醉马草—内生真菌共生体对胁迫的响应及其次生代谢产物活性的研究
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摘要
醉马草(Achnatherum inebrians (Hance) Keng)为禾本科(Gramineae)芨芨草属(Achnatherum)的多年生草本植物,是我国北方天然草原主要的烈性毒草之一,与甘肃内生真菌(Neotyphodium gansuense Li et Nan)形成共生是其对家畜致毒的原因。本研究以带内生真菌(E+)和不带内生真菌(E-)的醉马草群体为材料,研究了其抗虫性的异同；探讨了干旱和盐胁迫对E+醉马草产生麦角类生物碱的影响及其对重金属镉胁迫的响应；分离、鉴定了E+醉马草中的生物碱和挥发油等次生代谢产物,测定了其生物活性。主要结果如下：
1.室内饲喂和田间取食试验的结果表明,内生真菌的侵染显著(P<0.05)降低了亚洲小车蝗(Oedaleus decorus)和针毛收获蚁Messor aciculatus)对醉马草叶片和种子的取食量。
2.室内萌发和盆栽试验结果表明,当镉浓度≥100μmol/L时,内生真菌侵染显著(P<0.05)增加了醉马草种子的萌发和幼苗的生长,E+幼苗抗氧化酶活性和脯氨酸含量均显著(P<0.05)高于E-幼苗,但是E-幼苗丙二醛(MDA)的含量显著(P<0.05)高于E+幼苗。内生真菌侵染可以缓解镉胁迫对醉马草的毒害作用。
3.温室盆栽试验结果表明,干旱胁迫和盐胁迫均增加了E+醉马草中麦角生物碱的积累,两种胁迫条件下,均是麦角新碱的含量显著高于麦角酰胺(P<0.05)。
4.与乙醇冷浸法相比,超声波结合乙醇热回流法可从E+醉马草中提取更大量的粗浸膏；分离获得了E+醉马草中麦角类生物碱的纯品化合物,通过结构解析确定其为异麦角新碱和麦角新碱。E-醉马草不含有这两种麦角生物碱。
5.自E+醉马草获得的含有生物碱的粗浸膏对细交链孢(Alternaria alternata)、根腐离蠕孢(Bipolaris sorokiniana)、新月弯孢(Curvularia lunata)、燕麦镰孢(Fusarium avenaceum)和腐皮镰孢(Fusarium solani)等5种植物病原真菌以及绿色木霉菌(Trichoderma viride)的菌落生长、孢子萌发和芽管伸长均具有较强的抑制作用。两种麦角生物碱对动物平滑肌细胞均具有明显的细胞毒活性,且生物碱浓度与细胞的抑制率呈显著正相关(P<0.05),回归方程分别为：Y麦角=0.0041x+0.205(R2=0.945,P<0.05)和Y异麦角=0.0032x+0.2672(R2=0.9411,P<0.05),麦角新碱和异麦角新碱的半致死浓度分别为71.95μg/mL和72.75μg/mL。
6.通过水蒸汽蒸馏法,得到了E+和E-醉马草植株以及分离自E+醉马草植株中内生真菌的挥发油,通过气相色谱和质谱仪联用(GC-MS)分析其结构,发现自E+、E-植株和内生真菌中提取的挥发油分别含有61、59和34种化合物。其中7种化合物同时存在于E+、E-醉马草和内生真菌的挥发油,31种化合物同时存在于E+和E-醉马草的挥发油中,5种化合物为E+醉马草及其内生真菌所特有。十七烷烃是E+和E-醉马草挥发油中含量最高的化合物,正十四烷烃是E+醉马草及其内生真菌挥发油中的主要成分,二氧杂环戊烷为内生真菌主要的挥发油成分。
7.自E+与E-醉马草植株提取的挥发油对细交链孢、根腐离蠕孢、新月弯孢、燕麦镰孢、腐皮镰孢和绿色木霉等真菌均有抑制作用,与E-植株相比,E+植株中提取的挥发油有更强的抑菌活性(P<0.05),其中对腐皮镰孢孢子萌发抑制率最强,其半致死浓度(IC50)值为0.224mg/mL。E+与E-醉马草植株中提取的挥发油对多年生黑麦草(Lolium perenne)、高羊茅(Festuca arundinacea)和草地早熟禾(Poa pratensis)等3种牧草的种子萌发和幼苗生长亦有抑制作用,且受到的抑制随挥发油浓度而增加。自E+植株中提取的挥发油的抑制作用强于E-植株中的,当挥发油浓度达到300mg/mL,三种牧草的发芽率、胚芽长、胚根长、鲜重和干重等均表现出显著差异(P<0.05),过氧化物酶(POD)、抗坏血酸酶(APX)和过氧化氢酶(CAT)的活性以及可溶性糖和脯氨酸含量等表现出同样差异；超氧化物歧化酶(SOD)活性和电导率值以及MDA含量则是E+挥发油处理显著(P<0.05)高于E-处理。
Drunken horse grass (Achnatherum inebrians) is a toxic perennial bunchgrass, which is so-named because it is associated with the narcosis of grazing animals on native grasslands in Northwest of China. This species is usually infected by the fungal endophyte Neotyphodium gansuense. The difference of the pest resistance of endophyte-infected (E+) and endophyte-free (E-) plants was investigated in this study. A series of experiments were conducted to study the effects of cadmium stress on seed germination, seedling growth and anti-oxidative systems of this grass. Drought and salt stresses can influence the concentrations of ergot alkaloids. The chemical composition and antifungal activity of the second metabolites (such as alkaloids and volatile oil) of E+and E-drunken horse grass were compared. The results were summarised as the follows:
1. In the field experiment and laboratory tests, grasshopper species(Oedaleus decorus) and seed harvesting ant (Messor aciculatus) ate significantly (P<0.05) more E-than E+leaves and seeds, respectively.
2. Germination and greenhouse experiments showed that the seed germination, seedling growth, antioxidative enzyme activities of superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX) and the proline content of E+plants were significantly (P<0.05) higher than E-plants when the cadmium concentration was greater than or equal to100μmol/L. The malondialdehude (MDA) contents of E-seedlings were significantly (P<0.05) higher than E+seedlings. Endophyte infection was concluded to be of benefit to the growth and anti-oxidative mechanisms within A. inebrians under high concentrations of Cadmium chloride
3. Greenhouse experiments showed that drought stress had a significant (P＜0.05) effect on the levels of ergonovine and ergine in both the Yuzhong (YZ) and Xiahe (XH) ecotypes. Levels of ergonovine were significantly (P＜0.05) higher than those of ergine and the difference between these two ecotypes was also significant (P＜0.05). Salt stress also had a significant (P＜0.05) effect on the levels of both ergonovine and ergine in the two ecotypes. Levels of ergonovine were also significantly (P＜0.05) higher than those of ergine and the difference between YZ and XH ecotypes was not significant (P>0.05).
4. Compared with the method of ethanol immersion, ultrasound combined with hot alcohol reflux was a more effective method for extracting from drunken horse grass. Pure samples of the two ergot alkaloids from E+plants were obtained and the structures were identified as either ergonovinine and ergonovine, while these two alkaloids did not exist in the E-plants.
5. Crude extractions from E+plants significantly (P<0.05) inhibited the fungi mycelia growth, spores germination and the lengths of germ tube of5pathogenic fungi (Alternaria alternata, Bipolaris sorokiniana, Curvularia lunata, Fusarium solani, Fusarium avenaceum) and Trichoderma viride. The fraction, which contained the two ergot alkaloids, ergonovine and ergonovinine, shown the strongest inhibiting effect. Effects of E+and E-petroleum ether extraction on17different fungi were different, and the effects on the same fungi were also different between E+and E-. Both of the two ergot alkaloids have the cytotoxicity on animal smooth muscle cells, the cell inhibition rate was increasing as the alkaloid concentrations increased and there exist a significantly (P＜0.05) positive correlation. The equation of the regression for these two alkaloids were Yergonovine=0.0041x+0.205(R2=0.945, P＜0.05) and Yergonovinine=0.0032x+0.2672(R2=0.9411, P＜0.05). The median lethal concentration (IC50) for ergonovine and ergonovinine was71.95μg/mL and72.75μg/mL, respectively.
