S1P、Phyto-S1P和胞质pH在暗诱导气孔关闭中的作用及其与H_2O_2、NO的关系
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摘要
本文以蚕豆和拟南芥为材料,借助气孔试验、激光共聚焦显微镜技术、高效液相色谱技术,研究了鞘氨醇-1-磷酸(S1P)、植物鞘氨醇-1-磷酸(Phyto-S1P)和胞质pH在暗诱导气孔关闭中的作用及其与H202和NO的关系。所得实验结果主要如下：
1.暗明显诱导蚕豆保卫细胞胞质pH、H202和NO水平升高且引起气孔关闭,弱酸丁酸、H202调节剂(H202清除剂ASA、H202清除酶CAT、H202产生酶NADPH氧化酶抑制剂DPI)和NO调节剂(NO清除剂cPTIO、NO合酶抑制剂L-NAME)分别显著抑制上述暗效应,显示胞质碱化、H2O2和NO均参与暗诱导气孔关闭。暗处理10mmin胞质pH即显著升高,20mmin时H202和NO水平才迅速升高,光下甲胺显著提高H202和NO水平,暗中丁酸显著降低H202和NO水平,显示胞质碱化是H202和NO产生的诱导因素。ASA、CAT和DPI明显抑制甲胺触发的NO产生,cPTIO和L-NAME明显抑制甲胺诱导的H2O2产生,显示H2O2介导甲胺触发的NO产生,NO介导甲胺诱导的H2O2产生。胞外和胞内钙螯合剂BAPTA、BAPTA-AM显著阻止暗诱导胞质碱化、H2O2、NO产生和气孔关闭,显示钙通过诱导胞质碱化、H202和NO产生调节暗诱导气孔关闭。
2.暗明显诱导蚕豆S1P和H2O2水平提高且促进气孔关闭,长链碱基激酶抑制剂DL-threo-二氢鞘氨醇(DL-threo-DHS)和N,N-二甲基鞘氨醇(DMS)显著抑制这些暗效应,外源S1P明显诱导气孔关闭和H2O2产生,ASA、CAT和DPI显著抑制S1P的这些效应,显示S1P合成通过触发保卫细胞H2O2产生介导暗诱导气孔关闭。DL-threo-DHS和DMS显著抑制暗诱导保卫细胞胞质碱化和气孔关闭,外源S1P明显诱导保卫细胞胞质碱化和气孔关闭,丁酸明显降低外源S1P的这些效应,显示S1P合成通过诱导胞质碱化介导暗诱导气孔关闭。此外,丁酸明显抑制暗诱导H2O2产生,结合前述S1P通过诱导胞质碱化和H2O2产生调节暗诱导气孔关闭的结果,能够得出S1P引起的胞质碱化是H202产生的先决条件的结论。外源S1P处理后保卫细胞胞质pH升高较H202增加滞后期短且更早达到峰值以及丁酸显著抑制S1P诱导H202产生也支持这一结论。
3.暗明显诱导蚕豆S1P和NO水平提高且促进气孔关闭,DL-threo-DHS和DMS显著抑制这些暗效应,外源S1P明显诱导气孔关闭和NO产生,cPTIO和L-NAME显著抑制S1P的这些效应,显示S1P合成通过触发保卫细胞NO产生介导暗诱导气孔关闭。DL-reo-DHS和DMS显著抑制暗诱导保卫细胞胞质碱化和气孔关闭,外源S1P明显诱导保卫细胞胞质碱化和气孔关闭,丁酸明显降低外源S1P的这些效应,显示S1P合成通过诱导胞质碱化介导暗诱导气孔关闭。此外,丁酸明显抑制暗诱导NO产生,结合前述S1P通过诱导胞质碱化和NO产生调节暗诱导气孔关闭的结果,能够得出S1P引起的胞质碱化是NO产生的先决条件的结论。外源S1P处理后保卫细胞胞质pH升高较NO增加滞后期短且更早达到峰值以及丁酸显著抑制S1P诱导NO产生也支持这一结论。
4. DL-threo-DHS、DMS和SPHK1突变显著抑制暗诱导拟南芥气孔关闭,这些效应可被Phyto-S1P逆转,显示Phyto-S1P参与暗诱导拟南芥气孔关闭。DPI和AtRbohF, AtRbohD/F突变显著抑制、AtRbohD突变不抑制暗诱导拟南芥气孔关闭和H202产生,显示AtrbohF催化产生的H202参与暗诱导拟南芥气孔关闭。L-NAME、硝酸还原酶(NR)抑制剂]Na2WO4和AtNOAl, Nia1、Nia1Nia2突变显著抑制、Nia2突变不抑制暗诱导拟南芥气孔关闭和NO产生,显示暗诱导拟南芥气孔关闭过程中的NO产生依赖于Nia1途径与AtNOA1途径。
5.外源H202和SNP显著逆转DL-threo-DHS、DMS和SPHK1突变抑制暗诱导气孔关闭的效应,但Phyto-S1P不能逆转ASA、CAT和cPTIO抑制暗诱导气孔关闭的效应,而且DL-threo-DHS、DMS和SPHK1突变显著抑制暗诱导H202和NO产生。这些结果表明Phyto-SIP通过触发保卫细胞H202和NO产生介导暗诱导拟南芥气孔关闭。另外,ASA、CAT、DPI和AtRbohF、AtRbohD/F突变显著阻止、AtRbohD突变不阻止外源Phyto-S1P诱导气孔关闭及H202产生,cPTO、L-NAME、Na2WO4和AtNOA1、Nia1、NialNia2突变显著阻止、Nia2突变不阻止外源Phyto-S1P诱导气孔关闭及NO产生。这些结果进一步证明Phyto-S1P通过触发保卫细胞H202和NO产生介导暗诱导拟南芥气孔关闭,Phyto-S1P诱导的H2O2产生由AtrbohF催化,NO产生依赖于Nial途径和AtNOAl途径。
