外源亚精胺缓解黄瓜幼苗高温胁迫伤害的生理调节机制和蛋白质组学研究
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摘要
高温胁迫对农业生产的威胁是一个全球性的热点问题,严重影响着作物的生育和产量。黄瓜(Cucumis sativus L.)是世界性的重要蔬菜作物,也是我国设施栽培的主要蔬菜种类之一。然而,在我国大部分地区的保护设施中,正午40℃以上的高温经常出现,高温热害已经成为黄瓜夏秋露地与保护地栽培的主要限制因子。多胺(Polyamines, PAs)是生物代谢过程中产生的一类具有生物活性的低分子量脂肪族含氮碱,广泛作用于植物生长、形态建成、衰老和对逆境胁迫的响应。多胺的种类主要包括二胺类的腐胺(Putrescine, Put)、三胺类的亚精胺(Spermidine, Spd)和四胺类的精胺(Spermine, Spm)。近年来,通过使用外源多胺类物质来调节和介导植物各种胁迫耐性的研究越来越多。然而,关于多胺调节蔬菜作物高温胁迫的生理研究比较少见,尤其是蛋白质组学方面的研究尚为空白。
本研究以黄瓜品种‘津春4号’为试材,在人工气候箱内,采用营养钵内石英砂浇灌营养液栽培的方式,通过叶面喷施外源1mM Spd,测定了高温胁迫(42℃/32℃)下黄瓜植株生长、光合与荧光特性、叶绿体超微结构、膜脂过氧化程度、活性氧清除酶活性和同工酶表达、抗坏血酸-谷胱甘肽循环、氮素吸收代谢等方面的变化,研究了黄瓜叶片可溶性蛋白变化和蛋白质组功能、mRNA转录水平的变化,探讨了外源Spd提高黄瓜植株耐热性的生理和分子生物学机制。主要研究结果如下：
1.外源Spd对高温胁迫下黄瓜幼苗生长和内源多胺含量的影响：高温胁迫下,黄瓜幼苗生长受到明显抑制,株高、茎粗、地上部干鲜重、地下部干鲜重及主要功能叶的叶面积均显著降低,外源Spd处理可明显缓解高温胁迫对黄瓜幼苗生长的抑制,提高植株生物量的积累。高温胁迫下,黄瓜幼苗叶片中游离态、结合态和束缚态Put含量显著降低,而游离态、结合态和束缚态Spd和Spm含量显著升高。从多胺种类上来看,黄瓜幼苗体内三种形态Put均向Spd和Spm的转化可能是黄瓜幼苗(至少是该品种)对高温胁迫的一种适应性反应。喷施外源Spd处理促进叶片中Put和Spd含量的升高,而Spm含量略有下降,由于Put是Spd的上游产物而Spm是Spd的下游产物,外源Spd的作用即趋向于维持高水平的内源Spd含量。
2.外源Spd保护高温胁迫下黄瓜幼苗的光合能力：与常温对照相比,高温胁迫下叶绿素含量和净光合速率显著下降,气孔导度和蒸腾速率升高,PS Ⅱ潜在最大光化学效率及实际光化学效率亦明显下降；高温胁迫下施用外源Spd有助于提高叶片光合色素的含量,维持较高的净光合速率及PS Ⅱ光化学效率。单纯高温胁迫下,叶绿体内淀粉粒膨大并大量积累、基粒片层受到挤压且数目相对减少,嗜锇体大量出现；高温胁迫下喷施外源Spd,叶绿体超微结构几乎未受到影响。Spd对叶绿体结构与功能的维持和保护,可能是其改善黄瓜幼苗在高温胁迫下光合能力的主要原因,由此而增强植株对高温逆境的适应性。外源Spd可有效抑制高温胁迫下淀粉的水解,使糖分趋于向合成方向,积累更多的干物质。
3.外源Spd增强高温胁迫下黄瓜幼苗的抗氧化能力：高温胁迫下,黄瓜幼苗叶片膜脂过氧化程度显著加剧,表现为叶片相对电导率、MDA含量及脂氧合酶(LOX)活性以及ROS水平(包括O2和H202含量)均显著上升；而外源Spd处理可明显抑制高温胁迫下幼苗叶片的膜脂过氧化损伤,降低ROS水平,减少电解质渗漏和MDA积累。高温胁迫下,SOD活性大幅下降,POD和APX活性先升高后降低,CAT活性先降低后升高,这些酶的同工酶也发生明显的变化；外源Spd显著增强了高温胁迫下SOD活性,POD、CAT和APX活性也有不同程度的提高,除对POD同工酶影响较小外,外源Spd明显促进了其他保护酶同工酶的表达。AsA-GSH循环中,高温胁迫诱导MDAR.DHAR和GR活性升高,还原型抗氧化剂AsA和GSH含量上升且氧化还原比例发生变化；外源Spd处理进一步提高MDAR.DHAR和GR活性,在促进还原型抗氧化剂AsA和GSH绝对含量升高的同时,还提高了还原型抗氧化剂所占比例(AsA/DHA、GSH/GSSG)。黄瓜幼苗在高温胁迫下启动自身的抗氧化系统以抵御高温造成的氧化伤害,但随着胁迫时间的延长,这种抵御逐渐减弱,而外源Spd能显著降低高温胁迫造成的膜脂过氧化伤害,提高抗氧化酶活性并增强同工酶表达,活化AsA-GSH循环,促进了黄瓜幼苗整体抗氧化能力的提高。
4.外源Spd对高温胁迫下黄瓜幼苗氮素和其他代谢的影响：高温胁迫下,幼苗根系中N03--N含量升高但随胁迫处理时间的延长向地上部运输受阻,根系中硝酸还原酶(NR)钝化,叶片中NR活性升高,根系和叶片中NH4+-N含量大幅上升；外源Spd能有效调节高温胁迫下氮素代谢的平衡,促硝抑铵,提高NR活性。脯氨酸是一种重要的含氮化合物,逆境条件下较高的脯氨酸水平可增强植株的渗透调节能力,有助于维持植株体内的水分平衡。高温胁迫下,黄瓜幼苗叶片内脯氨酸含量升高,外源Spd进一步促进其含量的升高,从而为黄瓜幼苗在高温胁迫下生长发育提供额外的渗透调节能力。高温胁迫下,质膜蛋白含量降低而液泡膜蛋白含量升高,质子泵活性略有升高；外源Spd可进一步提高高温胁迫下黄瓜幼苗叶片质膜和液泡膜H+-ATPase,而液泡膜H+-PPase活性略有下降。外源Spd促进H+-ATPase的活性,从而稳定膜结构,建立跨膜质子推动力△pH,促进ATP的产生和维持细胞质酸碱平衡,缓解了高温胁迫对黄瓜幼苗生长的抑制。
