云南红豆杉生殖生态学研究
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摘要
云南红豆杉(Taxus yunnanensis Cheng et L. K. Fu)是分布于缅甸和不丹北部及我国西南部的红豆杉属(Taxus)植物。因为富含抗癌药物紫杉醇闻名于世,又因为处于濒危状态而倍受关注,但由于不清楚其濒危机制,使得保护难以对症下药,进而限制了自然资源合理利用。本文主要从生殖发育过程、传粉机制、性别决定及性表达等方面研究了云南红豆杉的生殖规律,以期为云南红豆杉濒危机制的探索、人工林建设及系统学研究服务,研究结果主要包括以下几个方面。
第一,雄性生殖系统发育过程。云南红豆杉小孢子叶球从6月底开始发生;小孢子从9月开始发生,11月成熟;雄配子体从12月开始发育,到次年4月产生精子。在小孢子母细胞减数分裂过程中,第一次分裂产生两个半球形细胞,第二次分裂形成T形、正方形或四面体形四分体;成熟的小孢子直径约20微米,单核,没有气囊,表面有大量的乌氏体。离体培养的雄配子体分别在培养后的第6天、第20天和第40天发现第一次、第二次和第三次分裂。在活体中,发生细胞核的分裂在细胞一侧进行,但最终分裂后形成了两个大小相等的精子。
第二,雌性生殖系统发育及胚的发育和萌发过程。云南红豆杉胚珠从8月开始发生,大孢子母细胞12月开始发生,呈方形,减数分裂后形成4个“一”字形大孢子,在大多数情况下,只有靠合点端的大孢子发育为功能大孢子。功能大孢子核随后开始分裂,形成游离核雌配子体,当游离核形成细胞壁,雌配子体即发育成熟。十多个颈卵器在同一个成熟雌配子体上发生,两次有丝分裂后,形成卵细胞。雄配子体产生的两个精子中的一个进入颈卵器与卵细胞结合形成受精卵,受精卵核到第3次分裂形成细胞壁,没有受精的卵细胞还要进行两次有丝分裂后才消失。胚珠发育过程中的数量变化显示:授粉是胚珠发育的瓶颈,胚珠的授粉率只有44.7%。在胚发育过程中,既产生简单多胚,又产生裂生多胚。离体培养中,刚刚成熟种子胚在2周左右萌发,在种子储藏的过程中,胚的结构和长度都没有发生变化,随着储藏时间的延长萌发率逐渐下降。幼苗到性成熟需要14年左右的时间。
第三,花期及传粉滴的活动规律。小孢子叶球的散粉期在11月中旬到12月中旬,小孢子在常温下保存42天,还有50%的花粉具有活力;胚珠成熟期从11月下旬持续到2月中旬,直到3月中旬还可见到带有传粉滴的胚珠。在小孢子叶球散粉期或人工授粉的传粉滴持续存在的时间较短,且授粉后不再出现,在非散粉期的传粉滴持续存在的时间较长,且在消失后又会重新出现。死花粉也具有与活花粉相同的水合性质,授粉后也能引起传粉滴消失并不再出现。
第四,性别控制与性表达。细胞学研究表明:雄性植株的核型为:2n=24=24m;雌性植株的核型为:2n=24=23m+1sm,据此推测云南红豆杉的性别控制类型为ZW型。性别表型构成调查结果显示:在个体水平上,多数植株是单性的,2005、2006和2007年单性植株分别占能辨别性别植株的92.5%、92%和94.2%。在构件水平上,两性植株的大部分主干是单性的,占能辨别性别主干的93.6%(2006年)和88.7%(2007年);在两性主干上,多数小孢子叶球和胚珠都出现异常。性别表型的年际变化调查结果显示:在个体水平上,性别表型发生变化只是少数植株,占能辨别性别植株的10%(2005至2006年)和7.6%(2006至2007年);雌株和雄株不直接相互转化,但雌株通过未知性别植株的过渡,可以转化为雄株,雄株也通过两性植株的过渡转化为雌株,其它各性别表型间都可以直接相互转化。在构件水平上,两性植株的多数主干的性别表型保持不变,雌性主干、雄性主干和两性主干分别有69.4%、89.4%和66.7%保持了原来的性别表型,所有主干的性别表型都可以直接相互转化。
第五,种子和小孢子叶球的时空分布。种子和小孢子叶球的空间分布调查结果表明,种子和小孢子叶球在树体的水平方向上不存在明显差异,在树体的垂直分布上差异显著,从上到下,小孢子叶球的相对密度依次递减,种子的相对密度最高的是中部,最低是下部。种子和小孢子叶球的相对密度在年际间变化明显,都达到了显著水平。50株雌株种子的相对密度在2006年和2007年间呈低度负相关,R=-0.46;26株雄株小孢子叶球的相对密度在2006年和2007年间呈高度正相关,R=0.86。174株雌株的种子相对密度同新枝相对密度及最长新枝长度分别呈低度负相关和微弱负相关,相关系数分别为R=-0.47和R=-0.29。
经过以上研究,我们认为生殖周期长,生殖方式不经济,传粉效率低及雌雄性生殖系统发育不同步是造成云南红豆杉濒危的主要原因。性别比例和搭配及合理利用光因子是人工林建设和管理中首要考虑的问题之一。从性别进化看,红豆杉属植物可能是从雌雄异株向雌雄同株进化,而云南红豆杉处在性别进化的初级阶段。
Taxus yunnanensis Cheng et L. K. Fu, distributing in north Myanmar, north Bhutan and southwest China, is famous for its high content of taxol which is an effective anti-cancer drug, and it becomes a research focus due to its endangered state. Endangered mechanism, however, is unclear till now, thus proper protection measures can not be conducted, and usage of this natural resource is limited. In order to investigate the endangered mechanism, this paper explored reproductive process, pollination mechanism and sexual determination and express in T. yunanens. This study can also contribute to plantation and systematics of T. yunnanensis. Main results are as follow.
