外源腐胺缓解黄瓜幼苗盐胁迫伤害的光合作用机理
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摘要
土壤盐渍化对农业生产的威胁是一个世界性的热点问题,也是影响全球生态环境的重要因素之一。近年来,随着设施园艺面积的不断扩大,我国已成为设施园艺大国。然而,由于不科学的施肥和灌溉,加之保护设施的特殊环境,导致设施土壤次生盐渍化日益严重,制约了我国设施园艺健康和可持续的发展。黄瓜(Cucumis sativus L.)是我国设施栽培面积最广的蔬菜作物之一,其根系对盐渍环境非常敏感,当土壤发生盐害时,黄瓜植株光化学效率明显降低,生长发育会受到显著抑制,严重影响了黄瓜的产量和品质。多胺(Polyamines,PAs)作为一种新型的植物生长调节物质,是生物体代谢过程中产生的一类具有强烈生物活性的低分子量脂肪族含氮碱。多胺在逆境胁迫中不仅作为一种直接的胁迫保护物质,而且作为一种信号分子间接地参与信号转导,有利于植物逆境胁迫抗性机制的构建。目前,国内外关于多胺可提高逆境胁迫下植物光合作用能力的观点已得到了普遍认可。然而,关于多胺缓解盐胁迫下植株光化学效率下降的机制至今仍缺乏深入研究。
本文以盐敏感的黄瓜品种‘津优4号’为试材,采用营养液栽培,通过叶面喷施腐胺(putrecine,Put),研究了外源Put对盐胁迫下(75mmol·L-1NaCl)黄瓜叶片光合器官结构和功能的影响,从光合作用、叶绿体超微结构、类囊体膜脂肪酸组分、类囊体膜蛋白质组等方面,探讨外源Put调控盐胁迫下黄瓜幼苗光合器官结构和功能适应性变化的作用机制。主要结果如下：
1.叶面喷施5～15mmol·L-1Put均能缓解盐胁迫对黄瓜植株光化学效率造成的抑制,其中以8mmol·L-1Put缓解效果最好,显著提高幼苗光合色素含量,促进盐胁迫下黄瓜幼苗的生长。
2.盐胁迫下,叶面喷施8mmol·L-1Put显著提高黄瓜幼苗叶片最大光化学效率(Fv/Fm)、PSⅡ实际光化学效率(ΦPSH)和保护性热耗散(ΦNPQ)能力,降低非调节性热耗散(ΦNO),并且Put显著增强光耐受能力和电子传递能力,降低光损伤程度。说明外源Put通过增强盐胁迫下黄瓜幼苗叶片热耗散能力,减轻不可逆光抑制,进而缓解盐胁迫对黄瓜幼苗光化学效率的抑制。
3.叶面喷施Put可显著提高盐胁迫下黄瓜幼苗单位反应中心电子传递速率(ETo/RC),增加原初光化学产额(Ψo)和电子传递量子产额(φEo),而降低单位反应中心的能态淬灭(DIo/RC)、单位反应中心吸收的光能(ABS/RC)和单位反应中心用于还原QA的能量(TRo/RC),使更多的能量用于光化学淬灭。表明Put能够调节盐胁迫下黄瓜幼苗原初光化学反应过程中电子传递和能量分配,优化光合器官的结构性能(PIABs),从而维持盐胁迫下具有较高的光合作用质子驱动力(DFABs)。
4.叶面喷施Put显著降低盐胁迫下黄瓜幼苗类囊体膜十四碳烯酸、棕榈酸以及总饱和脂肪酸(SFA)的含量,提高十六碳三烯酸、亚油酸、亚麻酸以及总不饱和脂肪酸(UFA)的含量,导致UFA/SFA的比率显著增加,并且Put也降低了盐胁迫下黄瓜幼苗类囊体膜脂的氧化程度,类囊体膜上嗜锇颗粒的数量减少。这些结果表明,外源Put通过提高幼苗类囊体膜上不饱和脂肪酸组分的含量,增强膜脂的流动性,降低盐胁迫对类囊体膜的氧化破坏,维持叶绿体内基粒和基质类囊体片层的有序排列,从而提高盐胁迫下黄瓜幼苗的光化学效率。
5.利用蓝绿温和胶凝胶电泳(BN-PAGE)和SDS-尿素-PAGE电泳技术对类囊体膜复合体蛋白亚基进行分离,总共有60多个膜蛋白点通过肉眼可见。选取差异表达的34个蛋白点进行质谱分析,结果表明,盐胁迫引起幼苗类囊体膜上能量合成和PSⅡ反应中心蛋白表达下调,如ATPase CF1、ATPase、CP47、D1、Qb和PsbA等(其中D1、CP47、Qb和PsbA膜蛋白下降幅度较大),而一些膜蛋白在盐胁迫下表达上调,如CP24蛋白、D2和LHCⅡ等。编码应答膜蛋白的基因转录分析表明,盐胁迫下,除CP47、LHCⅡ、D2和Atp1基因外,其它5个候选转录子与对应的蛋白丰度表现出了一致的变化。盐胁迫下,外源Put能够不同程度地逆转盐胁迫下类囊体膜蛋白合成和转录水平的表达。