5.外源Spdd对高温胁迫下黄瓜幼苗叶片蛋白质组和基因表达的影响：高温胁迫初时,幼苗叶片可溶性蛋白含量升高,随胁迫时间延长至5d后,叶片可溶性蛋白含量开始下降,外源Spd可显著提高叶片可溶性蛋白的含量。利用双向电泳(2-DE)和质谱分析(LC-ESI-MS/MS)的技术,比较常温对照和高温胁迫及外源Spd处理的幼苗叶片2-DE图谱,共发现62个差异表达蛋白点,其中有60个蛋白点成功得以MS鉴定。经功能分类后显示,25个蛋白点与光合作用有关,16个蛋白点涉及能量与物质代谢,6个蛋白点为分子伴侣,6个蛋白点与胁迫防御有关,7个蛋白点与蛋白质或核酸的生物合成相关,另有2个蛋白点因MS鉴定得分较低或EST功能尚不明确而被归为功能未知蛋白。主要差异蛋白有Rubisco大/小亚基、Rubisco活化酶(RCA)、转酮醇酶(TK)、磷酸核酮糖激酶(PRK)、热激蛋白70(HSP7)、分子伴侣60(CPN60)、Cu/Zn-SOD、类胡萝卜素相关蛋白、蛋白翻译延长因子(EF-Ts和EF-G)等。高温胁迫对光合作用、能量和物质代谢相关蛋白的影响最为明显,而外源Spd处理在蛋白质水平上表现出积极的保护作用,尤其是显著提高了部分高温下调蛋白(如Rubisco大/小亚基和Cu/Zn-SOD)的表达。光合相关基因(RbcL、RbcS、RCA、OEC23和OEC33等)、抗氧化相关基因(SOD、POD和Car等)和分子伴侣(Hsp70、Cpn60和Hsp20)都在nRNA水平对高温胁迫做出明显反应；外源Spd处理对部分基因的表达表现出明显的调控作用。除PRK、CPN60和sHSP外,大多数重要的功能蛋白受高温影响和受外源Spd诱导的mRNA转录特性与蛋白积累特性相一致。
Heat stress due to increased temperature is an agricultural problem in many areas in the world, which seriously affects plant growth and development and may lead to a drastic reduction in economic yield. Cucumber (Cucumis sativus L.) is one of the important vegetable crops worldwide, and also is the main type of vegetables cultivated in protected condition in China. However, in most parts of our protection facilities, the midday temperatures often above40℃, heat injury has become a main limiting factor in summer-autumn cucumber cultivation in open and protected field. Polyamines (PAs) are low molecular weight aliphatic amines with biological activity produced during metabolism, necessary for normal cell growth, morphogenesis, aging and stress response, mainly including putrescine (Put), spermidine (Spd) and spermine (Spm). In recent years, growing interest has focused on the subject that using exogenous PAs to regulate and mediate a variety of stress tolerance of plants. The information between PAs and high temperature stress in plant physiology is very limited; especially proteomics study is still blank.
In the present study, the more heat-resistant cucumber cultivar cv.'Jinchun No.4'is used in climate chambers and hydroponics. By using exogenous Spd (1mM) foliar spray, we determined the effects of high temperature stress (42℃/32℃) on the plant growth, photosynthesis and chlorophyll fluorescence, chloroplast ultrastructure, membrane lipid peroxidation, antioxidant enzymes activity and isozymes, ascorbate-glutathione cycle, nitrogen metabolism and so on. We also investigated on changes of soluble protein, proteomics and mRNA transcription level in leaves of cucumber seedlings to explore the molecular mechanism why exogenous Spd increased the heat resistance of cucumber seedlings. The main results are as follows:
