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植物与植食性昆虫在长期的协同进化过程中不断地相互作用,彼此形成了许多防御及适应机制[1-2]。植物抗虫性按其来源可分为组成抗性和诱导抗性[3]。昆虫取食、剪叶损伤、植物激素全株处理等生物或非生物刺激均能诱导植物产生诱导抗性,使植物体内产生大量对害虫有毒、抗营养和抗消化的次生代谢产物,抑制或干扰植食昆虫正常的生长、发育和繁殖[4-7]。而昆虫凭借行为防御机制和生理、生化防御机制来降低植物诱导抗性对其造成的影响[8]。在生理、生化防御机制中利用解毒酶系和保护酶系来进行解毒和排毒是昆虫适应其寄主植物防御的重要方式[9]。超氧化物歧化酶(superoxide dismutase,SOD)和过氧化物酶(peroxidase,POD)是用于缓解昆虫体内氧化压力的两种重要的保护酶[10-11];谷胱甘肽S-转移酶(glutathione S-transferases,GSTs)、酸性磷酸酯酶(acid phosphatase,ACP)、碱性磷酸酯酶(alkaline phosphatase,AKP)是昆虫体内重要的解毒酶,参与外源毒物的分解代谢[12-13]。
落叶松毛虫(Dendrolimus superans)主要分布于中国东北林区,是长白落叶松(Larix olgensis)重要的叶部害虫。茉莉酸甲酯(MeJA)作为一种重要的植物激素,被广泛用于提高植物的诱导抗性[14-15]。冯春富等[16-17]发现对兴安落叶松(Larix gmelinii)全株喷施茉莉酸甲酯,能干扰舞毒蛾幼虫体内保护酶和解毒酶的活性,使幼虫体质量显著下降,存活率降低,蛹质量减轻,产卵量减少。严善春等[18]发现茉莉酸甲酯处理兴安落叶松后对落叶松毛虫幼虫具有驱避作用。但用MeJA局部喷施长白落叶松,能否诱导全株对落叶松毛虫幼虫体内的保护酶和解毒酶的活性产生干扰,从而抑制其排毒代谢尚未见报道。
本研究用不同浓度的MeJA局部喷施长白落叶松,比较分析局部喷施后长白落叶松对落叶松毛虫3~5龄幼虫体内SOD、POD、GSTs、ACP、AKP活性的影响,以期弄清茉莉酸甲酯局部喷施长白落叶松能否诱导全株影响松毛虫幼虫体内保护酶和解毒酶的活力水平。
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2014年4月末,在黑龙江省平山森林植物检疫隔离试种苗圃内,将4年生长白落叶松移植于规格为230 mm × 250 mm(高×直径)的花盆中,恢复生长2个月。落叶松毛虫蛹采集于内蒙古克什克腾旗人工长白落叶松纯林,然后带回实验室使其进行羽化。将新羽化的雌雄成虫放置于规格为140 mm×120 mm×55 mm(长×宽×高)的塑料瓶内使其自行交配产卵,瓶内放一个饱蘸20%蜂蜜液的棉球供成虫补充营养,直至成虫死亡。将卵块收集起来,并在6月末使其进行孵化。初孵幼虫用新鲜的长白落叶松针叶饲养至2龄备用。羽化、交尾、孵化以及初孵幼虫饲养实验均在实验室光照培养箱室(哈尔滨市东联电子技术开发有限公司HPG-280HX型)进行,设置的条件均为温度(25±1)℃,相对湿度(70±1)%,光周期(16L :8D)。
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7月初,将健康、长势一致的长白落叶松苗随机分为4组,每个处理组100株,并对其进行诱导处理。将茉莉酸甲酯(MeJA,≥95%,Sigma-Aldrich)配制成0.01 mmol/L、0.10 mmol/L和1.00 mmol/L 3个浓度的水溶液。4组落叶松苗分为1个对照组和3个处理组,对照组喷施H2O,处理组分别用3个浓度茉莉酸甲酯对落叶松苗进行局部喷施处理。局部处理先将落叶松苗套袋,露出落叶松苗一侧的4个枝条,然后对其喷施茉莉酸甲酯溶液。每株喷施5 mL。各组的标记代码依次为:CK、MeJA0.01L、MeJA0.10L、MeJA1.00L。
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7月初选择新蜕皮的、个体大小发育一致、健康的松毛虫2龄幼虫,饥饿24 h后移置到4个不同处理组的长白落叶松苗枝条上,每株接2头幼虫,每个处理组共接200头幼虫,外罩纱网。每天记录各处理组的松毛虫幼虫生长发育情况,选取蜕皮不超过24 h的3龄、4龄、5龄幼虫,饥饿24 h后置于-40 ℃低温保存箱(青岛海尔特种电器有限公司DW-40L262型)中备用,用于测定体内保护酶和解毒酶的活性。
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参照冯春富等[16]的方法对虫体中的ACP、AKP和GSTs进行提取和酶活测定。重复测定3次。
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参照张鑫乾等[13]的方法对虫体中的SOD、POD进行提取和酶活测定。重复测定3次。