综上所述,本文的结果表明暗提高了蚕豆叶片S1P含量和保卫细胞胞内钙水平,因而引起了胞质碱化,最终诱导H202、NO产生和气孔关闭。另外,Phyto-S1P介导的暗诱导拟南芥气孔关闭中H2O2的产生依赖于AtrbohF,NO的产生依赖于Nia1途径和AtNOAl途径。
In the present study, by means of stomatal bioassays, laser scanning confocal microscopy and high-performance liquid chromatography, whether sphingosine-1-phosphate (SIP), phytosphingosine-1-phosphate (Phyto-S1P) and cytosolic pH are involved in darkness-induced stomatal closure in Vicia faba or Arabidopsis thaliana were studied, and the interrelationships between S1P, Phyto-S1P, cytosolic pH and H2O2, NO during darkness-induced stomatal closure were revealed. The main results are as follows:
1. Darkness obviously raised cytosolic pH, hydrogen peroxide (H2O2) and nitric oxide (NO) levels in guard cells while inducing Vicia faba stomatal closure. These darkness effects were prevented by weak acid butyric acid, H2O2modulators ASA, CAT, DPI and NO modulators c-PTIO, L-NAME, respectively. The data suggested that cytosolic alkalization, H2O2and NO all participate in darkness-induced stomatal closure. During darkness treatment, pH rise became noticeable at10min, while H2O2and NO production significantly increased at20min. The H2O2and NO levels were increased by methylamine in light and decreased by butyric acid in darkness. The results showed that cytosolic alkalization induces H2O2and NO production. ASA, CAT and DPI suppressed NO production by methylamine, c-PTIO and L-NAME prevented H2O2generation by methylamine, suggesting that H2O2mediates NO synthesis by alkalization, and vice versa. Extracellar and intracellar calcium chelators BAPTA and BAPTA-AM restricted darkness-induced cytosolic alkalization, H2O2and NO production and stomatal closure, indicating calcium may act upstream of cytosolic alkalization, H2O2and NO production during darkness-induced stomatal closure.