First, development of male reproductive system. Development of the pollen cone began in late June. Microsporogenesis occurred in September and November, and microgametogenesis occurred in December and April in the next years. The first meiotic division of the microspore mother cell formed two hemispherical cells. The second meiotic division formed isobilateral, T-shaped or tetrahedron tetrads of microspores. The mature microspores were uninucleate, non-saccate, and with numerous orbicules. During microgametogenesis in vitro, the first, second and third mitotic divisions were observed on the 6th, 20th and 40th days, respectively, and cell walls were formed on the first and second divisions. Spermatogenesis in vivo, the generative nucleus divided in one hemisphere of generative cell and then two equal-sized sperm were formed.
Second, development of female reproductive system, development and germination of embryo. Ovule development began in August, and rectangle megasporocyte began to occur in December, and linear tetrads of megaspores were formed in meiosis. In most occasions, only the chalazal megaspore was functional. Then the functional megaspore nucleus began to divide and form a free-nuclear megagametophyte. Megagametophyte got matured when the walls were formed. Ten or more archegoniums occurred at the edge of megagametophyte, and the egg was found after two mitosises. One of two sperm get into an archegonium and fused with egg. The nucleus of fertilized egg began to divide, and the walls were formed after the third division. The eggs without fertilization divided two times and then disappeared. Pollination, with a rate of 44.7%, was a bottleneck in the ovule development. Simple and cleaved polyembryony were found frequently in the embryo development. In vitro, embryos from the newly matured seeds germinated in 2 weeks, but the germination rate declined as seeds were stored in sands. The Length and structure of embryos were invariable as seeds were stored in sands. It took about 14 years for seedlings get matured in sex.
Third, the anthesis the movement of pollination drops. Microspores were released during the middle of November and the middle of December, and 50% microspores kept alive after been stored in room temperature for 42 days. Mature ovules were present from late December to mid-February in the next year, and the pollination drop were found until mid-March. During pollination, the pollination drops presented for a shorter period, and never appeared once ovules were pollinated. Without being pollinated, the pollination drops presented for a longer period, and it appeared again one more times after disappearance. As alive microspores, the died microspores could be hydrated, and the ovules no longer secret pollination drop once were pollinated.