1. Effects of exogenous Spd on growth and endogenous poyamines contents of cucumber seedlings under high temperature stress:under high temperature stress, seedling growth was inhibited, plant height, stem diameter, fresh and dry weight, and leaf area are significantly decreased, exogenous Spd could availably alleviate the heat damage on growth, increase plant biomass accumulation. Upon high temperature stress, the content of free, soluble conjugated and insoluble bound Put was significantly decreased, and the the content of free, soluble conjugated and insoluble bound Spd and Spm were significantly increased by high temperature stress. From the species of PAs, the conversion from Put to Spd and Spm was likely a kind of adaptive response to heat stress for cucumber seedlings. Exogenous Spd promoted the contents of Put and Spd, but a slight inhibitory effect on Spm content. That is means higher level of Spd, because Put is the precursor of Spd and Spm is the downstream product of Spd. Exogenous Spd promoted high levels of endogenous Spd may contribute to enhanced heat tolerance of cucumber seedlings.
2. Exogenous Spd increased the photosynthetic characteristics of cucumber seedlings under high temperature stress:Compared with normal temperature, pigment contents and net photosynthetic rate were decline, stomatal conductance and transpiration rate were increased under high temperature, PS Ⅱ photochemical efficiency was also decreased significantly; application of exogenous Spd under high temperature was helpful to improve the pigment contents, maintain a higher photosynthetic rate and photochemical efficiency. Without application of Spd, high temperature stress induced the accumulation of swollen starch grains in chloroplasts, the extrusion and reduction of grana lamellae, and the ubiquitous appearance of osmiophilic granules. However, the chloroplast ultrastructure of seedlings treated with spermidine was only very mildly affected by high temperatures. Spd protects the organelle structure and photochemical activity of chloroplasts, which is fairly important in the adaptation of cucumber seedlings against high temperature stress. Exogenous Spd also effectively inhibited the hydrolysis of starch under high temperature stress, so the sugars tend to synthesis and accumulated more dry matter.