6. The volatile oils of E+/E-plants and3endophyte strains from the grass grown in Xiahe (XH), Yuzhong (YZ) and Sunan (SN) counties of Gansu province of China were obtained by hydro-distillation. The chemical composition was analyzed by gas chromatography-mass spectrometry (GC-MS). This resulted in the identification of61,59and34components for E+, E-and YZ strain, respectively. Heptadecane was the main component in both E+and E-volatile oils, and the mass fraction of this compound was up to9.06%and10.28%, respectively. There were31compounds identified that existed simultaneously in the E+and E-plants. There were7compounds identified that existed simultaneously in the E+/E-and YZ strain, and5compounds existed simultaneously in the E+and YZ strain. The presence of N. gansuense apparently affected some qualitative and quantitative differences in the volatile compounds production of this grass. The number of the compounds identified was36and42for the XH and SN strain. Trimethylsilyl methanol (63.31%) was the main component for XH, while3-Dioxolane (75.63%) and2-Methoxy-1,3-dioxolane (70.49%) was the main component for YZ and SN.
7. Colonies of fungi were inhibited significantly (P＜0.05) by E+(vs. E-) volatiles when the oil's concentration was greater than0.02mg/mL and fungi showed increased inhibition with increasing oil dose. It is clear that the effect of the E+oil on spore germination was stronger than that of E-oil. The maximum inhibitory effect of the E+(vs. E-) volatile oil were observed against Fusarium solani and Fusarium avenaceum, the IC50values being0.224mg/mL and0.417mg/L, respectively. The germination experiment showed that the seed germination, activities of POD, CAT and APX of perennial ryegrass (Lolium perenne), tall fescue (Festuca arundinaced) and grassland bluegrass (Poe pratensis) under E-treatment were significantly (P＜0.05) higher than the E+treatment when the oil concentration was greater than or equal to300mg/mL. The experiment also showed that there was an increased inhibition with increasing oil dose, as did the contents of soluble sugar and proline. However, the activity of SOD, conductivity value and the MDA content of E+treatment were significantly (P<0.05) higher than E-treatment.
1.室内饲喂和田间取食试验的结果表明,内生真菌的侵染显著(P<0.05)降低了亚洲小车蝗(Oedaleus decorus)和针毛收获蚁Messor aciculatus)对醉马草叶片和种子的取食量。
2.室内萌发和盆栽试验结果表明,当镉浓度≥100μmol/L时,内生真菌侵染显著(P<0.05)增加了醉马草种子的萌发和幼苗的生长,E+幼苗抗氧化酶活性和脯氨酸含量均显著(P<0.05)高于E-幼苗,但是E-幼苗丙二醛(MDA)的含量显著(P<0.05)高于E+幼苗。内生真菌侵染可以缓解镉胁迫对醉马草的毒害作用。
3.温室盆栽试验结果表明,干旱胁迫和盐胁迫均增加了E+醉马草中麦角生物碱的积累,两种胁迫条件下,均是麦角新碱的含量显著高于麦角酰胺(P<0.05)。
4.与乙醇冷浸法相比,超声波结合乙醇热回流法可从E+醉马草中提取更大量的粗浸膏；分离获得了E+醉马草中麦角类生物碱的纯品化合物,通过结构解析确定其为异麦角新碱和麦角新碱。E-醉马草不含有这两种麦角生物碱。
5.自E+醉马草获得的含有生物碱的粗浸膏对细交链孢(Alternaria alternata)、根腐离蠕孢(Bipolaris sorokiniana)、新月弯孢(Curvularia lunata)、燕麦镰孢(Fusarium avenaceum)和腐皮镰孢(Fusarium solani)等5种植物病原真菌以及绿色木霉菌(Trichoderma viride)的菌落生长、孢子萌发和芽管伸长均具有较强的抑制作用。两种麦角生物碱对动物平滑肌细胞均具有明显的细胞毒活性,且生物碱浓度与细胞的抑制率呈显著正相关(P<0.05),回归方程分别为：Y麦角=0.0041x+0.205(R2=0.945,P<0.05)和Y异麦角=0.0032x+0.2672(R2=0.9411,P<0.05),麦角新碱和异麦角新碱的半致死浓度分别为71.95μg/mL和72.75μg/mL。