Fourth, sexual determination and express. Cytologic studies shew that the karyotype of male was 2n=24=24m, and the karyotype of female was 2n=24=23m+1sm,so it was speculated that sex determination in T. yunnanensis was ZZ/ZW. The results of sex expression shew that most individuals were unisexual, the ratio of unisexual individuals was 92.5%, 92% and 94.2% in 2005, 2006, 2007, respectively. In bisexual individuals, most stems was unisexual, the ratio of unisexual stems was 93.6% and 88.7% in 2006 and 2007, respectively. On bisexual stems, most reproductive organs were abnormal. Between years,the gender of most individuals were invariable, and 10% individuals transformed its gender from 2005 to 2006, and 7.6% individuals transformed its gender from 2006 to 2007. Males and females did not transform to each other directly, but males could transform to females by a medium, bisexual state, and females could also transform to males by a medium, unidentified state. Other gender could transform each other directly. In bisexual individuals, most stems were invariable, and 69.4% female stems, 89.4% male stems and 66.7% bisexual stems kept invariable from 2006 to 2007, and all stem gender could transform to each other directly.
Fifth, the distribution of pollen cones and seeds. Spacial distribution of seed and pollen cones shew that there was no obvious difference of the relative concentration of seed and pollen cones in horizontal directions, but the difference in vertical height was significant. Down from the top, relative concentration of pollen cones declined, while relative concentration of seeds was the highest in the middle, and the lowest on the base. Difference of seeds and pollen cones’production between years was significant. The seed production of 50 females in 2006 was negatively related to that in 2007, R=-0.46. The pollen cone production of 26 males in 2006 was positively related to that in 2007, R=0.86. The seed production of 174 females was negatively related to the production of new twigs, R=-0.47, and was negatively related to the length of longest new twigs, R=-0.29.
It can be seen from the results that long life history, uneconomical reproduction, unsynchronizated development between male reproductive system and female reproductive system and ineffective pollination are the possible causes for the endangered state of Taxus yunnanensis. Light and sexual ratio and match are principal factors in developing plantation. In Taxus, monoecious tends to evolve from dioecious, and Taxus yunnanensis is at primary stage in sexual evolution.
第一,雄性生殖系统发育过程。云南红豆杉小孢子叶球从6月底开始发生;小孢子从9月开始发生,11月成熟;雄配子体从12月开始发育,到次年4月产生精子。在小孢子母细胞减数分裂过程中,第一次分裂产生两个半球形细胞,第二次分裂形成T形、正方形或四面体形四分体;成熟的小孢子直径约20微米,单核,没有气囊,表面有大量的乌氏体。离体培养的雄配子体分别在培养后的第6天、第20天和第40天发现第一次、第二次和第三次分裂。在活体中,发生细胞核的分裂在细胞一侧进行,但最终分裂后形成了两个大小相等的精子。