6.外源Put处理可显著提高盐胁迫下叶绿体内超氧化物歧化酶(SOD)、过氧化物酶(POD)和过氧化氢酶(CAT)的活性,提高参与叶绿体内AsA-GSH循环的过氧化物酶(APX)、谷胱甘肽还原酶(GR)、脱氢抗坏血酸还原酶(DHAR)和单脱氢抗坏血酸还原酶(MDAR)的活性,以及增加抗坏血酸(AsA)、氧化性谷胱甘肽(GSSG)、还原性谷胱甘肽(GSH)、单脱氢抗坏血酸(DAsA)的含量,减少活性氧(ROS)的含量,显著降低盐胁迫下幼苗叶绿体内Na+和C1-含量的积累。这些结果表明,Put能够缓解盐胁迫对黄瓜幼苗光合器官诱导的氧化伤害和离子毒害。
7.外源Put显著提高盐胁迫下黄瓜幼苗叶片NPQfast组分中高能态淬灭(qE),显著增加盐胁迫下幼苗叶片紫黄质(V)、单环氧玉米黄质(A)、玉米黄质(Z)和总的叶黄素库(V+A+Z)的含量,并提高DEPS的比率。表明Put通过调节盐胁迫下类囊体膜能态化和促进叶黄素循环耗散过剩的激发能。
8.外源Put处理可显著增加盐胁迫下黄瓜幼苗叶绿体内和类囊体膜上束缚态、结合态多胺(Put、Spd和Spm)的含量,尤其是类囊体膜上结合态Spd和Spm,并且降低类囊体膜上束缚态和结合态Put/Spd的比率。说明Put可通过调节光合器官上不同种类、不同形态多胺含量的变化,缓解盐胁迫对黄瓜光合器官的伤害,从而保护黄瓜幼苗光合器官结构和功能的完整性。
Salinity is an important factor affecting ecological environment in the soil that threatens agricultural production, thus it is a global research focus in recent years. At present, due to the rapid development of protected cultivation and much fertilizer used in process of cultivation, the soil secondary salinization has become one of the most severe problems in the protected cultivation. Cucumber is an economically important horticultural crop and highly sensitive to salinity. The growth and development of cucumber seedlings are inhibited when they are subjected to salinity. The photochemical efficiency of cucumber is significantly declined by salinity, which severely affects yield and quality of cucumber. Polyamines as a new plant growth regulators are low molecular weight ubiquitous nitrogenous compounds with a strong biological activity in all organisms and cells. Under environmental condition, PAs act not only as a direct protective substance, but also a signaling molecule involved in signal transduction, which is conductive to the plant resistance. At present, the view that PAs could increase the photosynthesis under stress has been recognized at home and abroad. However, the mechanism of PAs alleviating the inhibition of photochemical efficiency is still unclear.
