologist,2005,166(1):119-128.
[30]Pannell J.Mixed genetic and environmental sex determination in an androdioecious population of Mercurialis annua.Heredity,1997,78(1):50-56.
[31]Walsh D.Sex lability discovered in Atriplex vesicaria Heward ex Benth.(Chenopodiaceae).Journal of Arid Environments,2005,60(2):201-210.
[32]Willson M F.Sexual selection in plants.The American Naturalist,1979,113(6):777-790.
[33]Wyatt R.Pollinator-plant interactions and the evolution of breeding systems//Read L,ed.Pollination Biology.Orlando:Academic Press.1983.
[34]Cruden R W.Pollen-Ovule Ratios:A conservative indicator of breeding systems in flowering plants.Evolution,1977,31(1):32-46.
[35]Preston R E.Pollen-ovule ratios in the Cruciferae.American Journal of Botany,1986,73(12):1732-1740.
[36]Pellmyr O.Pollination ecology of Cimicifuga arizonica(Ranunculaceae).Botanical Gazette,1985,146(5):404-412.
[37]Fausto J A Jr,Eckhart V M,Geber M A.Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana(Onagraceae).American Journal of Botany,2001,88(10):1794-1800.
[38]Charlesworth D.Androdioecy and the evolution of dioecy.Biological Journal of the Linnean Society,1984,22(4):333-348.
[39]Bawa K S,Beach J H.Evolution of sexual systems in flowering plants.Annals of the Missouri Botanical Garden,1981,68(2):254-274.
[40]Fritsch P,Rieseberg L H.High outcrossing rates maintain male and hermaphrodite individuals in populations of the flowering plant Datisca glomerata.Nature,1992,359(6396):633-636.
[41]Pannell J R.The evolution and maintenance of androdioecy.Annual Review of Ecology and Systematics,2002,33(1):397-425.
[42]Lepart J,Dommée B.Is Phillyrea angustifolia L.(Oleaceae)an androdioecious species?Botanical Journal of the Linnean Society,1992,108(4):375-387.
[43]Dommée B,Geslot A,Thompson J D,Reille M,Denelle N.Androdioecy in the entomophilous tree Fraxinus ornus(oleaceae).New Phytologist,1999,143(2):419-426.
[44]Ross M D.Five evolutionary pathways to subdioecy.The American Naturalist,1982,119(3):297-318.
[45]Wallander E,Albert V A.Phylogeny and classification of Oleaceae based on rps16 and trn L-F sequence data.American Journal of Botany,2000,87(12):1827-1841.
[46]Xu Y C,Zhou L H,Hu S Q,Hao R M,Huang C J,Zhao H B.The differentiation and development of pistils of hermaphrodites and pistillodes of males in androdioecious Osmanthus fragrans L.and implications for the evolution to androdioecy.Plant Systematics and Evolution,2014,300(5):843-849.
[47]Wallander E.Systematics of Fraxinus(Oleaceae)and evolution of dioecy.Plant Systematics and Evolution,2008,273(1/2):25-49.
[2]Anderson G J,Symon D E.Functional dioecy and andromonoecy in solanum.Evolution,1989,43(1):204-219.
[3]Schlessman M A,Lowry P P,Lloyd D G.Functional dioecism in the New Caledonian Endemic Polyscias pancheri(Araliaceae).Biotropica,1990,22(2):133-139.
[4]Cane J H.Reproductive role of sterile pollen in Saurauia(Actinidiaceae),a cryptically dioecious Neotropical tree.Biotropica,1993,25(4):493-495.
[5]Ishida K,Hiura T.Pollen fertility and flowering phenology in an androdioecious tree,Fraxinus lanuginosa(Oleaceae),in Hokkaido,Japan.International Journal of Plant Sciences,1998,159(6):941-947.
[6]Liston A,Rieseberg L H,Elias T S.Functional androdioecy in the flowering plant Datisca glomerata.Nature,1990,343(6259):641-642.
[7]Akimoto J,Fukuhara T,Kikuzawa K.Sex ratios and genetic variation in a functionally androdioecious species,Schizopepon bryoniaefolius(Cucurbitaceae).American Journal of Botany,1999,86(6):880-886.
[8]Vassiliadis C,Saumitou-Laprade P,Lepart J,Viard F.High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia.Evolution,2002,56(7):1362-1373.
[9]Nishide M,Saito K,Kato H,Sugawara T.Functional androdioecy in Morinda umbellata subsp.boninensis(Rubiaceae),endemic to the Bonin(Ogasawara)Islands.Apg Acta Phytotaxonomica Et Geobotanica,2009,60(2):61-70.
[10]Choudhury B I,Khan M L,Dayanandan S.Functional androdioecy in critically endangered Gymnocladus assamicus(Leguminosae)in the Eastern Himalayan Region of Northeast India.PLo S One,2014,9(2):e87287.
[11]Zhou X J,Ma L,Liu W Z.Functional androdioecy in the rare endemic tree Tapiscia sinensis.Botanical Journal of the Linnean Society,2016,180(4):504-514.
[12]张美珍,邱莲卿.中国植物志.北京:科学出版社,1992.
[13]Saeki I.Application of aerial survey for detecting a rare maple species and endangered wetland ecosystems.Forest Ecology and Management,2005,216(1/3):283-294.
[14]冯永峰.流苏树面临生存危机.光明日报,2013-04-03.
[15]刘迎彩,陈娟,孙开理,刘世东,齐晓青.流苏树播种育苗技术.现代农业科技,2012,(13):181-181,183-183.
[16]邓瑞雪,张创峰,刘普,段文录,尹卫平.流苏花黄酮类化学成分的分离鉴定.食品科学,2014,35(1):74-78.
