新型水仙生物碱Narciclasine影响植物根发育的特征及调控机理
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摘要
天然产物Narciclasine (NCS)是一种从水仙鳞茎中提取的新型水仙生物碱,具生长与发育以及对环境刺激响应中发挥着关键作用。根据已有的研究成果和植物对NCS的一些特殊生理响应,推断NCS可能通过干扰生长素信号传导或生长素运输等进而影响了一些依赖生长素的生长发育过程。为此,本研究主要以模式植物拟南芥与水稻等为实验材料,对NCS影响依赖生长素的生长发育过程等问题进行深入研究。主要研究结果如下：
1.NCS抑制了拟南芥根对生长素的生理响应。
NCS通过干扰拟南芥根对外源生长素的敏感性进而抑制了生长素促进侧根及根毛的发育。与野生型相比,生长素信号突变体axrl-3和axrl-12的主根伸长对低浓度NCS的抑制作用表现出适度抗性,表明NCS可能间接影响了SCFTIR1/AFB泛素连接酶复合物介导的生长素信号传导。利用生长素响应GUS报告基因、生长素响应的天然型启动子基因.IAA12::GUS, IAA13::GUS及qRT-PCR检测发现,NCS对生长素响应基因的表达具有明显的抑制作用；ELASA检测结果表明NCS处理对拟南芥幼苗中的IAA含量没有产生明显影响,表明NCS并未影响生长素的生物合成。利用拟南芥HS::AXR3NT-GUS报告系分析发现NCS能够缓解SCFTIR1/AFB复合物介导的生长素诱导Aux/IAA蛋白的泛素化降解过程；生化实验结果表明,NCS对Aux/IAA蛋白稳定性的作用不是通过影响26S蛋白酶体的活性来实现；体外Pull-down结果表明,NCS处理并不能促进Myc-TIR1与IAA7/AXR2(Aux/IAA proteins)相互作用,说明NCS可能是通过改变SCFTIRl／AFB复合物某些上游元件进而对生长素信号产生抑制作用。综上所述,NCS抑制拟南芥根对生长素的响应可能是通过作用于生长素信号传导途径来实现。
2.NCS通过调节生长素运输蛋白的表达进而影响生长素的运输。
NCS处理能引起拟南芥幼苗的根失去向地性,这与生长素运输抑制TIBA和NPA处理后的特征类似。DR5::GUS报告基因检测结果显示NCS扰乱了拟南芥根尖生长素的正常分布;通过淀粉粒染色发现NCS处理影响依赖生长素的根冠小柱细胞的正常发育;在向重力刺激下,DR5-GFP报告系显微分析发现NCS抑制了生长素迅速向根尖底侧细胞中的迅速积累,这些结果说明NCS对根向地性及根尖生长素再分布的影响与生长素运输有关。BY-2细胞中[3H]IAA的积累实验表明NCS抑制了生长素运输载体介导[3H]IAA的内流及外流。利用包含PINs-GFP, AUX1-YFP融合蛋白的转基因拟南芥检测发现,NCS处理12h拟南芥根中生长素外流载体蛋白PINs和内流载体蛋白AUXl的表达丰度明显降低;qRT-PCR进一步分析发现NCS在转录水平也能调节生长素运输载体基因的表达,说明NCS在转录水平及蛋白水平均能调节生长素运输蛋白的表达。
3.NCS影响了生长素载体蛋白的胞内转运。
对生长素载体蛋白亚细胞定位分析发现,尽管NCS没有影响PINs及AUXl蛋白在细胞质膜上的定位,但是PIN2-GFP, PIN3-GFP, PIN4-GFP, PIN7-GFP和AUX1-YFP却在胞内迅速内化并形成蛋白聚集物,我们将这类蛋白聚集物称为“NCS小体”。利用标记囊泡的荧光染料FM4-64染色发现NCS促进了植物细胞的胞吞作用。将NCS处理过的PIN2-GFP幼苗进行FM4-64染色发现,以NCS小体形式存在的PIN2-GFP与FM4-64标记的囊泡发生部分重合,说明NCS通过细胞的胞吞作用诱导质膜上的生长素运输蛋白内陷到胞内形成蛋白聚集物。蛋白质合成抑制剂CHX和NCS共同处理的结果表明,NCS产生这种细胞效应独立于蛋白质的合成及新合成蛋白质向质膜的转运。NCS处理对BRIl-GFP、PIP2-GFP和GFP-LTI6b三种膜融合蛋白的膜定位及胞内转运未产生明显影响,说明NCS对膜蛋白的作用具有选择性。利用ARA7-GFP, NAG-GFP, SYP22-YFP和SYP61-CFP特殊的内膜系统标记系亚细胞定位分析发现,NCS对内膜系统的影响也具有选择性。此外,利用微丝骨架ABD2-GFP转基因系分析发现NCS处理后破坏了肌动蛋白微丝的结构,导致束状的蛋白微丝减少。通过对内体小泡标记蛋白ARA7-GFP的分析发现NCS处理后减缓了内体小泡的运输速率。
4.NCS影响了水稻幼苗根系的发育。
NCS抑制了水稻根的生长、减少了侧根数目,但是促进不定根的形成。进一步研究发现NCS明显抑制了外源生长素对水稻根系的促进作用,这与拟南芥中的研究结果类似,暗示NCS可能也影响了水稻中生长素运输及信号转导等过程。利用水稻DR5:GUS转基因系发现NCS明显干扰了生长素对DR5:GUS报告基因的诱导作用,说明NCS可能通过影响生长素信号传导过程抑制了水稻中生长素响应基因的表达。RT-PCR结果显示NCS能够影响水稻根中生长素运输基因的表达。通过对[3H]-IAA放射性检测发现NCS影响了水稻根中生长素向顶和向基的运输,这些结果表明NCS对水稻根中生长素运输也有影响。NCS处理引起水稻根呈螺旋状生长,我们推测可能是NCS影响生长素的运输使得其在水稻根中的分布改变所致。