2. Darkness substantially raised SIP and H2O2levels and closed stomata. These darkness effects were significantly suppressed by DL-threo-dihydrosphingosine (DL-threo-DHS) and N,N-dimethylsphingosine (DMS), two inhibitors of long-chain base kinases. Exogenous S1P led to stomatal closure and H2O2production, and the effects of S1P were largely suppressed by the H2O2modulators ASA, CAT and DPI. These results indicated that SIP mediates darkness-induced stomatal closure by triggering H2O2production. In addition, DL-threo-DHS and DMS significantly suppressed darkness-induced cytosolic alkalization in guard cells and stomatal closure. Exogenous S1P caused cytosolic alkalization and stomatal closure, which could be largely abolished by butyric acid. These results demonstrated that SIP synthesis is necessary for cytosolic alkalization during stomatal closure by darkness. Furthermore, together with the data described above, inhibition of darkness-induced H2O2production by butyric acid revealed that SIP synthesis-induced cytosolic alkalization is a prerequisite for H2O2production during stomatal closure by darkness, a conclusion supported by the facts that the pH increase caused by exogenous S1P had a shorter lag and peaked faster than H2O2levels and that butyric acid prevented exogenous SIP-induced H2O2production.
3. Darkness obviously raised SIP and NO levels and closed stomata. These darkness effects were largely suppressed by DL-threo-DHS and DMS. Exogenous SIP led to stomatal closure and NO production, and the effects of SIP were significantly prevented by cPTIO and L-NAME. These results indicated that S1P mediates darkness-induced stomatal closure by causing NO production. Furthermore, together with the data described above, inhibition of darkness-induced NO production by butyric acid revealed that SIP synthesis-induced cytosolic alkalization is necessary for NO production during stomatal closure by darkness. This conclusion were supported by the facts that the pH increase caused by exogenous SIP had a shorter lag and peaked faster than NO levels and that butyric acid prevented exogenous SI P-induced NO production.
4. DL-threo-DHS, DMS and SPHK1mutation significantly inhibited darkness-induced stomatal closure in Arabidopsis thaliana, these effects were substantially reversed by exgenous Phyto-SIP, showing that Phyto-SIP is involved in darkness-induced stomatal closure. DPI and AtRbohF, AtRbohD/F mutation significantly suppressed darkness-induced stomatal closure and H2O2production, but AtRbohD did not, indicating that H2O2generated by AtrbohF is implicated in darkness-induced stomatal closure. In addition, L-NAME, tungstate and AtNOAl, Nial, NialNia2mutation evidently prevented darkness-induced stomatal closure and NO production, but Nia2mutation did not. The results showed that NO production is dependent on Nial and AtNOAl pathways during darkness-induced stomatal closure.
5. Exogenous H2O2and SNP significantly reversed the inhibitory effects of DL-threo-DHS, DMS and SPHK1mutation on darkness-induced stomatal closure. However, the effects of ASA, CAT and cPTIO on this process couldn't be reversed by exogenous Phyto-SIP. In addition, DL-threo-DHS, DMS and SPHK1mutation largely depressed darkness-induced H2O2and NO production. These results indicated that Phyto-S1P mediates darkness-induced stomatal closure by triggering H2O2and NO production in Arabidopsis thaliana. The further results showed that ASA, CAT, DPI and AtRbohF, AtRbohD/F mutation significantly inhibited Phyto-SIP-induced stomatal closure and H2O2production, but AtRbohD mutation did not. cPTIO, L-NAME, Na2WO4and AtNOAl, Nial, NialNia2mutation could inhibit exogenous Phyto-S IP-induced stomatal closure and NO production, but Nia2mutation could not. The results showed that Phyto-S1P mediates darkness-induced stomatal closure via triggering AtrbohF-dependent H2O2production and AtNOAl-and Nial-dependent NO synthesis in Arabidopsis thaliana.