The present study was conducted hydroponics to investigate the effects of exogenous spraying putrescine (8mM Put) on the structure and function of photo synthetic apparatus in salt-sensitive cucumber cultivar (Jinyou No.4) were exposed to NaCl stress. We discussed the interaction mechanism of adaption variation that exogenous Put regulated the changes of the structure and function of photosynthetic apparatus, chloroplast ultrastructure, thylakoid membrane fatty acid and proteome in salt-stressed cucumber plants. The main results are as follows:
1. Spayed application of5-15mM Put could alleviate the inhibition of photochemist-ry efficiency in cucumber. Among of them,8mM Put showed the best performance, which significantly enhanced photosynthetic pigment content and improved the cucumber seedlings growth.
2. Exogenous Put significantly enhanced the maximum quantum efficiency (Fv/Fm), the actual efficiency of photosystem Ⅱ (ΦPSⅡ) and protective heat dissipation (ΦNPQ) in the salt-stressed plants. But the destructive heat dissipation (ΦNO) and electron transport rate (ETR) were decreased by salinity. The result showed that exogenous Put could alleviate inhibition of photochemistry efficiency of cucumber through regulating heat dissipation capacity pathway.
3. Exogenous Put could significantly increase electron transport per active reaction center (ETo/RC), and promote the primary photochemistry (Ψo) and quantum yield for electron transport (ΨEo). However, it effectively reduced non-photochemical dissipation energy (DIo/RC), the functional size of the antenna per active reaction center (ABS/RC) and light-trapping efficiency per reaction center (TRo/RC), thus promoting total photosynthetic driving force (DFABS) and the structure performance index (PIABS).These results suggested that Put could effectively alleviate the damage of salt stress on the structure and function of photosynthetic apparatus in cucumber seedlings.
4. Foliar application of Put significantly reduced the content of tetradecane acrylic, palmitic acid and saturated fatty acids (SFA). The content of hexadecenoic acid, linoleic, linolenic and unsaturated fatty acids (UFA) and the ratio of UFA/SFA were significantly enhanced by exogenous Put treatment. The analysis of chloroplast ultrastructure showed that Put alleviated the disintegration of thylakoid grana lamellae and reduced the number of plastoglobuli in thylakoid membrane. These results indicated that Put could improve the salt tolerance of photosynthetic apparatus through enhancing the content of unsaturated fatty acid composition, thus increasing the liquidity of membrane and maintaining the ordered arrangement of grana thylakoids.
5. Blue native polyacrylamide gel electrophoresis (BN-PAGE) and SDS-urea-PAGE were used to separate the membrane proteins, and more than60membrane proteins were visible. Among of them,34protein spots were used to identify by liquid chromatography electro-spray ionization tandem mass spectrometry. Compared with the control, salt stress down-regulated the proteins expression of energy synthesis and PSⅡ reaction center in the thylakoid membrane, such as ATPase CF1, ATPase, CP47, D1, Qb and PsbA. Among of them, proteins spots of D1, CP47, Qb and PsbA had remarkable decrease. However, some membrane proteins were up-regulated by salt stress, such as CP24, D2and LHCⅡ; analysis in transcriptional level showed except the gene of CP47, LHCII, D2and Atpl, the rest of five candidate trancripts exhibited a consistent transcription accumulation changes with the corresponding protein abundance. These results suggested that Put regulated the proteins expression to varying degree in transcription and translation levels.
6. Exogenous Put significantly enhanced activities of SOD, POD, and CAT in chloroplast, and also was involved in increasing activities and content of APX, GR, DHAR, MDAR, AsA, GSSG, GSH, DAsA and AsA-GSH cycle, thus the levels of O2-and ROS production were decreased in the chloroplast of salt-stressed cucumber seedlings. In addition, Put treatment significantly decreased the accumulation of Na+and Cl-in chloroplast of cucumber seedlings exposed to salt stress. These results suggested that Put alleviated the oxidative damage and ion toxicity on photosynthetic apparatus of the salt-stressed cucumber seedlings.
