替码板栗混合芽细胞程序性死亡特征及调控信号因子研究
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摘要
单位面积产量低、土地和光能利用率差是制约中国板栗产业升级的关键问题,而解决这一问题的根本是选育适合集约密植栽培的新品种。替码板栗具有自然更新控冠、树体矮化、修剪省工的独特优势,极其适合密植栽培,但其‘替码’性状形成机制至今尚不清楚。
为研究‘替码’性状是否由混合芽PCD所造成,首先对替码板栗芽体生长发育进程中的形态特征进行了观测,之后采用DNA Ladder检测、PI染色细胞核、流式细胞仪检测凋亡细胞率以及超微细胞结构观察相结合的方法,研究了替码板栗混合芽衰亡进程中细胞内部变化特征,继而为研究几类调控信号因子(内源激素、矿质元素和金属离子)在混合芽PCD进程中的效应和级联关系,以普通板栗混合芽为对照,HPLC、GC和FAAS法测定了替码板栗混合芽PCD进程中上述调控信号因子含量的动态变化,并针对检测结果在树体上进行了诱导回验试验。取得主要研究结果如下：
1.替码板栗枝条上部混合芽在生长发育过程中顺次展现出失水、枯萎和脱落的植物PCD典型形态学特征,认为混合芽自然衰亡是板栗‘替码’性状形成的直接原因。相较同期普通板粟混合芽生长发育形态学特征，把替码板粟合芽自然衰亡历程划分为5个特征明显时期。
2.替码板栗混合芽衰亡进程中(花后20-40d),芽体细胞内部表现出一系列植物PCD典型生化特征,包括：DNA逐渐降解并可检测到"DNA Ladder",PI染色后的细胞核直径逐渐减小、可染性(荧光强度)逐渐降低,凋亡细胞在芽体细胞群体中比率逐渐上升、具完整DNA含量的正常细胞比率逐渐下降。进一步观察细胞超微结构发现,替码板栗混合芽衰亡进程中细胞内部表现出明显的异常变化,并呈现有序的细胞死亡过程,首先液泡数量增多、体积变大,细胞核内核仁消失,继而液泡膜破裂,染色质发生凝聚,叶绿体和线粒体也在液泡膜破裂后逐渐肿胀、解体,期间质壁分离现象出现,最后液泡完全消失,细胞核解体,细胞器降解形成明显碎片,细胞壁皱褶变形,此时胞内完全没有完整细胞核和细胞器存在,此过程中所有细胞器是在质膜包裹下有序地降解。而对照板栗混合芽花后20～40d内,细胞内DNA无降解现象,PI染色细胞核荧光强度不变,细胞群体中凋亡细胞率变化不大,质膜内部细胞核和液泡、线粒体等细胞器一直保持完整、没有裂解现象。总之,替码板栗混合芽自然衰亡进程中细胞异常变化表现出植物细胞程序性死亡(PCD)的典型形态学特征标记和生化标记(真质标记),由此断定替码板栗混合芽细胞异常死亡不是细胞坏死(Necrosis),而是PCD现象,并且主要依据此过程中液泡协同其它细胞器变化的时间和形态特征,认为替码板栗芽体细胞死亡类型属于液泡型细胞死亡(Vacuolar cell death),板栗植株混合芽组织发生PCD是‘替码’性状形成的根本原因。
3.替码板栗混合芽PCD进程中,随着细胞表现出PCD形态和生化特征(花后25d),ZT、ZR含量出现异于普通板栗的下降趋势,而IAA、ABA和Eth却在细胞PCD特征出现前5d(花后20d)含量突然急剧增加,尤以Eth变化最为明显,并在整个DNA降解、细胞器裂解过程中保持较高水平。后续诱导剂回验试验证实,CTK类和IAA均不能诱导板栗混合芽死亡,但可使替码板栗混合芽死亡时间延后,说明ZT、ZR和IAA在混合芽PCD中具有负调控作用,其中ZT、ZR含量缺失可能是芽体PCD的必要因子,而IAA可能在芽体PCD进程中以含量上升的方式来发挥拮抗作用；ABA既可诱导板栗芽体死亡,又可在芽体PCD进程中特定阶段发挥抑制作用,说明其在混合芽PCD进程中具有双重作用；Eth可以刺激替码板栗混合芽PCD进程加速,并可很快诱导混合芽死亡,说明Eth对板栗混合芽PCD不仅具有促进作用,而且具有诱导作用,是PCD发生的正向调控信号因子。进一步通过Eth/ABA分析发现,板栗混合芽发育过程中Eth/ABA存在一种呈波浪式变化的动态平衡,而当这种平衡在替码板栗混合芽内被Eth相对量的增加所打破,既诱导芽体PCD特征出现,因此认为Eth和ABA协同调控着替码板栗芽体PCD的进程,其中Eth是诱导芽体PCD的优势主效调控信号因子。同时芽体PCD执行期开始时间与Eth/ABA剧增时间点一致,认为Eth/ABA可以作为板栗芽体PCD执行期开始的生理标记。
4.替码板栗混合芽PCD进程中,随着细胞PCD形态和生化特征出现(花后25d),芽体N、P含量出现异于对照的下降趋势,而K含量出现与对照下降趋势相反的上升；当替码板栗混合芽PCD形态和生化特征刚出现时,Ca浓度出现剧烈增加,当细胞液泡膜裂解和DNA降解最为严重时期,Ca浓度达到最高值；Fe含量于替码板栗混合芽PCD形态和生化特征出现前5d(花后20d)升高,随着DNA降解开始,Fe含量又急剧增加,至细胞DNA降解最为严重时,伴随DNA Ladder出现,此时混合芽内Fe含量达到最高峰值。以上说明伴随替码板栗混合芽PCD形态和生化特征出现,芽体内N、P、K、Ca含量均出现异于对照品种的变化,推测其参与替码板栗混合芽PCD事件,其中N、P含量的缺失是PCD进行的必要因子,Ca含量上升提高了核酸内切酶活性,保证了PCD的进行,并促进PCD进程加速。Fe于板栗混合芽PCD形态和生化特征出现前含量剧增,推测Fe在混合芽PCD进程中具有正向调控作用。