6.通过水蒸汽蒸馏法,得到了E+和E-醉马草植株以及分离自E+醉马草植株中内生真菌的挥发油,通过气相色谱和质谱仪联用(GC-MS)分析其结构,发现自E+、E-植株和内生真菌中提取的挥发油分别含有61、59和34种化合物。其中7种化合物同时存在于E+、E-醉马草和内生真菌的挥发油,31种化合物同时存在于E+和E-醉马草的挥发油中,5种化合物为E+醉马草及其内生真菌所特有。十七烷烃是E+和E-醉马草挥发油中含量最高的化合物,正十四烷烃是E+醉马草及其内生真菌挥发油中的主要成分,二氧杂环戊烷为内生真菌主要的挥发油成分。
7.自E+与E-醉马草植株提取的挥发油对细交链孢、根腐离蠕孢、新月弯孢、燕麦镰孢、腐皮镰孢和绿色木霉等真菌均有抑制作用,与E-植株相比,E+植株中提取的挥发油有更强的抑菌活性(P<0.05),其中对腐皮镰孢孢子萌发抑制率最强,其半致死浓度(IC50)值为0.224mg/mL。E+与E-醉马草植株中提取的挥发油对多年生黑麦草(Lolium perenne)、高羊茅(Festuca arundinacea)和草地早熟禾(Poa pratensis)等3种牧草的种子萌发和幼苗生长亦有抑制作用,且受到的抑制随挥发油浓度而增加。自E+植株中提取的挥发油的抑制作用强于E-植株中的,当挥发油浓度达到300mg/mL,三种牧草的发芽率、胚芽长、胚根长、鲜重和干重等均表现出显著差异(P<0.05),过氧化物酶(POD)、抗坏血酸酶(APX)和过氧化氢酶(CAT)的活性以及可溶性糖和脯氨酸含量等表现出同样差异；超氧化物歧化酶(SOD)活性和电导率值以及MDA含量则是E+挥发油处理显著(P<0.05)高于E-处理。
Drunken horse grass (Achnatherum inebrians) is a toxic perennial bunchgrass, which is so-named because it is associated with the narcosis of grazing animals on native grasslands in Northwest of China. This species is usually infected by the fungal endophyte Neotyphodium gansuense. The difference of the pest resistance of endophyte-infected (E+) and endophyte-free (E-) plants was investigated in this study. A series of experiments were conducted to study the effects of cadmium stress on seed germination, seedling growth and anti-oxidative systems of this grass. Drought and salt stresses can influence the concentrations of ergot alkaloids. The chemical composition and antifungal activity of the second metabolites (such as alkaloids and volatile oil) of E+and E-drunken horse grass were compared. The results were summarised as the follows:
1. In the field experiment and laboratory tests, grasshopper species(Oedaleus decorus) and seed harvesting ant (Messor aciculatus) ate significantly (P<0.05) more E-than E+leaves and seeds, respectively.
2. Germination and greenhouse experiments showed that the seed germination, seedling growth, antioxidative enzyme activities of superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX) and the proline content of E+plants were significantly (P<0.05) higher than E-plants when the cadmium concentration was greater than or equal to100μmol/L. The malondialdehude (MDA) contents of E-seedlings were significantly (P<0.05) higher than E+seedlings. Endophyte infection was concluded to be of benefit to the growth and anti-oxidative mechanisms within A. inebrians under high concentrations of Cadmium chloride
3. Greenhouse experiments showed that drought stress had a significant (P＜0.05) effect on the levels of ergonovine and ergine in both the Yuzhong (YZ) and Xiahe (XH) ecotypes. Levels of ergonovine were significantly (P＜0.05) higher than those of ergine and the difference between these two ecotypes was also significant (P＜0.05). Salt stress also had a significant (P＜0.05) effect on the levels of both ergonovine and ergine in the two ecotypes. Levels of ergonovine were also significantly (P＜0.05) higher than those of ergine and the difference between YZ and XH ecotypes was not significant (P>0.05).