3-Exogenous Spd improved the antioxidant capacity for ROS cleaning in leaves of cucumber seedlings under high temperature stress:Under high temperature stress, membrane lipid peroxidation was significantly increased in leaves of cucumber seedlings, showing the relative conductivity, MDA content and lipoxygenase (LOX) activity were significantly increased, ROS levels (including O2production rate and H2O2content) were remarkably raised. Exogenous Spd treatment significantly inhibited the oxidative damage of membrane lipid in leaves under high temperature stress. Expose to high temperature, SOD activity decreased, POD and APX activity first increased and then decreased, CAT activity first decreased and then increased, the isozymes of these enzymes also changed accordingly; Exogenous Spd treatment significantly promoted the activities of SOD, and the POD, CAT and APX activities were also enhanced to varying degrees. Apart from Spd had little effect on POD isozymes, the expression of other kinds of protective isozymes were significantly enhanced by Spd. In AsA-GSH cycle, MDAR, DHAR and GR activity, and reduced form contents of AsA and GSH were increased under high temperature stress. Exogenous Spd treatment significantly promoted the activities of MDAR, DHAR and GR, and the contents of AsA and GSH under high temperature stress. In particular, the ratio of AsA/GSH and GSH/GSSG were also further increased. Cucumber seedlings have their own antioxidant system against oxidative stress caused by high temperatures, this resistance gradually weakened with the extension of stress time, but exogenous Spd could significantly reduce the lipid peroxidation caused by heat stress, improve antioxidant enzyme activity and enhance isozymes expression, activate the AsA-GSH cycle, so the total antioxidant capacity of cucumber seedlings for was totally improved.
4-Effects of exogenous Spd on nitrogen and other metabolism in leaves of cucumber seedlings under high temperature stress:Under high temperature stress, the nitrate content in roots was increased but transport to leaves was blocked, nitrate reductase (NR) in roots was deactivated, the ammonium content in both roots and leaves was largely increased. The exogenous Spd upon high temperature were helpful to regulate the balance of nitrogen metabolism, promoting nitrate, suppressing ammonium and activating the NR. Spd could availably modulate nitrogen metabolism in cucumber seedlings under high temperature stress. Proline is also a kind of important nitrogen-containing compound, the higher level of proline can enhance the ability of osmotic adjustment to maintain the water balance in plants. Proline content in leaves was increased by high temperature treatment, exogenous Spd promoted the enhancement. High temperature induced plasma membrane protein content decreased and tonoplast membrane protein content increased, proton pumps activity were enhanced; exogenous Spd could further improve activity of H+-ATPase but not H+-PPase to stabilize the membrane structure and establish the transmembrane proton driver△pH, promote the generation of ATP and maintenance of cytoplasmic acid-base balance.
5. Effects of exogenous Spd on proteomics changes and mRNA accumulation patterns in leaves of cucumber seedlings under high temperature stress:At the beginning of heat stress, the soluble protein content in leaves was increased, but with the stress time extended to5days, the soluble protein content started to decline, exogenous Spd increased soluble protein. By using the two-dimensional electrophoresis (2-DE) and mass spectrometry (LC-ESI-MS/MS) technology, compared the2-DE protein profiles of treatments of high temperature or exogenous Spd with control, we found62differentially expressed proteins,60spots were successfully been identified by MS. Functional classification revealed that25spots related to photosynthesis,16spots involved in energy and material metabolism,6spots for the molecular chaperone protein,6spots in defense and stress respond and7spots related to protein or nucleic acid biosynthesis, and another two spots identified by MS with too lower scores or EST function unknown protein. The main difference proteins such as Rubisco large/small subunit, Rubisco activase (RCA), Transketolase (TK), phosphate ribulose kinase (PRK), heat shock protein70(HSP70), chaperonin60(CPN60), Cu/Zn-SOD, carotenoids associated protein, protein translation elongation factor (EF-Ts and EF-G) and so on. These proteins related to photosynthesis, energy and metabolism were most seriously affected by high temperature stress. Exogenous Spd was helpful to inhibit parts of the down-regulated proteins under high temperature conditions, showing a positive protective role at protein level. Photosynthesis-related genes (RbcL, RbcS, RCA, OEC23and OEC3, etc.), antioxidant-related genes (SOD, POD and Car, etc.), molecular chaperones (Hsp70, Cpn60, and Hsp20) were prominently response to high temperature stress at mRNA level; exogenous Spd showed significant regulatory role on the expression of some genes. The mRNA transcriptional accumulation patterns of several important high-abundance proteins under high temperatures and/or treated with exogenous Spd were consistent with the proteomics accumulation patterns.