此研究结果拓展了木本植物器官PCD研究领域,在人为调控替码率、定向改变板栗结果枝组发育模式方面具有重要的理论及应用价值,同时为今后选育适合矮化密植的替码板栗新品种奠定理论基础。
The low yield, low utilization rate of land and light energy were the mostest restriction problem of China's chestnut industry. The apical-bud-senescence chestnut is characterized by the apical mixed bud of fruit bearing shoot, which usually senescence and abscission after flowering and the basal latent bud will develop to new fruit bearing shoot in next year. This has the advantages of facilitating intensive cultivation and increasing production. However the mechanism of mixed bud senescence still remained unknown by now.
In this study, the time course of cell death leading to mixed bud wilting and abscission on chestnuts were first observed, then hallmarks of programmed cell death (PCD) were studied in apical mixed bud undergoing senescence including DNA degradation, nuclear morphology, and cell death ratio and cell ultrastructure morphology, and then the contents of endogenous hormones, mineral elements contents in mixed bud undergoing PCD of chestnut were tested by HPLC, GC and FAAS in order to study the mode of action of these contral signal factors in the process of PCD and wether these control singals could induce the PCD in mixed bud of chestnut. The main results were as follows:
1. The apical mixed bud in shoots be senescenced was the direct cause of character 'apical-bud-senescence'of chestnut. The stage that mixed buds undergoing senescence was subdivided into five distinguished stages by visible symptom.
2. The results showed that DNA degradation occurred in apical mixed bud senescence prior to visible wilting. And nuclear stained with propidium iodide indicated that the fluorescence and diameter of nuclear significantly decreased in mixed bud undergoing senescence of apical-bud-senescence chestnut. Compared to the control chestnut buds, the cell apoptotic ratio, determined by flow cytometry, significantly increased in apical mixed buds undergoing senescence. Further cell ultrastructure detection proved that some characteristic of apoptosis including chromatin condensation, tonoplast invagination and DNA degradation occurred at an early stage of mixed bud senescence. This paper confirmed that PCD did occur in mixed bud of apical-bud-senescence chestnut, and what's more the type of PCD is vacuolar cell death rather than necrosis.