[17]Kwak J H,Kang M W,Roh J H,Choi S U,Zee O P.Cytotoxic phenolic compounds from Chionanthus retusus.Archives of Pharmacal Research,2009,32(12):1681-1687.
[18]Choi K S,Kim Y H,Kim S O,Shin K O,Chung K H.Effect of intake of sponge gourd(Luffa cylindrica)seed oil and Yukdomok(Chionanthus retusa L.)seed oil on lipid levels of blood and organs of a mice.Food Science and Biotechnology,2013,22(3):757-763.
[19]Arias R S,Techen N,Rinehart T A,Olsen R T,Kirkbride J H,Scheffler B E.Development of Simple Sequence Repeat Markers for Chionanthus Retusus(Oleaceae)and Effective Discrimination of Closely Related Taxa.Hortscience,2011,46(1):23-29.
[20]Chien C T,Kuo-Huang L L,Shen Y C,Zhang R C,Chen S Y,Yang J C,Pharis R P.Storage behavior of Chionanthus retusus seed and asynchronous development of the radicle and shoot apex during germination in relation to germination inhibitors,including abscisic acid and four phenolic glucosides.Plant and Cell Physiology,2004,45(9):1158-1167.
[21]Soejima A,Maki M,Ueda K.Genetic variation in relic and isolated populations of Chionanthus retusus(Oleaceae)of Tsushima Island and the T8no region,Japan.Genes&Genetic Systems,1998,73(1):29-37.
[22]Song J H,Oak M K,Hong S P.Morphological traits in an androdioecious species,Chionanthus retusus(Oleaceae).Flora-Morphology,Distribution,Functional Ecology of Plants,2016,223:129-137.
[23]Dafni A.Pollination ecology:A Practical Approach.OXford:Oxford University Press,1993.
[24]马红.流苏开花及种苗特性的研究[D].泰安:山东农业大学,2007.
[25]Barrett S C H,Case A L,Peters G B.Gender modification and resource allocation in subdioecious Wurmbea dioica(Colchicaceae).Journal of Ecology,1998,87(1):123-137.
[26]Lloyd D G,Webb C J.Secondary sex characters in plants.The Botanical Review,1977,43(2):177-216.
[27]Shea M M,Dixon P M,Sharitz R R.Size differences,sex ratio,and spatial distribution of male and female water tupelo,Nyssa aquatica(Nyssaceae).American Journal of Botany,1993,80(1):26-30.
[28]El-Keblawy A,Freeman D C.Spatial segregation by gender of the subdioecious shrub Thymelaea hirsuta in the Egyptian Desert.International Journal of Plant Sciences,1999,160(2):341-350.
[29]Delph L F,Wolf D E.Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems.New Phytologist,2005,166(1):119-128.
[30]Pannell J.Mixed genetic and environmental sex determination in an androdioecious population of Mercurialis annua.Heredity,1997,78(1):50-56.
[31]Walsh D.Sex lability discovered in Atriplex vesicaria Heward ex Benth.(Chenopodiaceae).Journal of Arid Environments,2005,60(2):201-210.
[32]Willson M F.Sexual selection in plants.The American Naturalist,1979,113(6):777-790.
[33]Wyatt R.Pollinator-plant interactions and the evolution of breeding systems//Read L,ed.Pollination Biology.Orlando:Academic Press.1983.
[34]Cruden R W.Pollen-Ovule Ratios:A conservative indicator of breeding systems in flowering plants.Evolution,1977,31(1):32-46.
[35]Preston R E.Pollen-ovule ratios in the Cruciferae.American Journal of Botany,1986,73(12):1732-1740.
[36]Pellmyr O.Pollination ecology of Cimicifuga arizonica(Ranunculaceae).Botanical Gazette,1985,146(5):404-412.
[37]Fausto J A Jr,Eckhart V M,Geber M A.Reproductive assurance and the evolutionary ecology of self-pollination in Clarkia xantiana(Onagraceae).American Journal of Botany,2001,88(10):1794-1800.
[38]Charlesworth D.Androdioecy and the evolution of dioecy.Biological Journal of the Linnean Society,1984,22(4):333-348.
[39]Bawa K S,Beach J H.Evolution of sexual systems in flowering plants.Annals of the Missouri Botanical Garden,1981,68(2):254-274.
[40]Fritsch P,Rieseberg L H.High outcrossing rates maintain male and hermaphrodite individuals in populations of the flowering plant Datisca glomerata.Nature,1992,359(6396):633-636.
[41]Pannell J R.The evolution and maintenance of androdioecy.Annual Review of Ecology and Systematics,2002,33(1):397-425.
[42]Lepart J,Dommée B.Is Phillyrea angustifolia L.(Oleaceae)an androdioecious species?Botanical Journal of the Linnean Society,1992,108(4):375-387.
[43]Dommée B,Geslot A,Thompson J D,Reille M,Denelle N.Androdioecy in the entomophilous tree Fraxinus ornus(oleaceae).New Phytologist,1999,143(2):419-426.
[44]Ross M D.Five evolutionary pathways to subdioecy.The American Naturalist,1982,119(3):297-318.
[45]Wallander E,Albert V A.Phylogeny and classification of Oleaceae based on rps16 and trn L-F sequence data.American Journal of Botany,2000,87(12):1827-1841.
[46]Xu Y C,Zhou L H,Hu S Q,Hao R M,Huang C J,Zhao H B.The differentiation and development of pistils of hermaphrodites and pistillodes of males in androdioecious Osmanthus fragrans L.and implications for the evolution to androdioecy.Plant Systematics and Evolution,2014,300(5):843-849.
[47]Wallander E.Systematics of Fraxinus(Oleaceae)and evolution of dioecy.Plant Systematics and Evolution,2008,273(1/2):25-49.