C1化合物影响拟南芥和烟草生长的生理基础和分子机理研究
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摘要
甲醇(CH30H)、甲醛(HCHO)和甲酸(HCOOH)的代谢是高等植物的C1代谢网络中重要的组成部分。大量研究结果显示外源性施用CH30H能促进多种植物的生长,但这种刺激生长的效果受到多种外界因素的影响。作为CH30H代谢的下游产物,HCHO和HCOOH对植物均有毒害作用,并且HCHO的毒性尤为强烈。本论文首先采用叶片喷洒的方式,向盆栽拟南芥分别施用这三种C1化合物,初步探索三者对植物的生长表型、生理生化特性以及胁迫应答、C1代谢、光合作用相关基因表达的影响。HCHO作为普遍存在的环境污染物,其致癌性和致畸性已引起世界的广泛关注,在医学领域对于HCHO的毒性机理也展开了广泛的研究,但目前有关HCHO对于植物毒性机理的研究还很少,也尚未见到在全基因组水平上对于高等植物HCHO应答基因进行鉴定的相关报道。模式植物拟南芥和烟草是植物学领域两种应用最广泛的研究材料,本实验室之前的研究显示二者对于HCHO的耐受性以及代谢途径均有显著的差异。基于此,本研究分别构建HCHO胁迫拟南芥和烟草的反向抑制性消减杂交(SSH) cDNA文库,结合HCHO胁迫下拟南芥cDNA芯片分析,分别对两种植物中潜在的HCHO胁迫响应基因进行分离鉴定,以期在转录水平上阐述HCHO对拟南芥和烟草的毒性机理及其抑制两种模式植物生长机制的相同点和不同点,为提高植物HCHO抗性的基因工程提供新的侯选基因。尽管已有的一些研究提出CH30H在植物体内的可能代谢走向和机制,但目前的研究结果仍然没有归纳出CH30H在植物中的具体代谢途径。13C-NMR技术是研究代谢途径的一个强有力的工具之一,本研究使用13CH3OH标记处理拟南芥和烟草获得其13C-NMR代谢谱,对拟南芥和烟草中的CH30H代谢途径和机制进行详细的解析,并结合使用光呼吸突变体和一系列CH30H代谢相关化合物分析CH30H代谢作用及其刺激植物生长的相关性。进一步分析甲醇对两种模式植物光合碳同化及相关基因表达的影响,在代谢水平和转录水平上阐述CH30H刺激两种模式植物生长的机制。主要研究结果和结论如下：
通过叶面喷施三种C1化合物处理盆栽拟南芥发现CH30H促进其生长,并诱导多数光合作用相关基因的表达,HCHO强烈抑制其生长,同时引发造成蛋白质过氧化损伤并激活胁迫应答系统,HCOOH的毒性与HCHO相比较小,三种化合物处理对多数Cl代谢基因表达没有显著影响,但都抑制5,10-亚甲基-四氢叶酸还原酶基因的表达。
综合生理水平和转录水平的分析发现,叶绿素的大量流失造成叶片的黄化甚至白化是两种模式植物经受HCHO胁迫的一种最典型的症状。HCHO胁迫可能通过抑制多种叶绿体结构蛋白以及光合作用关键酶基因的转录水平影响植物光和作用的正常进行。甲醛胁迫引发拟南芥中的DNA损伤和蛋白质过氧化损伤,热激蛋白的上调表达是拟南芥对甲醛胁迫的积极应答机制。医学领域的研究证实在动物体内吸入HCHO能够引起膜脂过氧化和蛋白质的氧化损伤,这也是HCHO对烟草产生毒害作用的一个显著特征,这可能由烟草中HCHO的代谢能力较差引起的。热激蛋白和蛋白质合成基因的下调表达也是降低烟草对甲醛胁迫抗性的主要原因之一。甲醛对甲基化循环关键酶基因表达的抑制是烟草中甲醛毒性的重要特征,这在一方面可能影响烟草中多种激素的合成从而对其生长产生严重的抑制作用,另一方面可能也破坏膜结构的组成,从而使膜脂易被氧化损伤。HCHO抑制拟南芥和烟草中大量脱毒相关基因如CYP、GT和GST的表达,这显示对脱毒途径的抑制可能是HCHO对植物产生毒害的普遍机制。
本研究利用13C-NMR技术对拟南芥和烟草中CH30H的代谢过程与其刺激植物生长的相关性分析,并结合CH30H对两种模式植物光合碳同化及相关基因表达的影响结果分析显示,在固体MS培养条件下,拟南芥和烟草中低浓度CH30H对植物生长的促进效果最为显著,而此时13CH30H代谢代谢产生的HCOOH更倾向于进入叶酸依赖的C1代谢途径,而不是氧化为CO2进入卡尔文循环,13CH30H代谢的主要产物是[3-13C]Ser,其代谢过程与其刺激生长作用不存在显著的相关性。低浓度CH30H强烈诱导光合作用相关基因的表达并刺激光合碳同化过程是其刺激拟南芥生长的主要机制。烟草对CH30H的氧化能力比拟南芥强,烟草中不同浓度CH30H的代谢机制很相似,对光合碳同化以及光合作用相关基因表达的刺激效果也相差不大,高浓度CH30H对烟草生长的刺激作用可能被其代谢积累的HCHO和HCOOH的毒性所抵消。
In the one-carbon (C1) metabolic network of higher plants, the folate-independent metabolism of three Cl compounds including methanol (CH3OH), formaldehyde (HCHO) and formate (HCOOH) is the most obscure sector. Application of exogenous methanol on a series of plants has been reported to be able to enhance their growth and yields. However, the effect of CH3OH stimulation on plant growth was affected by various environmental conditions. As the metabolites downstream CH3OH metabolism in higher plants, both HCHO and HCOOH are toxic to plants but the toxicity of HCOOH is weaker than that of HCHO. In this study, foliar application of these three C1compounds was firstly performed on pot-grown Arabidopsis plants to provide a preliminary exploration on whether foliar application of C1compounds at very low concentration exerted an influence on plant growth, physiological characteristics as well as expressions of genes related to the defense-responsive