In conclusion, our results suggested that darkness raises S1P content and intracellular calcium level, hence causes cytosolic alkalization, and finally induces H2O2, NO production and stomatal closure in Vicia faba. Additionally, H2O2production is dependent on AtrbohF and NO synthesis is associated with AtNOA1-and Nial-dependent pathways during Phyto-SIP-mediated darkness-induced stomatal closure in Arabidopsis thaliana.
1.暗明显诱导蚕豆保卫细胞胞质pH、H202和NO水平升高且引起气孔关闭,弱酸丁酸、H202调节剂(H202清除剂ASA、H202清除酶CAT、H202产生酶NADPH氧化酶抑制剂DPI)和NO调节剂(NO清除剂cPTIO、NO合酶抑制剂L-NAME)分别显著抑制上述暗效应,显示胞质碱化、H2O2和NO均参与暗诱导气孔关闭。暗处理10mmin胞质pH即显著升高,20mmin时H202和NO水平才迅速升高,光下甲胺显著提高H202和NO水平,暗中丁酸显著降低H202和NO水平,显示胞质碱化是H202和NO产生的诱导因素。ASA、CAT和DPI明显抑制甲胺触发的NO产生,cPTIO和L-NAME明显抑制甲胺诱导的H2O2产生,显示H2O2介导甲胺触发的NO产生,NO介导甲胺诱导的H2O2产生。胞外和胞内钙螯合剂BAPTA、BAPTA-AM显著阻止暗诱导胞质碱化、H2O2、NO产生和气孔关闭,显示钙通过诱导胞质碱化、H202和NO产生调节暗诱导气孔关闭。
2.暗明显诱导蚕豆S1P和H2O2水平提高且促进气孔关闭,长链碱基激酶抑制剂DL-threo-二氢鞘氨醇(DL-threo-DHS)和N,N-二甲基鞘氨醇(DMS)显著抑制这些暗效应,外源S1P明显诱导气孔关闭和H2O2产生,ASA、CAT和DPI显著抑制S1P的这些效应,显示S1P合成通过触发保卫细胞H2O2产生介导暗诱导气孔关闭。DL-threo-DHS和DMS显著抑制暗诱导保卫细胞胞质碱化和气孔关闭,外源S1P明显诱导保卫细胞胞质碱化和气孔关闭,丁酸明显降低外源S1P的这些效应,显示S1P合成通过诱导胞质碱化介导暗诱导气孔关闭。此外,丁酸明显抑制暗诱导H2O2产生,结合前述S1P通过诱导胞质碱化和H2O2产生调节暗诱导气孔关闭的结果,能够得出S1P引起的胞质碱化是H202产生的先决条件的结论。外源S1P处理后保卫细胞胞质pH升高较H202增加滞后期短且更早达到峰值以及丁酸显著抑制S1P诱导H202产生也支持这一结论。
3.暗明显诱导蚕豆S1P和NO水平提高且促进气孔关闭,DL-threo-DHS和DMS显著抑制这些暗效应,外源S1P明显诱导气孔关闭和NO产生,cPTIO和L-NAME显著抑制S1P的这些效应,显示S1P合成通过触发保卫细胞NO产生介导暗诱导气孔关闭。DL-reo-DHS和DMS显著抑制暗诱导保卫细胞胞质碱化和气孔关闭,外源S1P明显诱导保卫细胞胞质碱化和气孔关闭,丁酸明显降低外源S1P的这些效应,显示S1P合成通过诱导胞质碱化介导暗诱导气孔关闭。此外,丁酸明显抑制暗诱导NO产生,结合前述S1P通过诱导胞质碱化和NO产生调节暗诱导气孔关闭的结果,能够得出S1P引起的胞质碱化是NO产生的先决条件的结论。外源S1P处理后保卫细胞胞质pH升高较NO增加滞后期短且更早达到峰值以及丁酸显著抑制S1P诱导NO产生也支持这一结论。
4. DL-threo-DHS、DMS和SPHK1突变显著抑制暗诱导拟南芥气孔关闭,这些效应可被Phyto-S1P逆转,显示Phyto-S1P参与暗诱导拟南芥气孔关闭。DPI和AtRbohF, AtRbohD/F突变显著抑制、AtRbohD突变不抑制暗诱导拟南芥气孔关闭和H202产生,显示AtrbohF催化产生的H202参与暗诱导拟南芥气孔关闭。L-NAME、硝酸还原酶(NR)抑制剂]Na2WO4和AtNOAl, Nia1、Nia1Nia2突变显著抑制、Nia2突变不抑制暗诱导拟南芥气孔关闭和NO产生,显示暗诱导拟南芥气孔关闭过程中的NO产生依赖于Nia1途径与AtNOA1途径。