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参照Bradford[19]的考马斯亮蓝G-250染色法对虫体中的蛋白质进行提取和含量测定。重复测定3次。
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SOD、POD、GSTs的酶活(U/(mg ·min))=ΔA/(mt),式中:ΔA表示反应时间内吸光度的变化值(OD);m表示酶液中蛋白含量(mg);t表示反应时间(min)。ACP和AKP的酶活(μmol/(mg ·min))= n/(mt)=(A+0.007)/(0.009 3mt),式中:n表示反应时间内酶水解对硝基苯磷酸二钠生成的对硝基苯酚的含量(μmol);A表示反应结束后反应体系中的吸光度值(OD);m表示酶液中蛋白含量(mg);t表示反应时间(min)。
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使用SPSS19.0软件统计幼虫体内SOD、POD、ACP、AKP和GSTs活性的平均值和标准误差,采用one-way ANOVA进行差异显著性方差分析,以LSD (最小显著法)在0.05水平下检验取食不同处理的长白落叶松对松毛虫3~5龄幼虫体内保护酶和解毒酶的差异显著性。
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取食用MeJA局部处理的白落叶松针叶后,松毛虫幼虫体内SOD活性的变化见图 1。由图 1可知,各处理组的3、5龄幼虫体内SOD活性与CK差异不显著(P>0.05),但各处理组4龄幼虫的SOD活性均显著高于CK(P<0.05)。除了MeJA1.00L处理组在第4龄显著高于MeJA0.01L和MeJA0.10L处理组(P<0.05)之外,各处理组之间在3、4、5龄均差异不显著(P>0.05)。说明用MeJA局部处理的长白落叶松对落叶松毛虫幼虫的SOD活性有显著影响,但未发现与浓度有直接相关性。
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松毛虫幼虫体内POD活性的变化趋势与SOD一致,即各处理组的3、5龄幼虫体内POD活性与CK差异不显著(P>0.05),4龄幼虫的POD活性显著高于CK(P<0.05)(图 2)。相同龄期的各处理组之间的松毛虫幼虫体内POD活性差异不显著(P>0.05),对MeJA处理浓度不敏感。
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不同处理组幼虫体内的ACP活性均表现出先抑制后增强的趋势(图 3)。由图 3可知,各MeJA处理组的松毛虫幼虫体内ACP活性,在第3、4龄均显著低于CK(P<0.05),而在第5龄均高于CK,其中MeJA0.10L显著高于CK(P<0.05)。除了MeJA0.10L处理组在第4、5龄显著高于MeJA0.01L处理组(P<0.05)之外,各处理组之间在3、4、5龄均差异不显著(P>0.05)。说明MeJA局部处理能诱导长白落叶松干扰落叶松毛虫的解毒代谢,但未发现与浓度有直接相关性,而松毛虫幼虫能在逐渐适应后,通过提高ACP的活性去响应诱导抗性造成的毒害。
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不同处理组的落叶松毛虫幼虫体内的AKP活性见图 4。由图 4可知,各处理组的松毛虫幼虫,在3、4龄AKP活性均低于CK,其中在4龄显著低于CK(P<0.05);而在5龄AKP活性均高于CK,其中MeJA0.10L、MeJA1.00L处理组显著高于CK(P<0.05)。AKP活性,除了5龄的MeJA1.00L处理组显著高于MeJA0.01L和MeJA0.10L处理组之外(P<0.05),其他同龄各处理组之间差异均不显著(P>0.05)。说明用MeJA局部处理长白落叶松能显著干扰松毛虫幼虫AKP活性,但未发现与浓度有直接相关性;AKP对MeJA局部处理长白落叶松的响应趋势与ACP一致。
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各处理组的松毛虫幼虫体内GSTs活性,在第3、4龄均低于CK,其中MeJA0.10L和MeJA1.00L处理组在第3、4龄显著低于CK,MeJA0.01L处理组在第4龄显著低于CK(P<0.05);各处理组的5龄幼虫体内GSTs活性均显著高于CK(P<0.05)(图 5)。GSTs活性对MeJA不同浓度的响应未表现出任何规律性。说明MeJA局部处理能诱导提高长白落叶松的抗虫性,但未发现与浓度有直接相关性,松毛虫幼虫体内的GSTs活性对长白落叶松的抗虫性的响应趋势与ACP和AKP一致。