systems, C1metabolic pathways and photosynthesis. As a ubiquitous environmental pollutant, comprehensive studies have been carried out to investigate the molecular mechanism of HCHO toxicity in medical field, while limited researches were performed to explore the toxicity mechanism of HCHO in plants. Arabidopsis and tobacco are the most widely used model plants in the fields of plant science. Our previous studies indicated that Arabidopsis and tobacco displayed different tolerance to exogenous HCHO due to their radically different HCHO-metabolic mechanisms. In this study, the reverse suppression subtractive hybridization (SSH) cDNA library was constructed in Arabidopsis and tobacco under2mM HCHO stress, respectively, combining with cDNA microarray analysis in Arabidopsis, to identify the potential HCHO-repressive genes in Arabidopsis and tobacco. The main purpose of this section is to reveal the HCHO toxic mechanisms in the two model plants and to interpret the similarities and differences in mechanisms of HCHO inhibition on the growth of Arabidopsis and tobacco at the transcriptional level as well as to provide new candidate genes for genetic manipulation to improve plant HCHO-resistant ability. Although previous studies have already provided some clues on the possible metabolic flux of CH3OH in plants, the detailed metabolic pathway of CH3OH in plants is still unclear. Both Arabidopsis and tobacco were treated with13CH3OH to obtain their13C-NMR metabolic profiles for further clarification of their CH3OH-metabolic mechanisms. In addition, using a photorespiration mutant of Arabidopsis and different compounds related to CH3OH metabolism, further analysis were performed to clarity the correlation of CH3OH metabolism and the stimulatory effects of CH3OH on plant growth. In the end, the effects of CH3OH on the NaH13CO3metabolic profiles and the expression of photosynthesis-related genes were comprehensively analyzed to clarify the mechanism of CH3OH stimulation on the growth of the two model plants at the metabolic and transcriptional levels. The major results and conclusions are as follows.
Effects of foliar spraying different C1compounds on Arabidopsis grown under greenhouse conditions were analyzed. The results indicated that methanol stimulated the growth of Arabidopsis, accompanied by activation on expression of photosynthesis-related genes. On the contrary, formaldehyde and formic acid inhibited its growth and the inhibition of formaldehyde was much remarkable. Formaldehyde treatment elevated the levels of soluble sugars, H2O2and carbonyl-proteins in leaves, suggesting occurrence of oxidative stress. Meanwhile, formaldehyde activated the stress-responsive system in Arabidopsis. Interestingly, three C1compounds had no remarkable impacts on expressions of most selected genes involved in C1metabolism but all repressed the expression of5,10-methylene-THF reductase.