第二,雌性生殖系统发育及胚的发育和萌发过程。云南红豆杉胚珠从8月开始发生,大孢子母细胞12月开始发生,呈方形,减数分裂后形成4个“一”字形大孢子,在大多数情况下,只有靠合点端的大孢子发育为功能大孢子。功能大孢子核随后开始分裂,形成游离核雌配子体,当游离核形成细胞壁,雌配子体即发育成熟。十多个颈卵器在同一个成熟雌配子体上发生,两次有丝分裂后,形成卵细胞。雄配子体产生的两个精子中的一个进入颈卵器与卵细胞结合形成受精卵,受精卵核到第3次分裂形成细胞壁,没有受精的卵细胞还要进行两次有丝分裂后才消失。胚珠发育过程中的数量变化显示:授粉是胚珠发育的瓶颈,胚珠的授粉率只有44.7%。在胚发育过程中,既产生简单多胚,又产生裂生多胚。离体培养中,刚刚成熟种子胚在2周左右萌发,在种子储藏的过程中,胚的结构和长度都没有发生变化,随着储藏时间的延长萌发率逐渐下降。幼苗到性成熟需要14年左右的时间。
第三,花期及传粉滴的活动规律。小孢子叶球的散粉期在11月中旬到12月中旬,小孢子在常温下保存42天,还有50%的花粉具有活力;胚珠成熟期从11月下旬持续到2月中旬,直到3月中旬还可见到带有传粉滴的胚珠。在小孢子叶球散粉期或人工授粉的传粉滴持续存在的时间较短,且授粉后不再出现,在非散粉期的传粉滴持续存在的时间较长,且在消失后又会重新出现。死花粉也具有与活花粉相同的水合性质,授粉后也能引起传粉滴消失并不再出现。
第四,性别控制与性表达。细胞学研究表明:雄性植株的核型为:2n=24=24m;雌性植株的核型为:2n=24=23m+1sm,据此推测云南红豆杉的性别控制类型为ZW型。性别表型构成调查结果显示:在个体水平上,多数植株是单性的,2005、2006和2007年单性植株分别占能辨别性别植株的92.5%、92%和94.2%。在构件水平上,两性植株的大部分主干是单性的,占能辨别性别主干的93.6%(2006年)和88.7%(2007年);在两性主干上,多数小孢子叶球和胚珠都出现异常。性别表型的年际变化调查结果显示:在个体水平上,性别表型发生变化只是少数植株,占能辨别性别植株的10%(2005至2006年)和7.6%(2006至2007年);雌株和雄株不直接相互转化,但雌株通过未知性别植株的过渡,可以转化为雄株,雄株也通过两性植株的过渡转化为雌株,其它各性别表型间都可以直接相互转化。在构件水平上,两性植株的多数主干的性别表型保持不变,雌性主干、雄性主干和两性主干分别有69.4%、89.4%和66.7%保持了原来的性别表型,所有主干的性别表型都可以直接相互转化。
第五,种子和小孢子叶球的时空分布。种子和小孢子叶球的空间分布调查结果表明,种子和小孢子叶球在树体的水平方向上不存在明显差异,在树体的垂直分布上差异显著,从上到下,小孢子叶球的相对密度依次递减,种子的相对密度最高的是中部,最低是下部。种子和小孢子叶球的相对密度在年际间变化明显,都达到了显著水平。50株雌株种子的相对密度在2006年和2007年间呈低度负相关,R=-0.46;26株雄株小孢子叶球的相对密度在2006年和2007年间呈高度正相关,R=0.86。174株雌株的种子相对密度同新枝相对密度及最长新枝长度分别呈低度负相关和微弱负相关,相关系数分别为R=-0.47和R=-0.29。
经过以上研究,我们认为生殖周期长,生殖方式不经济,传粉效率低及雌雄性生殖系统发育不同步是造成云南红豆杉濒危的主要原因。性别比例和搭配及合理利用光因子是人工林建设和管理中首要考虑的问题之一。从性别进化看,红豆杉属植物可能是从雌雄异株向雌雄同株进化,而云南红豆杉处在性别进化的初级阶段。
Taxus yunnanensis Cheng et L. K. Fu, distributing in north Myanmar, north Bhutan and southwest China, is famous for its high content of taxol which is an effective anti-cancer drug, and it becomes a research focus due to its endangered state. Endangered mechanism, however, is unclear till now, thus proper protection measures can not be conducted, and usage of this natural resource is limited. In order to investigate the endangered mechanism, this paper explored reproductive process, pollination mechanism and sexual determination and express in T. yunanens. This study can also contribute to plantation and systematics of T. yunnanensis. Main results are as follow.
First, development of male reproductive system. Development of the pollen cone began in late June. Microsporogenesis occurred in September and November, and microgametogenesis occurred in December and April in the next years. The first meiotic division of the microspore mother cell formed two hemispherical cells. The second meiotic division formed isobilateral, T-shaped or tetrahedron tetrads of microspores. The mature microspores were uninucleate, non-saccate, and with numerous orbicules. During microgametogenesis in vitro, the first, second and third mitotic divisions were observed on the 6th, 20th and 40th days, respectively, and cell walls were formed on the first and second divisions. Spermatogenesis in vivo, the generative nucleus divided in one hemisphere of generative cell and then two equal-sized sperm were formed.