3. When in the progress of mixed buds undergoing PCD in apical-bud-senescence chestnut, contents of ZT and ZR, which was belonged to CTK, declined gradually with the DNA degradation more and more seriously during mixed bud senescence, and it indicated that ZT and ZR have a negative regulatory role in the PCD, the deletion of content of them may be the essential factors of PCD in bud, then spraying KT-30also proved that CTK has an inhibitory role in bud PCD. Content of IAA sharply rose suddenly5d before DNA degradation, and kept high content during the whole DNA degradation, then sharply decreased with the end of DNA degradation in bud. So IAA may be had the negative regulation role in PCD. Changes of ABA in mixed bud of apical-bud-senescence chestnut was similar to Eth, contents of the two hormones sharply rose suddenly5d before DNA degradation in mixed bud, and kept high content, which indicated that ABA and Eth were the induced factors of PCD in mixed bud, then the test of spraying ethylene and ABA indicated that ethylene could induce death of bud quickly, and ABA had the double role in bud cell death. Analysis of Eth/ABA indicated that Eth and ABA have a wave-type dynamic balance, with the sharply increasing of Eth/ABA, the balance was broken by Eth increased and induced physiological changes of PCD in chestnut bud, meantime the start time of PCD was the same to the time of Eth/ABA sharply increased, so Eth/ABA increased could be used as physiololgical markers of the begin of execution in PCD. In summary, in the process of PCD in mixed buds of apical-bud-senescence chestnut, changes of IAA, ABA, and Eth contents were earlier than DNA degradation, and Eth maybe was the main control signals in mixed buds undergoing PCD of apical-bud-senescence chestnut.
4. When in the progress of mixed buds undergoing PCD in apical-bud-senescence chestnut, the PCD process accompanied by degradation of N, P contents, and the degradation time of N, P contents was the same to start time of PCD. With the beginning of the PCD in bud, the content of K presented the upward trend, content of Ca2+sharply increased when PCD started, and significantly higher the former content, then come to the maximum value in the time when DNA degraded most seriously. Content of Fe increased before DNA degradation, and then sharply increased with the beginning of PCD, come to the maximum value in the time when DNA degradation accompanied with appearance of DNA ladder was most seriously30d after bloom in apical mixed bud senescence. The study indicated that with the DNA degradation in the PCD, content changes of N、P、K、Ca and Fe were different with CK, which could indicated that they maybe involve in PCD, and deletion of content of N, P may be the essential factor of PCD, increasing of content of Ca maybe increase the activity of related endoenzyme, which promoted PCD process. Content of Fe sharply increased before DNA degradation, and kept a high content level during DNA degradation, which indicated that Fe may be the positive control signals of PCD.