Comprehensive analyses at physiological and transcriptional levels were performed to analyze toxic effects of HCHO exposure on Arabidopsis and tobacco. Leaf chlorosis and bleach were identified as the most representative symptoms when plants were exposed to HCHO. HCHO treatment exerted impacts on photosynthesis by repressing expressions of photosynthesis and chloroplast structure-related genes. Exposure to2mM HCHO led to a remarkable increase in levels of protein carbonyl and DNA-protein crosslinks in Arabidopsis, indicating the accumulation of oxidative damage to proteins and DNA. Up-regulation in many genes encoding heat shock proteins was suggested to be an important protective mechanism for Arabidopsis plants in response to the oxidative damage of proteins produced under HCHO stress. Previous investigations on HCHO toxicity in animals validated that inhalation of exogenous HCHO induced accumulation of oxidative damages on membrane lipids and proteins, which was suggested to be the typical toxic effects of HCHO in tobacco. This may be due to the relative weaker ability to metabolize exogenous HCHO by tobacco as compared with Arabidopsis. Meanwhile, down-regulations of HSPs (such as HSP70and DNAJ) might be a potential cause of the oxidative damage to proteins. Moreover, repressed expression of a large number of transcripts related to protein synthesis might be one of the molecular bases of the weak tolerance of tobacco to HCHO stress. Differing from cases in Arabidopsis, transcription of many key enzymes (such as SAMS, SAMDC, SAMMT) related to the activated methylation cycle in C1metabolic network were repressed in tobacco under HCHO stress. This might have impacts on synthesis of hormones and the components of membrane structure, which would lead to the oxidative damage to membrane lipids and the severe inhibition on the growth of tobacco. Repressive effects of HCHO on expressions of transcripts involved in detoxification metabolism in higher plants, such as CYP, GT and GST, were proposed to be the common toxic mechanism of HCHO in plants.
The most important index indicating the stimulatory effect of CH3OH on plant growth is reflected as an increase in biomass, which is mainly attributed to photosynthesis. Using13C-NMR analysis, the relation between metabolism of13CH3OH and the effects of CH3OH stimulation on plant growth was investigated The results indicated that, when grown on MS agar medium, addition of2mM exogenous CH3OH had best effects on the growth of Arabidopsis and tobacco. However, the H13COOH produced from the metabolism of2mM13CH3OH in Arabidopsis preferred to flow into the C1metabolic pathways and produce large amount of [3-13C]Ser rather than oxidized as CO2which was then incorporated into the Calvin cycle and converted into carbohydrates. These results suggest that the stimulation effects of CH3OH on Arabidopsis growth are independent from its metabolism. Thus, it is hypothesized that the free CH3OH absorbed by Arabidopsis might act as a signal molecule to modulate the plant growth. Further analysis validated the presence of low concentration of CH3OH significantly induced the expression of most photosynthesis-related transcripts, which is suggested to be the main molecular basis for stimulation of CH3OH on plant growth. In tobacco,[3-13C]Ser was also identified to be a major product of13CH3OH metabolism. A comparison for metabolic profiles of13CH3OH with different concentration indicated no significant difference in the mechanism between lower and higher concentration of CH3OH metabolism in tobacco. Further analysis on the expression profiles of chloroplast proteins and photosynthesis-related key enzymes obtained a different result from those with Arabidopsis. CH3OH had no significant inducible effects on expressions of chloroplast structural proteins but pronouncedly stimulated expressions of key enzymes involved in CO2assimilation. Moreover, different concentrations of CH3OH showed almost same inducible effects on expression of these genes in tobacco.