Natural product narciclasine (NCS) is a new Amaryllidaceae alkaloid isolated from Narcissus tazetta bulbs and possesses a broad range of biological activities such as antimitotic and antiviral functions. A broad range of inhibitory effects of NCS in plant were found, however, it is still poorly understood about the molecular mechanisms of NCS involvement in plant developmental responses. The plant hormone auxin plays a central role in the regulation of plant growth and development, as well as in responses to environmental stimuli. Basing on the preliminary studies and some special physiology responses of NCS to plant, we hypothesized that NCS may act as an auxin response inhibitor through interfering with auxin signaling pathway or/and auxin transport to affect the auxin-mediated growth and development process. In the present study, the model plant Arabidopsis and rice was used as materials to further study the mechanism of the effects of NCS on the auxin-mediated growth and development process. The main results are as follows:
1. NCS inhibits the physiological responses of Arabidopsis root to auxin.
The inhibitory effects of NCS on auxin-inducible lateral root and root hair formation by altering the sensitivity of Arabidopsis roots to auxin were demonstrated. The auxin insensitive mutant axr1-3and axr1-12showed a modest resistance to lower concentrations of NCS in primary root elongation compared to WT seedlings, indicating that NCS may indirectly affect theFTIR1/AFB complex-mediated auxin signaling. It was also found that NCS inhibited the expression of primary auxin-inducible genes in Arabidopsis roots using DR5::GUS reporter gene, native auxin promoters (IAA12::GUS, LAA13::GUS) and quantitative reverse transcription PCR analysis. It was further indicated that NCS treatment did not affect the endogenous IAA content in Arabidopsis roots by ELISA assaysis, demonstrating that NCS dose not inhibit auxin biosynthesis. Analysis of Arabidopsis HS::AXR3NT-GUS line showed that NCS relieved the auxin-enhanced degradation of Aux/1AA repressor modulated by the SCFTIR1ubiquitin-proteasome pathway. Biochemical experiments indicated that the impairment of NCS on the degradation of Aux/IAA proteins was not achieved by inhibiting the26S proteasome activity. In addition, the pull-down assay in vitro demonstrated that NCS did not alter the auxin-stimulated interaction between IAA7/AXR2(Aux/IAA proteins) and the F-box protein TIRl activity, suggesting that the inhibition of NCS to auxin signaling maybe by modulating to the some upstream elements of SCFTIR1/AFB complex. In conclusion, NCS inhibits the responses of Arabidopsis roots to auxin by probably affecting on auxin signaling transduction.