本研究以黄瓜品种‘津春4号’为试材,在人工气候箱内,采用营养钵内石英砂浇灌营养液栽培的方式,通过叶面喷施外源1mM Spd,测定了高温胁迫(42℃/32℃)下黄瓜植株生长、光合与荧光特性、叶绿体超微结构、膜脂过氧化程度、活性氧清除酶活性和同工酶表达、抗坏血酸-谷胱甘肽循环、氮素吸收代谢等方面的变化,研究了黄瓜叶片可溶性蛋白变化和蛋白质组功能、mRNA转录水平的变化,探讨了外源Spd提高黄瓜植株耐热性的生理和分子生物学机制。主要研究结果如下：
1.外源Spd对高温胁迫下黄瓜幼苗生长和内源多胺含量的影响：高温胁迫下,黄瓜幼苗生长受到明显抑制,株高、茎粗、地上部干鲜重、地下部干鲜重及主要功能叶的叶面积均显著降低,外源Spd处理可明显缓解高温胁迫对黄瓜幼苗生长的抑制,提高植株生物量的积累。高温胁迫下,黄瓜幼苗叶片中游离态、结合态和束缚态Put含量显著降低,而游离态、结合态和束缚态Spd和Spm含量显著升高。从多胺种类上来看,黄瓜幼苗体内三种形态Put均向Spd和Spm的转化可能是黄瓜幼苗(至少是该品种)对高温胁迫的一种适应性反应。喷施外源Spd处理促进叶片中Put和Spd含量的升高,而Spm含量略有下降,由于Put是Spd的上游产物而Spm是Spd的下游产物,外源Spd的作用即趋向于维持高水平的内源Spd含量。
2.外源Spd保护高温胁迫下黄瓜幼苗的光合能力：与常温对照相比,高温胁迫下叶绿素含量和净光合速率显著下降,气孔导度和蒸腾速率升高,PS Ⅱ潜在最大光化学效率及实际光化学效率亦明显下降；高温胁迫下施用外源Spd有助于提高叶片光合色素的含量,维持较高的净光合速率及PS Ⅱ光化学效率。单纯高温胁迫下,叶绿体内淀粉粒膨大并大量积累、基粒片层受到挤压且数目相对减少,嗜锇体大量出现；高温胁迫下喷施外源Spd,叶绿体超微结构几乎未受到影响。Spd对叶绿体结构与功能的维持和保护,可能是其改善黄瓜幼苗在高温胁迫下光合能力的主要原因,由此而增强植株对高温逆境的适应性。外源Spd可有效抑制高温胁迫下淀粉的水解,使糖分趋于向合成方向,积累更多的干物质。
3.外源Spd增强高温胁迫下黄瓜幼苗的抗氧化能力：高温胁迫下,黄瓜幼苗叶片膜脂过氧化程度显著加剧,表现为叶片相对电导率、MDA含量及脂氧合酶(LOX)活性以及ROS水平(包括O2和H202含量)均显著上升；而外源Spd处理可明显抑制高温胁迫下幼苗叶片的膜脂过氧化损伤,降低ROS水平,减少电解质渗漏和MDA积累。高温胁迫下,SOD活性大幅下降,POD和APX活性先升高后降低,CAT活性先降低后升高,这些酶的同工酶也发生明显的变化；外源Spd显著增强了高温胁迫下SOD活性,POD、CAT和APX活性也有不同程度的提高,除对POD同工酶影响较小外,外源Spd明显促进了其他保护酶同工酶的表达。AsA-GSH循环中,高温胁迫诱导MDAR.DHAR和GR活性升高,还原型抗氧化剂AsA和GSH含量上升且氧化还原比例发生变化；外源Spd处理进一步提高MDAR.DHAR和GR活性,在促进还原型抗氧化剂AsA和GSH绝对含量升高的同时,还提高了还原型抗氧化剂所占比例(AsA/DHA、GSH/GSSG)。黄瓜幼苗在高温胁迫下启动自身的抗氧化系统以抵御高温造成的氧化伤害,但随着胁迫时间的延长,这种抵御逐渐减弱,而外源Spd能显著降低高温胁迫造成的膜脂过氧化伤害,提高抗氧化酶活性并增强同工酶表达,活化AsA-GSH循环,促进了黄瓜幼苗整体抗氧化能力的提高。
4.外源Spd对高温胁迫下黄瓜幼苗氮素和其他代谢的影响：高温胁迫下,幼苗根系中N03--N含量升高但随胁迫处理时间的延长向地上部运输受阻,根系中硝酸还原酶(NR)钝化,叶片中NR活性升高,根系和叶片中NH4+-N含量大幅上升；外源Spd能有效调节高温胁迫下氮素代谢的平衡,促硝抑铵,提高NR活性。脯氨酸是一种重要的含氮化合物,逆境条件下较高的脯氨酸水平可增强植株的渗透调节能力,有助于维持植株体内的水分平衡。高温胁迫下,黄瓜幼苗叶片内脯氨酸含量升高,外源Spd进一步促进其含量的升高,从而为黄瓜幼苗在高温胁迫下生长发育提供额外的渗透调节能力。高温胁迫下,质膜蛋白含量降低而液泡膜蛋白含量升高,质子泵活性略有升高；外源Spd可进一步提高高温胁迫下黄瓜幼苗叶片质膜和液泡膜H+-ATPase,而液泡膜H+-PPase活性略有下降。外源Spd促进H+-ATPase的活性,从而稳定膜结构,建立跨膜质子推动力△pH,促进ATP的产生和维持细胞质酸碱平衡,缓解了高温胁迫对黄瓜幼苗生长的抑制。