4. Compared with the method of ethanol immersion, ultrasound combined with hot alcohol reflux was a more effective method for extracting from drunken horse grass. Pure samples of the two ergot alkaloids from E+plants were obtained and the structures were identified as either ergonovinine and ergonovine, while these two alkaloids did not exist in the E-plants.
5. Crude extractions from E+plants significantly (P<0.05) inhibited the fungi mycelia growth, spores germination and the lengths of germ tube of5pathogenic fungi (Alternaria alternata, Bipolaris sorokiniana, Curvularia lunata, Fusarium solani, Fusarium avenaceum) and Trichoderma viride. The fraction, which contained the two ergot alkaloids, ergonovine and ergonovinine, shown the strongest inhibiting effect. Effects of E+and E-petroleum ether extraction on17different fungi were different, and the effects on the same fungi were also different between E+and E-. Both of the two ergot alkaloids have the cytotoxicity on animal smooth muscle cells, the cell inhibition rate was increasing as the alkaloid concentrations increased and there exist a significantly (P＜0.05) positive correlation. The equation of the regression for these two alkaloids were Yergonovine=0.0041x+0.205(R2=0.945, P＜0.05) and Yergonovinine=0.0032x+0.2672(R2=0.9411, P＜0.05). The median lethal concentration (IC50) for ergonovine and ergonovinine was71.95μg/mL and72.75μg/mL, respectively.
6. The volatile oils of E+/E-plants and3endophyte strains from the grass grown in Xiahe (XH), Yuzhong (YZ) and Sunan (SN) counties of Gansu province of China were obtained by hydro-distillation. The chemical composition was analyzed by gas chromatography-mass spectrometry (GC-MS). This resulted in the identification of61,59and34components for E+, E-and YZ strain, respectively. Heptadecane was the main component in both E+and E-volatile oils, and the mass fraction of this compound was up to9.06%and10.28%, respectively. There were31compounds identified that existed simultaneously in the E+and E-plants. There were7compounds identified that existed simultaneously in the E+/E-and YZ strain, and5compounds existed simultaneously in the E+and YZ strain. The presence of N. gansuense apparently affected some qualitative and quantitative differences in the volatile compounds production of this grass. The number of the compounds identified was36and42for the XH and SN strain. Trimethylsilyl methanol (63.31%) was the main component for XH, while3-Dioxolane (75.63%) and2-Methoxy-1,3-dioxolane (70.49%) was the main component for YZ and SN.
7. Colonies of fungi were inhibited significantly (P＜0.05) by E+(vs. E-) volatiles when the oil's concentration was greater than0.02mg/mL and fungi showed increased inhibition with increasing oil dose. It is clear that the effect of the E+oil on spore germination was stronger than that of E-oil. The maximum inhibitory effect of the E+(vs. E-) volatile oil were observed against Fusarium solani and Fusarium avenaceum, the IC50values being0.224mg/mL and0.417mg/L, respectively. The germination experiment showed that the seed germination, activities of POD, CAT and APX of perennial ryegrass (Lolium perenne), tall fescue (Festuca arundinaced) and grassland bluegrass (Poe pratensis) under E-treatment were significantly (P＜0.05) higher than the E+treatment when the oil concentration was greater than or equal to300mg/mL. The experiment also showed that there was an increased inhibition with increasing oil dose, as did the contents of soluble sugar and proline. However, the activity of SOD, conductivity value and the MDA content of E+treatment were significantly (P<0.05) higher than E-treatment.
引文
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