7. Exogenous Put significantly improved energy-dependent quenching (qE) in NPQfast component, Put also increased the composition of xanthophyll cycle and promoted the de-epoxidation (DEPS) of the xanthophyll cycle in cucumber leaves under salt stress. The result indicated that Put dissipated the excess excitation energy through regulating the protion gradient in thylakoid membrane and promoting xanthophyll cycle.
8. Exogenous Put significantly increased free, bound and conjugated polyamines (Put, Spd and Spm) of the chloroplast and thylakoid in salt-stressed cucumber seedlings, especially the conjugated Spd and Spm. Bound and conjugated Put/Spd ratios in the thylakoids were significantly decreased by Put treatment. These results indicated that Put alleviated the salt-induced damage of photosynthetic apparatus structure though regulating levels and forms of endogenous PAs in photosynthetic apparatus.
本文以盐敏感的黄瓜品种‘津优4号’为试材,采用营养液栽培,通过叶面喷施腐胺(putrecine,Put),研究了外源Put对盐胁迫下(75mmol·L-1NaCl)黄瓜叶片光合器官结构和功能的影响,从光合作用、叶绿体超微结构、类囊体膜脂肪酸组分、类囊体膜蛋白质组等方面,探讨外源Put调控盐胁迫下黄瓜幼苗光合器官结构和功能适应性变化的作用机制。主要结果如下：
1.叶面喷施5～15mmol·L-1Put均能缓解盐胁迫对黄瓜植株光化学效率造成的抑制,其中以8mmol·L-1Put缓解效果最好,显著提高幼苗光合色素含量,促进盐胁迫下黄瓜幼苗的生长。
2.盐胁迫下,叶面喷施8mmol·L-1Put显著提高黄瓜幼苗叶片最大光化学效率(Fv/Fm)、PSⅡ实际光化学效率(ΦPSH)和保护性热耗散(ΦNPQ)能力,降低非调节性热耗散(ΦNO),并且Put显著增强光耐受能力和电子传递能力,降低光损伤程度。说明外源Put通过增强盐胁迫下黄瓜幼苗叶片热耗散能力,减轻不可逆光抑制,进而缓解盐胁迫对黄瓜幼苗光化学效率的抑制。
3.叶面喷施Put可显著提高盐胁迫下黄瓜幼苗单位反应中心电子传递速率(ETo/RC),增加原初光化学产额(Ψo)和电子传递量子产额(φEo),而降低单位反应中心的能态淬灭(DIo/RC)、单位反应中心吸收的光能(ABS/RC)和单位反应中心用于还原QA的能量(TRo/RC),使更多的能量用于光化学淬灭。表明Put能够调节盐胁迫下黄瓜幼苗原初光化学反应过程中电子传递和能量分配,优化光合器官的结构性能(PIABs),从而维持盐胁迫下具有较高的光合作用质子驱动力(DFABs)。
4.叶面喷施Put显著降低盐胁迫下黄瓜幼苗类囊体膜十四碳烯酸、棕榈酸以及总饱和脂肪酸(SFA)的含量,提高十六碳三烯酸、亚油酸、亚麻酸以及总不饱和脂肪酸(UFA)的含量,导致UFA/SFA的比率显著增加,并且Put也降低了盐胁迫下黄瓜幼苗类囊体膜脂的氧化程度,类囊体膜上嗜锇颗粒的数量减少。这些结果表明,外源Put通过提高幼苗类囊体膜上不饱和脂肪酸组分的含量,增强膜脂的流动性,降低盐胁迫对类囊体膜的氧化破坏,维持叶绿体内基粒和基质类囊体片层的有序排列,从而提高盐胁迫下黄瓜幼苗的光化学效率。
5.利用蓝绿温和胶凝胶电泳(BN-PAGE)和SDS-尿素-PAGE电泳技术对类囊体膜复合体蛋白亚基进行分离,总共有60多个膜蛋白点通过肉眼可见。选取差异表达的34个蛋白点进行质谱分析,结果表明,盐胁迫引起幼苗类囊体膜上能量合成和PSⅡ反应中心蛋白表达下调,如ATPase CF1、ATPase、CP47、D1、Qb和PsbA等(其中D1、CP47、Qb和PsbA膜蛋白下降幅度较大),而一些膜蛋白在盐胁迫下表达上调,如CP24蛋白、D2和LHCⅡ等。编码应答膜蛋白的基因转录分析表明,盐胁迫下,除CP47、LHCⅡ、D2和Atp1基因外,其它5个候选转录子与对应的蛋白丰度表现出了一致的变化。盐胁迫下,外源Put能够不同程度地逆转盐胁迫下类囊体膜蛋白合成和转录水平的表达。
6.外源Put处理可显著提高盐胁迫下叶绿体内超氧化物歧化酶(SOD)、过氧化物酶(POD)和过氧化氢酶(CAT)的活性,提高参与叶绿体内AsA-GSH循环的过氧化物酶(APX)、谷胱甘肽还原酶(GR)、脱氢抗坏血酸还原酶(DHAR)和单脱氢抗坏血酸还原酶(MDAR)的活性,以及增加抗坏血酸(AsA)、氧化性谷胱甘肽(GSSG)、还原性谷胱甘肽(GSH)、单脱氢抗坏血酸(DAsA)的含量,减少活性氧(ROS)的含量,显著降低盐胁迫下幼苗叶绿体内Na+和C1-含量的积累。这些结果表明,Put能够缓解盐胁迫对黄瓜幼苗光合器官诱导的氧化伤害和离子毒害。