5.外源H202和SNP显著逆转DL-threo-DHS、DMS和SPHK1突变抑制暗诱导气孔关闭的效应,但Phyto-S1P不能逆转ASA、CAT和cPTIO抑制暗诱导气孔关闭的效应,而且DL-threo-DHS、DMS和SPHK1突变显著抑制暗诱导H202和NO产生。这些结果表明Phyto-SIP通过触发保卫细胞H202和NO产生介导暗诱导拟南芥气孔关闭。另外,ASA、CAT、DPI和AtRbohF、AtRbohD/F突变显著阻止、AtRbohD突变不阻止外源Phyto-S1P诱导气孔关闭及H202产生,cPTO、L-NAME、Na2WO4和AtNOA1、Nia1、NialNia2突变显著阻止、Nia2突变不阻止外源Phyto-S1P诱导气孔关闭及NO产生。这些结果进一步证明Phyto-S1P通过触发保卫细胞H202和NO产生介导暗诱导拟南芥气孔关闭,Phyto-S1P诱导的H2O2产生由AtrbohF催化,NO产生依赖于Nial途径和AtNOAl途径。
综上所述,本文的结果表明暗提高了蚕豆叶片S1P含量和保卫细胞胞内钙水平,因而引起了胞质碱化,最终诱导H202、NO产生和气孔关闭。另外,Phyto-S1P介导的暗诱导拟南芥气孔关闭中H2O2的产生依赖于AtrbohF,NO的产生依赖于Nia1途径和AtNOAl途径。
In the present study, by means of stomatal bioassays, laser scanning confocal microscopy and high-performance liquid chromatography, whether sphingosine-1-phosphate (SIP), phytosphingosine-1-phosphate (Phyto-S1P) and cytosolic pH are involved in darkness-induced stomatal closure in Vicia faba or Arabidopsis thaliana were studied, and the interrelationships between S1P, Phyto-S1P, cytosolic pH and H2O2, NO during darkness-induced stomatal closure were revealed. The main results are as follows:
1. Darkness obviously raised cytosolic pH, hydrogen peroxide (H2O2) and nitric oxide (NO) levels in guard cells while inducing Vicia faba stomatal closure. These darkness effects were prevented by weak acid butyric acid, H2O2modulators ASA, CAT, DPI and NO modulators c-PTIO, L-NAME, respectively. The data suggested that cytosolic alkalization, H2O2and NO all participate in darkness-induced stomatal closure. During darkness treatment, pH rise became noticeable at10min, while H2O2and NO production significantly increased at20min. The H2O2and NO levels were increased by methylamine in light and decreased by butyric acid in darkness. The results showed that cytosolic alkalization induces H2O2and NO production. ASA, CAT and DPI suppressed NO production by methylamine, c-PTIO and L-NAME prevented H2O2generation by methylamine, suggesting that H2O2mediates NO synthesis by alkalization, and vice versa. Extracellar and intracellar calcium chelators BAPTA and BAPTA-AM restricted darkness-induced cytosolic alkalization, H2O2and NO production and stomatal closure, indicating calcium may act upstream of cytosolic alkalization, H2O2and NO production during darkness-induced stomatal closure.