The datas obtained here may promote the PCD research on woody plants and lay the foundation for artificial regulation of mixed bud senescence so as to remodel the development pattern of fruit branches of chestnut.
为研究‘替码’性状是否由混合芽PCD所造成,首先对替码板栗芽体生长发育进程中的形态特征进行了观测,之后采用DNA Ladder检测、PI染色细胞核、流式细胞仪检测凋亡细胞率以及超微细胞结构观察相结合的方法,研究了替码板栗混合芽衰亡进程中细胞内部变化特征,继而为研究几类调控信号因子(内源激素、矿质元素和金属离子)在混合芽PCD进程中的效应和级联关系,以普通板栗混合芽为对照,HPLC、GC和FAAS法测定了替码板栗混合芽PCD进程中上述调控信号因子含量的动态变化,并针对检测结果在树体上进行了诱导回验试验。取得主要研究结果如下：
1.替码板栗枝条上部混合芽在生长发育过程中顺次展现出失水、枯萎和脱落的植物PCD典型形态学特征,认为混合芽自然衰亡是板栗‘替码’性状形成的直接原因。相较同期普通板粟混合芽生长发育形态学特征，把替码板粟合芽自然衰亡历程划分为5个特征明显时期。
2.替码板栗混合芽衰亡进程中(花后20-40d),芽体细胞内部表现出一系列植物PCD典型生化特征,包括：DNA逐渐降解并可检测到"DNA Ladder",PI染色后的细胞核直径逐渐减小、可染性(荧光强度)逐渐降低,凋亡细胞在芽体细胞群体中比率逐渐上升、具完整DNA含量的正常细胞比率逐渐下降。进一步观察细胞超微结构发现,替码板栗混合芽衰亡进程中细胞内部表现出明显的异常变化,并呈现有序的细胞死亡过程,首先液泡数量增多、体积变大,细胞核内核仁消失,继而液泡膜破裂,染色质发生凝聚,叶绿体和线粒体也在液泡膜破裂后逐渐肿胀、解体,期间质壁分离现象出现,最后液泡完全消失,细胞核解体,细胞器降解形成明显碎片,细胞壁皱褶变形,此时胞内完全没有完整细胞核和细胞器存在,此过程中所有细胞器是在质膜包裹下有序地降解。而对照板栗混合芽花后20～40d内,细胞内DNA无降解现象,PI染色细胞核荧光强度不变,细胞群体中凋亡细胞率变化不大,质膜内部细胞核和液泡、线粒体等细胞器一直保持完整、没有裂解现象。总之,替码板栗混合芽自然衰亡进程中细胞异常变化表现出植物细胞程序性死亡(PCD)的典型形态学特征标记和生化标记(真质标记),由此断定替码板栗混合芽细胞异常死亡不是细胞坏死(Necrosis),而是PCD现象,并且主要依据此过程中液泡协同其它细胞器变化的时间和形态特征,认为替码板栗芽体细胞死亡类型属于液泡型细胞死亡(Vacuolar cell death),板栗植株混合芽组织发生PCD是‘替码’性状形成的根本原因。
3.替码板栗混合芽PCD进程中,随着细胞表现出PCD形态和生化特征(花后25d),ZT、ZR含量出现异于普通板栗的下降趋势,而IAA、ABA和Eth却在细胞PCD特征出现前5d(花后20d)含量突然急剧增加,尤以Eth变化最为明显,并在整个DNA降解、细胞器裂解过程中保持较高水平。后续诱导剂回验试验证实,CTK类和IAA均不能诱导板栗混合芽死亡,但可使替码板栗混合芽死亡时间延后,说明ZT、ZR和IAA在混合芽PCD中具有负调控作用,其中ZT、ZR含量缺失可能是芽体PCD的必要因子,而IAA可能在芽体PCD进程中以含量上升的方式来发挥拮抗作用；ABA既可诱导板栗芽体死亡,又可在芽体PCD进程中特定阶段发挥抑制作用,说明其在混合芽PCD进程中具有双重作用；Eth可以刺激替码板栗混合芽PCD进程加速,并可很快诱导混合芽死亡,说明Eth对板栗混合芽PCD不仅具有促进作用,而且具有诱导作用,是PCD发生的正向调控信号因子。进一步通过Eth/ABA分析发现,板栗混合芽发育过程中Eth/ABA存在一种呈波浪式变化的动态平衡,而当这种平衡在替码板栗混合芽内被Eth相对量的增加所打破,既诱导芽体PCD特征出现,因此认为Eth和ABA协同调控着替码板栗芽体PCD的进程,其中Eth是诱导芽体PCD的优势主效调控信号因子。同时芽体PCD执行期开始时间与Eth/ABA剧增时间点一致,认为Eth/ABA可以作为板栗芽体PCD执行期开始的生理标记。
4.替码板栗混合芽PCD进程中,随着细胞PCD形态和生化特征出现(花后25d),芽体N、P含量出现异于对照的下降趋势,而K含量出现与对照下降趋势相反的上升；当替码板栗混合芽PCD形态和生化特征刚出现时,Ca浓度出现剧烈增加,当细胞液泡膜裂解和DNA降解最为严重时期,Ca浓度达到最高值；Fe含量于替码板栗混合芽PCD形态和生化特征出现前5d(花后20d)升高,随着DNA降解开始,Fe含量又急剧增加,至细胞DNA降解最为严重时,伴随DNA Ladder出现,此时混合芽内Fe含量达到最高峰值。以上说明伴随替码板栗混合芽PCD形态和生化特征出现,芽体内N、P、K、Ca含量均出现异于对照品种的变化,推测其参与替码板栗混合芽PCD事件,其中N、P含量的缺失是PCD进行的必要因子,Ca含量上升提高了核酸内切酶活性,保证了PCD的进行,并促进PCD进程加速。Fe于板栗混合芽PCD形态和生化特征出现前含量剧增,推测Fe在混合芽PCD进程中具有正向调控作用。
此研究结果拓展了木本植物器官PCD研究领域,在人为调控替码率、定向改变板栗结果枝组发育模式方面具有重要的理论及应用价值,同时为今后选育适合矮化密植的替码板栗新品种奠定理论基础。
The low yield, low utilization rate of land and light energy were the mostest restriction problem of China's chestnut industry. The apical-bud-senescence chestnut is characterized by the apical mixed bud of fruit bearing shoot, which usually senescence and abscission after flowering and the basal latent bud will develop to new fruit bearing shoot in next year. This has the advantages of facilitating intensive cultivation and increasing production. However the mechanism of mixed bud senescence still remained unknown by now.