Second, development of female reproductive system, development and germination of embryo. Ovule development began in August, and rectangle megasporocyte began to occur in December, and linear tetrads of megaspores were formed in meiosis. In most occasions, only the chalazal megaspore was functional. Then the functional megaspore nucleus began to divide and form a free-nuclear megagametophyte. Megagametophyte got matured when the walls were formed. Ten or more archegoniums occurred at the edge of megagametophyte, and the egg was found after two mitosises. One of two sperm get into an archegonium and fused with egg. The nucleus of fertilized egg began to divide, and the walls were formed after the third division. The eggs without fertilization divided two times and then disappeared. Pollination, with a rate of 44.7%, was a bottleneck in the ovule development. Simple and cleaved polyembryony were found frequently in the embryo development. In vitro, embryos from the newly matured seeds germinated in 2 weeks, but the germination rate declined as seeds were stored in sands. The Length and structure of embryos were invariable as seeds were stored in sands. It took about 14 years for seedlings get matured in sex.
Third, the anthesis the movement of pollination drops. Microspores were released during the middle of November and the middle of December, and 50% microspores kept alive after been stored in room temperature for 42 days. Mature ovules were present from late December to mid-February in the next year, and the pollination drop were found until mid-March. During pollination, the pollination drops presented for a shorter period, and never appeared once ovules were pollinated. Without being pollinated, the pollination drops presented for a longer period, and it appeared again one more times after disappearance. As alive microspores, the died microspores could be hydrated, and the ovules no longer secret pollination drop once were pollinated.
Fourth, sexual determination and express. Cytologic studies shew that the karyotype of male was 2n=24=24m, and the karyotype of female was 2n=24=23m+1sm,so it was speculated that sex determination in T. yunnanensis was ZZ/ZW. The results of sex expression shew that most individuals were unisexual, the ratio of unisexual individuals was 92.5%, 92% and 94.2% in 2005, 2006, 2007, respectively. In bisexual individuals, most stems was unisexual, the ratio of unisexual stems was 93.6% and 88.7% in 2006 and 2007, respectively. On bisexual stems, most reproductive organs were abnormal. Between years,the gender of most individuals were invariable, and 10% individuals transformed its gender from 2005 to 2006, and 7.6% individuals transformed its gender from 2006 to 2007. Males and females did not transform to each other directly, but males could transform to females by a medium, bisexual state, and females could also transform to males by a medium, unidentified state. Other gender could transform each other directly. In bisexual individuals, most stems were invariable, and 69.4% female stems, 89.4% male stems and 66.7% bisexual stems kept invariable from 2006 to 2007, and all stem gender could transform to each other directly.
Fifth, the distribution of pollen cones and seeds. Spacial distribution of seed and pollen cones shew that there was no obvious difference of the relative concentration of seed and pollen cones in horizontal directions, but the difference in vertical height was significant. Down from the top, relative concentration of pollen cones declined, while relative concentration of seeds was the highest in the middle, and the lowest on the base. Difference of seeds and pollen cones’production between years was significant. The seed production of 50 females in 2006 was negatively related to that in 2007, R=-0.46. The pollen cone production of 26 males in 2006 was positively related to that in 2007, R=0.86. The seed production of 174 females was negatively related to the production of new twigs, R=-0.47, and was negatively related to the length of longest new twigs, R=-0.29.
It can be seen from the results that long life history, uneconomical reproduction, unsynchronizated development between male reproductive system and female reproductive system and ineffective pollination are the possible causes for the endangered state of Taxus yunnanensis. Light and sexual ratio and match are principal factors in developing plantation. In Taxus, monoecious tends to evolve from dioecious, and Taxus yunnanensis is at primary stage in sexual evolution.
引文
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