通过叶面喷施三种C1化合物处理盆栽拟南芥发现CH30H促进其生长,并诱导多数光合作用相关基因的表达,HCHO强烈抑制其生长,同时引发造成蛋白质过氧化损伤并激活胁迫应答系统,HCOOH的毒性与HCHO相比较小,三种化合物处理对多数Cl代谢基因表达没有显著影响,但都抑制5,10-亚甲基-四氢叶酸还原酶基因的表达。
综合生理水平和转录水平的分析发现,叶绿素的大量流失造成叶片的黄化甚至白化是两种模式植物经受HCHO胁迫的一种最典型的症状。HCHO胁迫可能通过抑制多种叶绿体结构蛋白以及光合作用关键酶基因的转录水平影响植物光和作用的正常进行。甲醛胁迫引发拟南芥中的DNA损伤和蛋白质过氧化损伤,热激蛋白的上调表达是拟南芥对甲醛胁迫的积极应答机制。医学领域的研究证实在动物体内吸入HCHO能够引起膜脂过氧化和蛋白质的氧化损伤,这也是HCHO对烟草产生毒害作用的一个显著特征,这可能由烟草中HCHO的代谢能力较差引起的。热激蛋白和蛋白质合成基因的下调表达也是降低烟草对甲醛胁迫抗性的主要原因之一。甲醛对甲基化循环关键酶基因表达的抑制是烟草中甲醛毒性的重要特征,这在一方面可能影响烟草中多种激素的合成从而对其生长产生严重的抑制作用,另一方面可能也破坏膜结构的组成,从而使膜脂易被氧化损伤。HCHO抑制拟南芥和烟草中大量脱毒相关基因如CYP、GT和GST的表达,这显示对脱毒途径的抑制可能是HCHO对植物产生毒害的普遍机制。
本研究利用13C-NMR技术对拟南芥和烟草中CH30H的代谢过程与其刺激植物生长的相关性分析,并结合CH30H对两种模式植物光合碳同化及相关基因表达的影响结果分析显示,在固体MS培养条件下,拟南芥和烟草中低浓度CH30H对植物生长的促进效果最为显著,而此时13CH30H代谢代谢产生的HCOOH更倾向于进入叶酸依赖的C1代谢途径,而不是氧化为CO2进入卡尔文循环,13CH30H代谢的主要产物是[3-13C]Ser,其代谢过程与其刺激生长作用不存在显著的相关性。低浓度CH30H强烈诱导光合作用相关基因的表达并刺激光合碳同化过程是其刺激拟南芥生长的主要机制。烟草对CH30H的氧化能力比拟南芥强,烟草中不同浓度CH30H的代谢机制很相似,对光合碳同化以及光合作用相关基因表达的刺激效果也相差不大,高浓度CH30H对烟草生长的刺激作用可能被其代谢积累的HCHO和HCOOH的毒性所抵消。
In the one-carbon (C1) metabolic network of higher plants, the folate-independent metabolism of three Cl compounds including methanol (CH3OH), formaldehyde (HCHO) and formate (HCOOH) is the most obscure sector. Application of exogenous methanol on a series of plants has been reported to be able to enhance their growth and yields. However, the effect of CH3OH stimulation on plant growth was affected by various environmental conditions. As the metabolites downstream CH3OH metabolism in higher plants, both HCHO and HCOOH are toxic to plants but the toxicity of HCOOH is weaker than that of HCHO. In this study, foliar application of these three C1compounds was firstly performed on pot-grown Arabidopsis plants to provide a preliminary exploration on whether foliar application of C1compounds at very low concentration exerted an influence on plant growth, physiological characteristics as well as expressions of genes related to the defense-responsive systems, C1metabolic pathways and photosynthesis. As a ubiquitous environmental pollutant, comprehensive studies have been carried out to investigate the molecular mechanism of HCHO toxicity in medical field, while limited researches were performed to explore the toxicity mechanism of HCHO in plants. Arabidopsis and tobacco are the most widely used model plants in the fields of plant science. Our previous studies indicated that Arabidopsis and tobacco displayed different tolerance to exogenous HCHO due to their radically different HCHO-metabolic mechanisms. In this study, the reverse suppression subtractive hybridization (SSH) cDNA library was constructed in Arabidopsis and tobacco under2mM HCHO stress, respectively, combining with cDNA microarray analysis in Arabidopsis, to identify the potential HCHO-repressive genes in Arabidopsis and tobacco. The main purpose of this section is to reveal the HCHO toxic mechanisms in the two model plants and to interpret the similarities and differences in mechanisms of HCHO inhibition on the growth of Arabidopsis and tobacco at the transcriptional level as well as to provide new candidate genes for genetic manipulation to improve plant HCHO-resistant ability. Although previous studies have already provided some clues on the possible metabolic flux of CH3OH in plants, the detailed metabolic pathway of CH3OH in plants is still unclear. Both Arabidopsis and tobacco were treated with13CH3OH to obtain their13C-NMR metabolic profiles for further clarification of their CH3OH-metabolic mechanisms. In addition, using a photorespiration mutant of Arabidopsis and different compounds related to CH3OH metabolism, further analysis were performed to clarity the correlation of CH3OH metabolism and the stimulatory effects of CH3OH on plant growth. In the end, the effects of CH3OH on the NaH13CO3metabolic profiles and the expression of photosynthesis-related genes were comprehensively analyzed to clarify the mechanism of CH3OH stimulation on the growth of the two model plants at the metabolic and transcriptional levels. The major results and conclusions are as follows.