In this study, the time course of cell death leading to mixed bud wilting and abscission on chestnuts were first observed, then hallmarks of programmed cell death (PCD) were studied in apical mixed bud undergoing senescence including DNA degradation, nuclear morphology, and cell death ratio and cell ultrastructure morphology, and then the contents of endogenous hormones, mineral elements contents in mixed bud undergoing PCD of chestnut were tested by HPLC, GC and FAAS in order to study the mode of action of these contral signal factors in the process of PCD and wether these control singals could induce the PCD in mixed bud of chestnut. The main results were as follows:
1. The apical mixed bud in shoots be senescenced was the direct cause of character 'apical-bud-senescence'of chestnut. The stage that mixed buds undergoing senescence was subdivided into five distinguished stages by visible symptom.
2. The results showed that DNA degradation occurred in apical mixed bud senescence prior to visible wilting. And nuclear stained with propidium iodide indicated that the fluorescence and diameter of nuclear significantly decreased in mixed bud undergoing senescence of apical-bud-senescence chestnut. Compared to the control chestnut buds, the cell apoptotic ratio, determined by flow cytometry, significantly increased in apical mixed buds undergoing senescence. Further cell ultrastructure detection proved that some characteristic of apoptosis including chromatin condensation, tonoplast invagination and DNA degradation occurred at an early stage of mixed bud senescence. This paper confirmed that PCD did occur in mixed bud of apical-bud-senescence chestnut, and what's more the type of PCD is vacuolar cell death rather than necrosis.
3. When in the progress of mixed buds undergoing PCD in apical-bud-senescence chestnut, contents of ZT and ZR, which was belonged to CTK, declined gradually with the DNA degradation more and more seriously during mixed bud senescence, and it indicated that ZT and ZR have a negative regulatory role in the PCD, the deletion of content of them may be the essential factors of PCD in bud, then spraying KT-30also proved that CTK has an inhibitory role in bud PCD. Content of IAA sharply rose suddenly5d before DNA degradation, and kept high content during the whole DNA degradation, then sharply decreased with the end of DNA degradation in bud. So IAA may be had the negative regulation role in PCD. Changes of ABA in mixed bud of apical-bud-senescence chestnut was similar to Eth, contents of the two hormones sharply rose suddenly5d before DNA degradation in mixed bud, and kept high content, which indicated that ABA and Eth were the induced factors of PCD in mixed bud, then the test of spraying ethylene and ABA indicated that ethylene could induce death of bud quickly, and ABA had the double role in bud cell death. Analysis of Eth/ABA indicated that Eth and ABA have a wave-type dynamic balance, with the sharply increasing of Eth/ABA, the balance was broken by Eth increased and induced physiological changes of PCD in chestnut bud, meantime the start time of PCD was the same to the time of Eth/ABA sharply increased, so Eth/ABA increased could be used as physiololgical markers of the begin of execution in PCD. In summary, in the process of PCD in mixed buds of apical-bud-senescence chestnut, changes of IAA, ABA, and Eth contents were earlier than DNA degradation, and Eth maybe was the main control signals in mixed buds undergoing PCD of apical-bud-senescence chestnut.
4. When in the progress of mixed buds undergoing PCD in apical-bud-senescence chestnut, the PCD process accompanied by degradation of N, P contents, and the degradation time of N, P contents was the same to start time of PCD. With the beginning of the PCD in bud, the content of K presented the upward trend, content of Ca2+sharply increased when PCD started, and significantly higher the former content, then come to the maximum value in the time when DNA degraded most seriously. Content of Fe increased before DNA degradation, and then sharply increased with the beginning of PCD, come to the maximum value in the time when DNA degradation accompanied with appearance of DNA ladder was most seriously30d after bloom in apical mixed bud senescence. The study indicated that with the DNA degradation in the PCD, content changes of N、P、K、Ca and Fe were different with CK, which could indicated that they maybe involve in PCD, and deletion of content of N, P may be the essential factor of PCD, increasing of content of Ca maybe increase the activity of related endoenzyme, which promoted PCD process. Content of Fe sharply increased before DNA degradation, and kept a high content level during DNA degradation, which indicated that Fe may be the positive control signals of PCD.
The datas obtained here may promote the PCD research on woody plants and lay the foundation for artificial regulation of mixed bud senescence so as to remodel the development pattern of fruit branches of chestnut.
引文
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