5.外源Spdd对高温胁迫下黄瓜幼苗叶片蛋白质组和基因表达的影响：高温胁迫初时,幼苗叶片可溶性蛋白含量升高,随胁迫时间延长至5d后,叶片可溶性蛋白含量开始下降,外源Spd可显著提高叶片可溶性蛋白的含量。利用双向电泳(2-DE)和质谱分析(LC-ESI-MS/MS)的技术,比较常温对照和高温胁迫及外源Spd处理的幼苗叶片2-DE图谱,共发现62个差异表达蛋白点,其中有60个蛋白点成功得以MS鉴定。经功能分类后显示,25个蛋白点与光合作用有关,16个蛋白点涉及能量与物质代谢,6个蛋白点为分子伴侣,6个蛋白点与胁迫防御有关,7个蛋白点与蛋白质或核酸的生物合成相关,另有2个蛋白点因MS鉴定得分较低或EST功能尚不明确而被归为功能未知蛋白。主要差异蛋白有Rubisco大/小亚基、Rubisco活化酶(RCA)、转酮醇酶(TK)、磷酸核酮糖激酶(PRK)、热激蛋白70(HSP7)、分子伴侣60(CPN60)、Cu/Zn-SOD、类胡萝卜素相关蛋白、蛋白翻译延长因子(EF-Ts和EF-G)等。高温胁迫对光合作用、能量和物质代谢相关蛋白的影响最为明显,而外源Spd处理在蛋白质水平上表现出积极的保护作用,尤其是显著提高了部分高温下调蛋白(如Rubisco大/小亚基和Cu/Zn-SOD)的表达。光合相关基因(RbcL、RbcS、RCA、OEC23和OEC33等)、抗氧化相关基因(SOD、POD和Car等)和分子伴侣(Hsp70、Cpn60和Hsp20)都在nRNA水平对高温胁迫做出明显反应；外源Spd处理对部分基因的表达表现出明显的调控作用。除PRK、CPN60和sHSP外,大多数重要的功能蛋白受高温影响和受外源Spd诱导的mRNA转录特性与蛋白积累特性相一致。
Heat stress due to increased temperature is an agricultural problem in many areas in the world, which seriously affects plant growth and development and may lead to a drastic reduction in economic yield. Cucumber (Cucumis sativus L.) is one of the important vegetable crops worldwide, and also is the main type of vegetables cultivated in protected condition in China. However, in most parts of our protection facilities, the midday temperatures often above40℃, heat injury has become a main limiting factor in summer-autumn cucumber cultivation in open and protected field. Polyamines (PAs) are low molecular weight aliphatic amines with biological activity produced during metabolism, necessary for normal cell growth, morphogenesis, aging and stress response, mainly including putrescine (Put), spermidine (Spd) and spermine (Spm). In recent years, growing interest has focused on the subject that using exogenous PAs to regulate and mediate a variety of stress tolerance of plants. The information between PAs and high temperature stress in plant physiology is very limited; especially proteomics study is still blank.