2. NCS affects auxin transport through modulating the expression of auxin transport proteins in Arabidopsis roots.
NCS treatments can cause defects in root gravitropism of Arabidopsis seedlings, which is similar to the characteristic of auxin transport inhibitors TIBA and NPA. The results by DR5::GUS reporter detection showed that the distribution of auxin in Arabidopsis root tips was disturbed by NCS. NCS also affected the auxin-dependent organization of columella cells by starch grain staining. After stimulation of gravity, NCS inhibited asymmetry auxin flow, and no auxin accumulation occurred at the lower side of the root by detecting of auxin response reporter DR5rev::GFP. These results suggested that NCS disturbed asymmetric auxin distribution and root gravitropic responses associated with related to auxin transport in Arabidopsis roots. NCS inhibited both cellular [3H]-IAA import and export by [3H]-IAA radiotracer transport assay in cultured BY-2cells. Using transgenic plants containing the promoters of PINs and AUX1, we found that the expression levels of PIN proteins and AUX1are substantially reduced after12h NCS treatments. qRT-PCR analysis further showed that the expressions of auxin transport genes in Arabidopsis roots was also regulated under NCS treatment. These results indicated that NCS negatively modulates auxin transport in the root is due to a general reduction of auxin carrier protein expression at the transcriptional level and protein level.
3. NCS affects the intracellular trafficking of auxin carrier proteins.
The analysis to the subcellular localization of auxin carrier proteins in the root tips of Arabidopsis seedlings showed that NCS did not affect the localization of PINs and AUXI proteins in the plasma membrane but PIN2-GFP, PIN3-GFP, PIN4-GFP, PIN7-GFP and AUX1-YFP in the plasma membrane were rapid internalized and formed intracellular agglomerations that we termed as "NCS bodies". The observation of fluorescent images showed that NCS promoted general endocytosis traced by styryl dye FM4-64staining labeled vesicles. Results further indicated that NCS-induced intracellular compartments of PIN2-GFP partially co-localized by the staining to PIN2-GFP seedlings in NCS treatment with the membrane-selective endocytic tracer FM4-64, suggesting that the internalization of auxin carrier proteins and formation intracellular agglomerations induced by NCS was dependent on endocytosis pathway. The treatments of CHX (an inhibitor of protein biosynthesis) and NCS indicated that the effect of NCS on endocytosis was independent of protein synthesis and the delivery of newly synthesized proteins to the PM. Furthermore, the membrane localization and the intracellular transfor of the three membrane fusion proteins BRI1-GFP, PIP2-GFP and LTI6B-GFP was not affected by NCS treatment, demonstrating that the effect of NCS on the stability of membrane proteins has pronounced proteins specificity. The analysisi of subcellular localization by using endomembrane markers ARA7-GFP, NAG-GFP, SYP22-YFP and SYP61-CFP showed that NCS also exhibited the specificity. In addition, the results by using the transgenic plant ABD2-GFP of actin cytoskeleton demonstrated that NCS could disrupt the structure of actin cytoskeletal organization and lead to decrease in the protein filaments. Using real-time live-cell microscopy, we also found that NCS influences actin-based vesicle motility through endosomal markers protein ARA7-GFP.
4. NCS modulates the development of root system in rice seedlings.
NCS inhibits rice root growth and diminishes the number of lateral roots, but it promotes adventitious root formation in rice seedlings. NCS also inhibits the promotion of exogenous auxin on rice root architecture, which is similar to the observations in Arabidopsis, suggesting that NCS may also interferred with auxin signaling or auxin transport in rice seedlings. Histochemical staining showed that auxin-induced DR5gene expression was markedly decreased in rice root tips after NCS treatment, impling that the inhibitory effect of NCS on auxin-responsive gene expression is also achieved by directly affecting the auxin signaling. Semiquantitative RT-PCR analysis demonstrated that NCS inhibited the expression of putative OsPIN genes in rice roots. The assay of in nanoscale [3H]-IAA radiotracer transport in rice roots showed that NCS reduced the acropetal or basipetal [3H]-IAA transport, respectively. These results revealed that NCS also affects auxin transport in rice roots. Very interesting, the phenotype of spiral roots was observed in0.5μM NCS treatment, which maybe due to the alteration in auxin distribution by disruption of auxin transport in NCS treatment.