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MeJA全株处理植物能激发植物体内的茉莉酸途径,诱导产生许多有毒的次生代谢产物以及增强防御蛋白酶的活性用于抵御害虫的危害[20-22]。本研究发现用3种浓度的MeJA局部处理长白落叶松对落叶松毛虫幼虫体内保护酶和解毒酶活性均有显著的影响(P<0.05),均表现为先降低后升高的趋势,但未发现与浓度有直接相关性。说明局部喷施MeJA能诱导提高长白落叶松全株的系统抗性,对危害其针叶的落叶松毛虫幼虫产生毒害作用。王杰等[23]研究发现用外源茉莉酸局部喷施长白落叶松时可以系统诱导增强其防御蛋白的活性,这与本研究结果相互印证,进一步表明局部喷施外源茉莉酸类物质能提高植株整株的系统抗性。作者同时研究发现用MeJA局部处理长白落叶松后,能显著降低舞毒蛾(Lymantria dispar)3~6龄幼虫平均质量、幼虫存活率、蛹质量、化蛹率、羽化率以及成虫产卵数量[24]。说明用外源MeJA局部处理诱导长白落叶松产生的系统抗性对食叶害虫具有广谱性。
昆虫可以通过其体内复杂的保护酶系和解毒酶系来降低植物防御反应对其造成的影响[16, 25]。张雄帅等[26]发现油松毛虫(Dendrolimus tabulaeformis)在取食不同取食刺激下的油松(Pinus tabuliformis)之后,其体内的保护酶活性显著增强。王瑞龙等[27]在用分别添加6种植物次生物质的人工饲料饲养斜纹夜蛾(Spodoptera litura)时,发现斜纹夜蛾增强解毒酶的活性来提高对毒素的抗性。本研究发现,各处理组幼虫体内的SOD和POD活性均在第4龄显著高于CK(P<0.05),但3、5龄幼虫体内的SOD和POD活性与CK差异不显著(P>0.05);ACP、AKP和GSTs活性呈现出先抑制后增强的趋势。说明MeJA局部处理能诱导长白落叶松干扰落叶松毛虫的解毒代谢,而松毛虫幼虫能在逐渐适应后,通过调整和提高解毒酶的活性去响应和修复诱导抗性造成的毒害。
研究昆虫体内保护酶和解毒酶对植株诱导抗性的响应规律,有助于了解植食性昆虫对植物的反防御机制,为今后林木害虫的综合防治提供理论依据。但本研究发现落叶松毛虫能在逐渐适应后,通过提高保护酶和解毒酶的活性去响应诱导抗性造成的毒害,那么茉莉酸甲酯局部喷施长白落叶松苗能否对落叶松毛虫的生长发育造成干扰?有待进一步研究。
Effects of partially spraying Larix olgensis seedlings with exogenous methyl jasmonate on the defensive enzyme activities of Dendrolimus superans larvae
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摘要: 为明确茉莉酸甲酯局部处理林木对落叶松毛虫解毒代谢的影响,本研究以3种不同浓度的茉莉酸甲酯(MeJA,0.01、0.10和1.00mmol/L)局部处理长白落叶松苗的侧枝,分析不同处理对取食其针叶的落叶松毛虫3~5龄幼虫体内保护酶和解毒酶活性的影响。研究发现,3个浓度的MeJA局部处理长白落叶松对松毛虫幼虫体内保护酶和解毒酶活性均有显著影响(P < 0.05),酶活变化趋势一致,但未呈浓度依赖关系。各处理组幼虫体内的SOD和POD活性均在第4龄显著高于CK(P < 0.05),但3、5龄幼虫体内的SOD和POD活性与CK差异不显著(P>0.05);而ACP、AKP和GSTs活性先在第3龄低于CK、第4龄均显著低于CK(P < 0.05),后在第5龄不同程度地高于CK。表明用MeJA局部喷施能诱导提高长白落叶松的系统抗性,且其对食叶害虫具有广谱性,能干扰落叶松毛虫的解毒代谢,抵御其危害;落叶松毛虫能在逐渐适应后,通过提高保护酶和解毒酶的活性去响应诱导抗性造成的毒害。Abstract: In order to investigate the effects of exogenous methyl jasmonate on the detoxification metabolism of Dendrolimus superans larvae, three concentrations of methyl jasmonate (MeJA, 0.01, 0.10 and 1.00 mmol/L) were sprayed partially onto lateral branch of Larix olgensis seedlings; and the protective and detoxification enzyme activities of the 3rd-5th instars of Dendrolimus superans larvae that fed on these seedlings were analyzed. Our results