In the present study, the more heat-resistant cucumber cultivar cv.'Jinchun No.4'is used in climate chambers and hydroponics. By using exogenous Spd (1mM) foliar spray, we determined the effects of high temperature stress (42℃/32℃) on the plant growth, photosynthesis and chlorophyll fluorescence, chloroplast ultrastructure, membrane lipid peroxidation, antioxidant enzymes activity and isozymes, ascorbate-glutathione cycle, nitrogen metabolism and so on. We also investigated on changes of soluble protein, proteomics and mRNA transcription level in leaves of cucumber seedlings to explore the molecular mechanism why exogenous Spd increased the heat resistance of cucumber seedlings. The main results are as follows:
1. Effects of exogenous Spd on growth and endogenous poyamines contents of cucumber seedlings under high temperature stress:under high temperature stress, seedling growth was inhibited, plant height, stem diameter, fresh and dry weight, and leaf area are significantly decreased, exogenous Spd could availably alleviate the heat damage on growth, increase plant biomass accumulation. Upon high temperature stress, the content of free, soluble conjugated and insoluble bound Put was significantly decreased, and the the content of free, soluble conjugated and insoluble bound Spd and Spm were significantly increased by high temperature stress. From the species of PAs, the conversion from Put to Spd and Spm was likely a kind of adaptive response to heat stress for cucumber seedlings. Exogenous Spd promoted the contents of Put and Spd, but a slight inhibitory effect on Spm content. That is means higher level of Spd, because Put is the precursor of Spd and Spm is the downstream product of Spd. Exogenous Spd promoted high levels of endogenous Spd may contribute to enhanced heat tolerance of cucumber seedlings.
2. Exogenous Spd increased the photosynthetic characteristics of cucumber seedlings under high temperature stress:Compared with normal temperature, pigment contents and net photosynthetic rate were decline, stomatal conductance and transpiration rate were increased under high temperature, PS Ⅱ photochemical efficiency was also decreased significantly; application of exogenous Spd under high temperature was helpful to improve the pigment contents, maintain a higher photosynthetic rate and photochemical efficiency. Without application of Spd, high temperature stress induced the accumulation of swollen starch grains in chloroplasts, the extrusion and reduction of grana lamellae, and the ubiquitous appearance of osmiophilic granules. However, the chloroplast ultrastructure of seedlings treated with spermidine was only very mildly affected by high temperatures. Spd protects the organelle structure and photochemical activity of chloroplasts, which is fairly important in the adaptation of cucumber seedlings against high temperature stress. Exogenous Spd also effectively inhibited the hydrolysis of starch under high temperature stress, so the sugars tend to synthesis and accumulated more dry matter.