2. Darkness substantially raised SIP and H2O2levels and closed stomata. These darkness effects were significantly suppressed by DL-threo-dihydrosphingosine (DL-threo-DHS) and N,N-dimethylsphingosine (DMS), two inhibitors of long-chain base kinases. Exogenous S1P led to stomatal closure and H2O2production, and the effects of S1P were largely suppressed by the H2O2modulators ASA, CAT and DPI. These results indicated that SIP mediates darkness-induced stomatal closure by triggering H2O2production. In addition, DL-threo-DHS and DMS significantly suppressed darkness-induced cytosolic alkalization in guard cells and stomatal closure. Exogenous S1P caused cytosolic alkalization and stomatal closure, which could be largely abolished by butyric acid. These results demonstrated that SIP synthesis is necessary for cytosolic alkalization during stomatal closure by darkness. Furthermore, together with the data described above, inhibition of darkness-induced H2O2production by butyric acid revealed that SIP synthesis-induced cytosolic alkalization is a prerequisite for H2O2production during stomatal closure by darkness, a conclusion supported by the facts that the pH increase caused by exogenous S1P had a shorter lag and peaked faster than H2O2levels and that butyric acid prevented exogenous SIP-induced H2O2production.
3. Darkness obviously raised SIP and NO levels and closed stomata. These darkness effects were largely suppressed by DL-threo-DHS and DMS. Exogenous SIP led to stomatal closure and NO production, and the effects of SIP were significantly prevented by cPTIO and L-NAME. These results indicated that S1P mediates darkness-induced stomatal closure by causing NO production. Furthermore, together with the data described above, inhibition of darkness-induced NO production by butyric acid revealed that SIP synthesis-induced cytosolic alkalization is necessary for NO production during stomatal closure by darkness. This conclusion were supported by the facts that the pH increase caused by exogenous SIP had a shorter lag and peaked faster than NO levels and that butyric acid prevented exogenous SI P-induced NO production.
4. DL-threo-DHS, DMS and SPHK1mutation significantly inhibited darkness-induced stomatal closure in Arabidopsis thaliana, these effects were substantially reversed by exgenous Phyto-SIP, showing that Phyto-SIP is involved in darkness-induced stomatal closure. DPI and AtRbohF, AtRbohD/F mutation significantly suppressed darkness-induced stomatal closure and H2O2production, but AtRbohD did not, indicating that H2O2generated by AtrbohF is implicated in darkness-induced stomatal closure. In addition, L-NAME, tungstate and AtNOAl, Nial, NialNia2mutation evidently prevented darkness-induced stomatal closure and NO production, but Nia2mutation did not. The results showed that NO production is dependent on Nial and AtNOAl pathways during darkness-induced stomatal closure.
5. Exogenous H2O2and SNP significantly reversed the inhibitory effects of DL-threo-DHS, DMS and SPHK1mutation on darkness-induced stomatal closure. However, the effects of ASA, CAT and cPTIO on this process couldn't be reversed by exogenous Phyto-SIP. In addition, DL-threo-DHS, DMS and SPHK1mutation largely depressed darkness-induced H2O2and NO production. These results indicated that Phyto-S1P mediates darkness-induced stomatal closure by triggering H2O2and NO production in Arabidopsis thaliana. The further results showed that ASA, CAT, DPI and AtRbohF, AtRbohD/F mutation significantly inhibited Phyto-SIP-induced stomatal closure and H2O2production, but AtRbohD mutation did not. cPTIO, L-NAME, Na2WO4and AtNOAl, Nial, NialNia2mutation could inhibit exogenous Phyto-S IP-induced stomatal closure and NO production, but Nia2mutation could not. The results showed that Phyto-S1P mediates darkness-induced stomatal closure via triggering AtrbohF-dependent H2O2production and AtNOAl-and Nial-dependent NO synthesis in Arabidopsis thaliana.
In conclusion, our results suggested that darkness raises S1P content and intracellular calcium level, hence causes cytosolic alkalization, and finally induces H2O2, NO production and stomatal closure in Vicia faba. Additionally, H2O2production is dependent on AtrbohF and NO synthesis is associated with AtNOA1-and Nial-dependent pathways during Phyto-SIP-mediated darkness-induced stomatal closure in Arabidopsis thaliana.
引文
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