showed that exogenous applications (partial sprays) of methyl jasmonate at three different concentrations on larch seedlings had significant effects on both the protective and detoxification enzyme activities of Dendrolimus superans larvae (P < 0.05) with similar trends, but were concentration-independent. The SOD and POD activities of the 4th instar larvae in each treatment group were significantly higher than those in CK (P < 0.05), but the differences were not significant for the 3rd and 5th instars (P>0.05). The ACP, AKP and GST activities of D. superans larvae in the MeJA treated groups were slightly lower than those in CK at the 3rd instar, and were significantly lower than those in CK at the 4th instar (P < 0.05), but were to some extent higher than those in CK at the 5th instar. The above results indicate that partially spraying exogenous methyl jasmonate can increase the induced systemic resistance of Larix olgensis against various defoliators, such as D. superans by disturbing its detoxification and metabolism mechanisms. However, D. superans larvae, in turn, might respond and even adapt to the induced systemic resistance of larch trees by quickly increasing the bio-activities of their protective and detoxification enzymes.
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Key words:
- methyl jasmonate /
- partially spraying /
- Larix olgensis /
- Dendrolimus superans
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图 1 MeJA局部处理长白落叶松对落叶松毛虫幼虫体内SOD活性的影响
数据标注均为平均值±标准差(n=3);同一龄期柱形图上,不同小写字母表示同一龄期不同局部处理浓度之间差异显著(P<0.05); MeJA0.01L、MeJA0.10L、MeJA1.00L分别表示MeJA局部喷施浓度为0.01、0.10和1.00 mmol/L。下同。
Figure 1. Effects of local spraying MeJA on the SOD activity of Dendrolimus superans larvae
Data in the figure are means±SD; different lowercase letters in the same age bar chart mean there is significant difference among varied local spraying concentrations in the same instar (P < 0.05). MeJA0.01L, MeJA0.10L and MeJA1.00L mean the local spraying concentrations of MeJA were 0.01, 0.10 and 1.00 mmol/L, respectively. The same below.
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