3-Exogenous Spd improved the antioxidant capacity for ROS cleaning in leaves of cucumber seedlings under high temperature stress:Under high temperature stress, membrane lipid peroxidation was significantly increased in leaves of cucumber seedlings, showing the relative conductivity, MDA content and lipoxygenase (LOX) activity were significantly increased, ROS levels (including O2production rate and H2O2content) were remarkably raised. Exogenous Spd treatment significantly inhibited the oxidative damage of membrane lipid in leaves under high temperature stress. Expose to high temperature, SOD activity decreased, POD and APX activity first increased and then decreased, CAT activity first decreased and then increased, the isozymes of these enzymes also changed accordingly; Exogenous Spd treatment significantly promoted the activities of SOD, and the POD, CAT and APX activities were also enhanced to varying degrees. Apart from Spd had little effect on POD isozymes, the expression of other kinds of protective isozymes were significantly enhanced by Spd. In AsA-GSH cycle, MDAR, DHAR and GR activity, and reduced form contents of AsA and GSH were increased under high temperature stress. Exogenous Spd treatment significantly promoted the activities of MDAR, DHAR and GR, and the contents of AsA and GSH under high temperature stress. In particular, the ratio of AsA/GSH and GSH/GSSG were also further increased. Cucumber seedlings have their own antioxidant system against oxidative stress caused by high temperatures, this resistance gradually weakened with the extension of stress time, but exogenous Spd could significantly reduce the lipid peroxidation caused by heat stress, improve antioxidant enzyme activity and enhance isozymes expression, activate the AsA-GSH cycle, so the total antioxidant capacity of cucumber seedlings for was totally improved.
4-Effects of exogenous Spd on nitrogen and other metabolism in leaves of cucumber seedlings under high temperature stress:Under high temperature stress, the nitrate content in roots was increased but transport to leaves was blocked, nitrate reductase (NR) in roots was deactivated, the ammonium content in both roots and leaves was largely increased. The exogenous Spd upon high temperature were helpful to regulate the balance of nitrogen metabolism, promoting nitrate, suppressing ammonium and activating the NR. Spd could availably modulate nitrogen metabolism in cucumber seedlings under high temperature stress. Proline is also a kind of important nitrogen-containing compound, the higher level of proline can enhance the ability of osmotic adjustment to maintain the water balance in plants. Proline content in leaves was increased by high temperature treatment, exogenous Spd promoted the enhancement. High temperature induced plasma membrane protein content decreased and tonoplast membrane protein content increased, proton pumps activity were enhanced; exogenous Spd could further improve activity of H+-ATPase but not H+-PPase to stabilize the membrane structure and establish the transmembrane proton driver△pH, promote the generation of ATP and maintenance of cytoplasmic acid-base balance.
5. Effects of exogenous Spd on proteomics changes and mRNA accumulation patterns in leaves of cucumber seedlings under high temperature stress:At the beginning of heat stress, the soluble protein content in leaves was increased, but with the stress time extended to5days, the soluble protein content started to decline, exogenous Spd increased soluble protein. By using the two-dimensional electrophoresis (2-DE) and mass spectrometry (LC-ESI-MS/MS) technology, compared the2-DE protein profiles of treatments of high temperature or exogenous Spd with control, we found62differentially expressed proteins,60spots were successfully been identified by MS. Functional classification revealed that25spots related to photosynthesis,16spots involved in energy and material metabolism,6spots for the molecular chaperone protein,6spots in defense and stress respond and7spots related to protein or nucleic acid biosynthesis, and another two spots identified by MS with too lower scores or EST function unknown protein. The main difference proteins such as Rubisco large/small subunit, Rubisco activase (RCA), Transketolase (TK), phosphate ribulose kinase (PRK), heat shock protein70(HSP70), chaperonin60(CPN60), Cu/Zn-SOD, carotenoids associated protein, protein translation elongation factor (EF-Ts and EF-G) and so on. These proteins related to photosynthesis, energy and metabolism were most seriously affected by high temperature stress. Exogenous Spd was helpful to inhibit parts of the down-regulated proteins under high temperature conditions, showing a positive protective role at protein level. Photosynthesis-related genes (RbcL, RbcS, RCA, OEC23and OEC3, etc.), antioxidant-related genes (SOD, POD and Car, etc.), molecular chaperones (Hsp70, Cpn60, and Hsp20) were prominently response to high temperature stress at mRNA level; exogenous Spd showed significant regulatory role on the expression of some genes. The mRNA transcriptional accumulation patterns of several important high-abundance proteins under high temperatures and/or treated with exogenous Spd were consistent with the proteomics accumulation patterns.
引文
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