1.NCS抑制了拟南芥根对生长素的生理响应。
NCS通过干扰拟南芥根对外源生长素的敏感性进而抑制了生长素促进侧根及根毛的发育。与野生型相比,生长素信号突变体axrl-3和axrl-12的主根伸长对低浓度NCS的抑制作用表现出适度抗性,表明NCS可能间接影响了SCFTIR1/AFB泛素连接酶复合物介导的生长素信号传导。利用生长素响应GUS报告基因、生长素响应的天然型启动子基因.IAA12::GUS, IAA13::GUS及qRT-PCR检测发现,NCS对生长素响应基因的表达具有明显的抑制作用；ELASA检测结果表明NCS处理对拟南芥幼苗中的IAA含量没有产生明显影响,表明NCS并未影响生长素的生物合成。利用拟南芥HS::AXR3NT-GUS报告系分析发现NCS能够缓解SCFTIR1/AFB复合物介导的生长素诱导Aux/IAA蛋白的泛素化降解过程；生化实验结果表明,NCS对Aux/IAA蛋白稳定性的作用不是通过影响26S蛋白酶体的活性来实现；体外Pull-down结果表明,NCS处理并不能促进Myc-TIR1与IAA7/AXR2(Aux/IAA proteins)相互作用,说明NCS可能是通过改变SCFTIRl／AFB复合物某些上游元件进而对生长素信号产生抑制作用。综上所述,NCS抑制拟南芥根对生长素的响应可能是通过作用于生长素信号传导途径来实现。
2.NCS通过调节生长素运输蛋白的表达进而影响生长素的运输。
NCS处理能引起拟南芥幼苗的根失去向地性,这与生长素运输抑制TIBA和NPA处理后的特征类似。DR5::GUS报告基因检测结果显示NCS扰乱了拟南芥根尖生长素的正常分布;通过淀粉粒染色发现NCS处理影响依赖生长素的根冠小柱细胞的正常发育;在向重力刺激下,DR5-GFP报告系显微分析发现NCS抑制了生长素迅速向根尖底侧细胞中的迅速积累,这些结果说明NCS对根向地性及根尖生长素再分布的影响与生长素运输有关。BY-2细胞中[3H]IAA的积累实验表明NCS抑制了生长素运输载体介导[3H]IAA的内流及外流。利用包含PINs-GFP, AUX1-YFP融合蛋白的转基因拟南芥检测发现,NCS处理12h拟南芥根中生长素外流载体蛋白PINs和内流载体蛋白AUXl的表达丰度明显降低;qRT-PCR进一步分析发现NCS在转录水平也能调节生长素运输载体基因的表达,说明NCS在转录水平及蛋白水平均能调节生长素运输蛋白的表达。
3.NCS影响了生长素载体蛋白的胞内转运。
对生长素载体蛋白亚细胞定位分析发现,尽管NCS没有影响PINs及AUXl蛋白在细胞质膜上的定位,但是PIN2-GFP, PIN3-GFP, PIN4-GFP, PIN7-GFP和AUX1-YFP却在胞内迅速内化并形成蛋白聚集物,我们将这类蛋白聚集物称为“NCS小体”。利用标记囊泡的荧光染料FM4-64染色发现NCS促进了植物细胞的胞吞作用。将NCS处理过的PIN2-GFP幼苗进行FM4-64染色发现,以NCS小体形式存在的PIN2-GFP与FM4-64标记的囊泡发生部分重合,说明NCS通过细胞的胞吞作用诱导质膜上的生长素运输蛋白内陷到胞内形成蛋白聚集物。蛋白质合成抑制剂CHX和NCS共同处理的结果表明,NCS产生这种细胞效应独立于蛋白质的合成及新合成蛋白质向质膜的转运。NCS处理对BRIl-GFP、PIP2-GFP和GFP-LTI6b三种膜融合蛋白的膜定位及胞内转运未产生明显影响,说明NCS对膜蛋白的作用具有选择性。利用ARA7-GFP, NAG-GFP, SYP22-YFP和SYP61-CFP特殊的内膜系统标记系亚细胞定位分析发现,NCS对内膜系统的影响也具有选择性。此外,利用微丝骨架ABD2-GFP转基因系分析发现NCS处理后破坏了肌动蛋白微丝的结构,导致束状的蛋白微丝减少。通过对内体小泡标记蛋白ARA7-GFP的分析发现NCS处理后减缓了内体小泡的运输速率。
4.NCS影响了水稻幼苗根系的发育。
NCS抑制了水稻根的生长、减少了侧根数目,但是促进不定根的形成。进一步研究发现NCS明显抑制了外源生长素对水稻根系的促进作用,这与拟南芥中的研究结果类似,暗示NCS可能也影响了水稻中生长素运输及信号转导等过程。利用水稻DR5:GUS转基因系发现NCS明显干扰了生长素对DR5:GUS报告基因的诱导作用,说明NCS可能通过影响生长素信号传导过程抑制了水稻中生长素响应基因的表达。RT-PCR结果显示NCS能够影响水稻根中生长素运输基因的表达。通过对[3H]-IAA放射性检测发现NCS影响了水稻根中生长素向顶和向基的运输,这些结果表明NCS对水稻根中生长素运输也有影响。NCS处理引起水稻根呈螺旋状生长,我们推测可能是NCS影响生长素的运输使得其在水稻根中的分布改变所致。
Natural product narciclasine (NCS) is a new Amaryllidaceae alkaloid isolated from Narcissus tazetta bulbs and possesses a broad range of biological activities such as antimitotic and antiviral functions. A broad range of inhibitory effects of NCS in plant were found, however, it is still poorly understood about the molecular mechanisms of NCS involvement in plant