7.外源Put显著提高盐胁迫下黄瓜幼苗叶片NPQfast组分中高能态淬灭(qE),显著增加盐胁迫下幼苗叶片紫黄质(V)、单环氧玉米黄质(A)、玉米黄质(Z)和总的叶黄素库(V+A+Z)的含量,并提高DEPS的比率。表明Put通过调节盐胁迫下类囊体膜能态化和促进叶黄素循环耗散过剩的激发能。
8.外源Put处理可显著增加盐胁迫下黄瓜幼苗叶绿体内和类囊体膜上束缚态、结合态多胺(Put、Spd和Spm)的含量,尤其是类囊体膜上结合态Spd和Spm,并且降低类囊体膜上束缚态和结合态Put/Spd的比率。说明Put可通过调节光合器官上不同种类、不同形态多胺含量的变化,缓解盐胁迫对黄瓜光合器官的伤害,从而保护黄瓜幼苗光合器官结构和功能的完整性。
Salinity is an important factor affecting ecological environment in the soil that threatens agricultural production, thus it is a global research focus in recent years. At present, due to the rapid development of protected cultivation and much fertilizer used in process of cultivation, the soil secondary salinization has become one of the most severe problems in the protected cultivation. Cucumber is an economically important horticultural crop and highly sensitive to salinity. The growth and development of cucumber seedlings are inhibited when they are subjected to salinity. The photochemical efficiency of cucumber is significantly declined by salinity, which severely affects yield and quality of cucumber. Polyamines as a new plant growth regulators are low molecular weight ubiquitous nitrogenous compounds with a strong biological activity in all organisms and cells. Under environmental condition, PAs act not only as a direct protective substance, but also a signaling molecule involved in signal transduction, which is conductive to the plant resistance. At present, the view that PAs could increase the photosynthesis under stress has been recognized at home and abroad. However, the mechanism of PAs alleviating the inhibition of photochemical efficiency is still unclear.
The present study was conducted hydroponics to investigate the effects of exogenous spraying putrescine (8mM Put) on the structure and function of photo synthetic apparatus in salt-sensitive cucumber cultivar (Jinyou No.4) were exposed to NaCl stress. We discussed the interaction mechanism of adaption variation that exogenous Put regulated the changes of the structure and function of photosynthetic apparatus, chloroplast ultrastructure, thylakoid membrane fatty acid and proteome in salt-stressed cucumber plants. The main results are as follows:
1. Spayed application of5-15mM Put could alleviate the inhibition of photochemist-ry efficiency in cucumber. Among of them,8mM Put showed the best performance, which significantly enhanced photosynthetic pigment content and improved the cucumber seedlings growth.