Effects of foliar spraying different C1compounds on Arabidopsis grown under greenhouse conditions were analyzed. The results indicated that methanol stimulated the growth of Arabidopsis, accompanied by activation on expression of photosynthesis-related genes. On the contrary, formaldehyde and formic acid inhibited its growth and the inhibition of formaldehyde was much remarkable. Formaldehyde treatment elevated the levels of soluble sugars, H2O2and carbonyl-proteins in leaves, suggesting occurrence of oxidative stress. Meanwhile, formaldehyde activated the stress-responsive system in Arabidopsis. Interestingly, three C1compounds had no remarkable impacts on expressions of most selected genes involved in C1metabolism but all repressed the expression of5,10-methylene-THF reductase.
Comprehensive analyses at physiological and transcriptional levels were performed to analyze toxic effects of HCHO exposure on Arabidopsis and tobacco. Leaf chlorosis and bleach were identified as the most representative symptoms when plants were exposed to HCHO. HCHO treatment exerted impacts on photosynthesis by repressing expressions of photosynthesis and chloroplast structure-related genes. Exposure to2mM HCHO led to a remarkable increase in levels of protein carbonyl and DNA-protein crosslinks in Arabidopsis, indicating the accumulation of oxidative damage to proteins and DNA. Up-regulation in many genes encoding heat shock proteins was suggested to be an important protective mechanism for Arabidopsis plants in response to the oxidative damage of proteins produced under HCHO stress. Previous investigations on HCHO toxicity in animals validated that inhalation of exogenous HCHO induced accumulation of oxidative damages on membrane lipids and proteins, which was suggested to be the typical toxic effects of HCHO in tobacco. This may be due to the relative weaker ability to metabolize exogenous HCHO by tobacco as compared with Arabidopsis. Meanwhile, down-regulations of HSPs (such as HSP70and DNAJ) might be a potential cause of the oxidative damage to proteins. Moreover, repressed expression of a large number of transcripts related to protein synthesis might be one of the molecular bases of the weak tolerance of tobacco to HCHO stress. Differing from cases in Arabidopsis, transcription of many key enzymes (such as SAMS, SAMDC, SAMMT) related to the activated methylation cycle in C1metabolic network were repressed in tobacco under HCHO stress. This might have impacts on synthesis of hormones and the components of membrane structure, which would lead to the oxidative damage to membrane lipids and the severe inhibition on the growth of tobacco. Repressive effects of HCHO on expressions of transcripts involved in detoxification metabolism in higher plants, such as CYP, GT and GST, were proposed to be the common toxic mechanism of HCHO in plants.
The most important index indicating the stimulatory effect of CH3OH on plant growth is reflected as an increase in biomass, which is mainly attributed to photosynthesis. Using13C-NMR analysis, the relation between metabolism of13CH3OH and the effects of CH3OH stimulation on plant growth was investigated The results indicated that, when grown on MS agar medium, addition of2mM exogenous CH3OH had best effects on the growth of Arabidopsis and tobacco. However, the H13COOH produced from the metabolism of2mM13CH3OH in Arabidopsis preferred to flow into the C1metabolic pathways and produce large amount of [3-13C]Ser rather than oxidized as CO2which was then incorporated into the Calvin cycle and converted into carbohydrates. These results suggest that the stimulation effects of CH3OH on Arabidopsis growth are independent from its metabolism. Thus, it is hypothesized that the free CH3OH absorbed by Arabidopsis might act as a signal molecule to modulate the plant growth. Further analysis validated the presence of low concentration of CH3OH significantly induced the expression of most photosynthesis-related transcripts, which is suggested to be the main molecular basis for stimulation of CH3OH on plant growth. In tobacco,[3-13C]Ser was also identified to be a major product of13CH3OH metabolism. A comparison for metabolic profiles of13CH3OH with different concentration indicated no significant difference in the mechanism between lower and higher concentration of CH3OH metabolism in tobacco. Further analysis on the expression profiles of chloroplast proteins and photosynthesis-related key enzymes obtained a different result from those with Arabidopsis. CH3OH had no significant inducible effects on expressions of chloroplast structural proteins but pronouncedly stimulated expressions of key enzymes involved in CO2assimilation. Moreover, different concentrations of CH3OH showed almost same inducible effects on expression of these genes in tobacco.
引文
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