developmental responses. The plant hormone auxin plays a central role in the regulation of plant growth and development, as well as in responses to environmental stimuli. Basing on the preliminary studies and some special physiology responses of NCS to plant, we hypothesized that NCS may act as an auxin response inhibitor through interfering with auxin signaling pathway or/and auxin transport to affect the auxin-mediated growth and development process. In the present study, the model plant Arabidopsis and rice was used as materials to further study the mechanism of the effects of NCS on the auxin-mediated growth and development process. The main results are as follows:
1. NCS inhibits the physiological responses of Arabidopsis root to auxin.
The inhibitory effects of NCS on auxin-inducible lateral root and root hair formation by altering the sensitivity of Arabidopsis roots to auxin were demonstrated. The auxin insensitive mutant axr1-3and axr1-12showed a modest resistance to lower concentrations of NCS in primary root elongation compared to WT seedlings, indicating that NCS may indirectly affect theFTIR1/AFB complex-mediated auxin signaling. It was also found that NCS inhibited the expression of primary auxin-inducible genes in Arabidopsis roots using DR5::GUS reporter gene, native auxin promoters (IAA12::GUS, LAA13::GUS) and quantitative reverse transcription PCR analysis. It was further indicated that NCS treatment did not affect the endogenous IAA content in Arabidopsis roots by ELISA assaysis, demonstrating that NCS dose not inhibit auxin biosynthesis. Analysis of Arabidopsis HS::AXR3NT-GUS line showed that NCS relieved the auxin-enhanced degradation of Aux/1AA repressor modulated by the SCFTIR1ubiquitin-proteasome pathway. Biochemical experiments indicated that the impairment of NCS on the degradation of Aux/IAA proteins was not achieved by inhibiting the26S proteasome activity. In addition, the pull-down assay in vitro demonstrated that NCS did not alter the auxin-stimulated interaction between IAA7/AXR2(Aux/IAA proteins) and the F-box protein TIRl activity, suggesting that the inhibition of NCS to auxin signaling maybe by modulating to the some upstream elements of SCFTIR1/AFB complex. In conclusion, NCS inhibits the responses of Arabidopsis roots to auxin by probably affecting on auxin signaling transduction.