2. Exogenous Put significantly enhanced the maximum quantum efficiency (Fv/Fm), the actual efficiency of photosystem Ⅱ (ΦPSⅡ) and protective heat dissipation (ΦNPQ) in the salt-stressed plants. But the destructive heat dissipation (ΦNO) and electron transport rate (ETR) were decreased by salinity. The result showed that exogenous Put could alleviate inhibition of photochemistry efficiency of cucumber through regulating heat dissipation capacity pathway.
3. Exogenous Put could significantly increase electron transport per active reaction center (ETo/RC), and promote the primary photochemistry (Ψo) and quantum yield for electron transport (ΨEo). However, it effectively reduced non-photochemical dissipation energy (DIo/RC), the functional size of the antenna per active reaction center (ABS/RC) and light-trapping efficiency per reaction center (TRo/RC), thus promoting total photosynthetic driving force (DFABS) and the structure performance index (PIABS).These results suggested that Put could effectively alleviate the damage of salt stress on the structure and function of photosynthetic apparatus in cucumber seedlings.
4. Foliar application of Put significantly reduced the content of tetradecane acrylic, palmitic acid and saturated fatty acids (SFA). The content of hexadecenoic acid, linoleic, linolenic and unsaturated fatty acids (UFA) and the ratio of UFA/SFA were significantly enhanced by exogenous Put treatment. The analysis of chloroplast ultrastructure showed that Put alleviated the disintegration of thylakoid grana lamellae and reduced the number of plastoglobuli in thylakoid membrane. These results indicated that Put could improve the salt tolerance of photosynthetic apparatus through enhancing the content of unsaturated fatty acid composition, thus increasing the liquidity of membrane and maintaining the ordered arrangement of grana thylakoids.
5. Blue native polyacrylamide gel electrophoresis (BN-PAGE) and SDS-urea-PAGE were used to separate the membrane proteins, and more than60membrane proteins were visible. Among of them,34protein spots were used to identify by liquid chromatography electro-spray ionization tandem mass spectrometry. Compared with the control, salt stress down-regulated the proteins expression of energy synthesis and PSⅡ reaction center in the thylakoid membrane, such as ATPase CF1, ATPase, CP47, D1, Qb and PsbA. Among of them, proteins spots of D1, CP47, Qb and PsbA had remarkable decrease. However, some membrane proteins were up-regulated by salt stress, such as CP24, D2and LHCⅡ; analysis in transcriptional level showed except the gene of CP47, LHCII, D2and Atpl, the rest of five candidate trancripts exhibited a consistent transcription accumulation changes with the corresponding protein abundance. These results suggested that Put regulated the proteins expression to varying degree in transcription and translation levels.
6. Exogenous Put significantly enhanced activities of SOD, POD, and CAT in chloroplast, and also was involved in increasing activities and content of APX, GR, DHAR, MDAR, AsA, GSSG, GSH, DAsA and AsA-GSH cycle, thus the levels of O2-and ROS production were decreased in the chloroplast of salt-stressed cucumber seedlings. In addition, Put treatment significantly decreased the accumulation of Na+and Cl-in chloroplast of cucumber seedlings exposed to salt stress. These results suggested that Put alleviated the oxidative damage and ion toxicity on photosynthetic apparatus of the salt-stressed cucumber seedlings.
7. Exogenous Put significantly improved energy-dependent quenching (qE) in NPQfast component, Put also increased the composition of xanthophyll cycle and promoted the de-epoxidation (DEPS) of the xanthophyll cycle in cucumber leaves under salt stress. The result indicated that Put dissipated the excess excitation energy through regulating the protion gradient in thylakoid membrane and promoting xanthophyll cycle.
8. Exogenous Put significantly increased free, bound and conjugated polyamines (Put, Spd and Spm) of the chloroplast and thylakoid in salt-stressed cucumber seedlings, especially the conjugated Spd and Spm. Bound and conjugated Put/Spd ratios in the thylakoids were significantly decreased by Put treatment. These results indicated that Put alleviated the salt-induced damage of photosynthetic apparatus structure though regulating levels and forms of endogenous PAs in photosynthetic apparatus.
引文
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