2. NCS affects auxin transport through modulating the expression of auxin transport proteins in Arabidopsis roots.
NCS treatments can cause defects in root gravitropism of Arabidopsis seedlings, which is similar to the characteristic of auxin transport inhibitors TIBA and NPA. The results by DR5::GUS reporter detection showed that the distribution of auxin in Arabidopsis root tips was disturbed by NCS. NCS also affected the auxin-dependent organization of columella cells by starch grain staining. After stimulation of gravity, NCS inhibited asymmetry auxin flow, and no auxin accumulation occurred at the lower side of the root by detecting of auxin response reporter DR5rev::GFP. These results suggested that NCS disturbed asymmetric auxin distribution and root gravitropic responses associated with related to auxin transport in Arabidopsis roots. NCS inhibited both cellular [3H]-IAA import and export by [3H]-IAA radiotracer transport assay in cultured BY-2cells. Using transgenic plants containing the promoters of PINs and AUX1, we found that the expression levels of PIN proteins and AUX1are substantially reduced after12h NCS treatments. qRT-PCR analysis further showed that the expressions of auxin transport genes in Arabidopsis roots was also regulated under NCS treatment. These results indicated that NCS negatively modulates auxin transport in the root is due to a general reduction of auxin carrier protein expression at the transcriptional level and protein level.
3. NCS affects the intracellular trafficking of auxin carrier proteins.
The analysis to the subcellular localization of auxin carrier proteins in the root tips of Arabidopsis seedlings showed that NCS did not affect the localization of PINs and AUXI proteins in the plasma membrane but PIN2-GFP, PIN3-GFP, PIN4-GFP, PIN7-GFP and AUX1-YFP in the plasma membrane were rapid internalized and formed intracellular agglomerations that we termed as "NCS bodies". The observation of fluorescent images showed that NCS promoted general endocytosis traced by styryl dye FM4-64staining labeled vesicles. Results further indicated that NCS-induced intracellular compartments of PIN2-GFP partially co-localized by the staining to PIN2-GFP seedlings in NCS treatment with the membrane-selective endocytic tracer FM4-64, suggesting that the internalization of auxin carrier proteins and formation intracellular agglomerations induced by NCS was dependent on endocytosis pathway. The treatments of CHX (an inhibitor of protein biosynthesis) and NCS indicated that the effect of NCS on endocytosis was independent of protein synthesis and the delivery of newly synthesized proteins to the PM. Furthermore, the membrane localization and the intracellular transfor of the three membrane fusion proteins BRI1-GFP, PIP2-GFP and LTI6B-GFP was not affected by NCS treatment, demonstrating that the effect of NCS on the stability of membrane proteins has pronounced proteins specificity. The analysisi of subcellular localization by using endomembrane markers ARA7-GFP, NAG-GFP, SYP22-YFP and SYP61-CFP showed that NCS also exhibited the specificity. In addition, the results by using the transgenic plant ABD2-GFP of actin cytoskeleton demonstrated that NCS could disrupt the structure of actin cytoskeletal organization and lead to decrease in the protein filaments. Using real-time live-cell microscopy, we also found that NCS influences actin-based vesicle motility through endosomal markers protein ARA7-GFP.
4. NCS modulates the development of root system in rice seedlings.
NCS inhibits rice root growth and diminishes the number of lateral roots, but it promotes adventitious root formation in rice seedlings. NCS also inhibits the promotion of exogenous auxin on rice root architecture, which is similar to the observations in Arabidopsis, suggesting that NCS may also interferred with auxin signaling or auxin transport in rice seedlings. Histochemical staining showed that auxin-induced DR5gene expression was markedly decreased in rice root tips after NCS treatment, impling that the inhibitory effect of NCS on auxin-responsive gene expression is also achieved by directly affecting the auxin signaling. Semiquantitative RT-PCR analysis demonstrated that NCS inhibited the expression of putative OsPIN genes in rice roots. The assay of in nanoscale [3H]-IAA radiotracer transport in rice roots showed that NCS reduced the acropetal or basipetal [3H]-IAA transport, respectively. These results revealed that NCS also affects auxin transport in rice roots. Very interesting, the phenotype of spiral roots was observed in0.5μM NCS treatment, which maybe due to the alteration in auxin distribution by disruption of auxin transport in NCS treatment.
引文
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