Effects of arbuscular mycorrhizal fungal colonization on Populus pseudo-cathayana × P. deltoides resistance to Lymantria dispar larvae
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摘要:目的
研究丛枝菌根真菌(AMF)对青山杨抗虫性的影响以及舞毒蛾对AMF定殖青山杨的适应能力,为AMF定殖青山杨后抗虫性的研究提供科学依据。
方法分别以对照(CK,无AMF定殖)、根内根孢囊霉(GI)或摩西管柄囊霉(GM)定殖的青山杨叶片饲喂舞毒蛾幼虫,统计3、4、5龄幼虫的体重、体长、头壳宽和食物利用率,测定4、5龄幼虫解毒酶酸性磷酸酯酶(ACP)和碱性磷酸酯酶(AKP)的活性。
结果GI组3、4龄幼虫的体重显著高于对照组(P < 0.05),5龄与对照组差异不显著,GM组5龄幼虫的体长、体重、头壳宽、食物利用率均显著高于对照组。GI组3龄幼虫取食量显著高于对照组(P < 0.05),4、5龄显著低于对照组,GM组5龄显著高于对照组,3、4龄与对照组差异不显著。GI组ACP显著低于对照组(P < 0.05),AKP在4龄显著高于对照组,5龄AKP活性显著低于对照组。GM组两种解毒酶活性均显著高于对照组。
结论GI定殖的青山杨能促进舞毒蛾低龄幼虫的生长,对舞毒蛾老熟幼虫的生长影响不显著。GM定殖青山杨叶片促进了舞毒蛾幼虫的生长发育,提高了食物的利用效率,激发了幼虫体内磷酸酯酶活性,表明舞毒蛾对GM定植的青山杨有更好的适应性。AMF对树木及植食性昆虫的影响具有种类特异性,GI定殖对青山杨的抗虫性的影响呈中性,GM定殖对青山杨的抗舞毒蛾产生负效应。
Abstract:ObjectiveThis paper explores the effects of arbuscular mycorrhizal fungi (AMF) on the resistance of Qingshan poplar (Populus pseudo-cathayana × P. deltoides) to the gypsy moth (Lymantria dispar) larvae and the adaptability of L. dispar larvae to the AMF colonization, so as to provide a scientific basis for the study of insect resistance of Qingshan poplar colonized by AMF.
MethodThe spongy moth larvae were fed with fresh leaves of Qingshan poplar seedlings, which were treated with Glomus intraradices or G. mosseae or untreated (CK: control). The body mass, length, head capsule width and food utilization of the 3rd, 4th and 5th instars of L. dispar larvae were measured, and the activities of acid phosphatase (ACP) and alkaline phosphatase (AKP) of the 4th and 5th instars of larvae were determined.
ResultThe body mass of the 3rd/4th instar larvae in GI group was significantly higher than that in the control group, but there was no significant difference in the body mass of the 5th instar larvae between the GI group and the control group. The body length, mass, head capsule width and food utilization of the 5th instar larvae in the GM group were significantly higher than those in the control group. Food intake of the 3rd instar larvae in the GI group was significantly higher than that in the control group, but the reverse was true for the 4th and 5th instars; the food intake of the 5th instar larvae in the GM group was significantly higher than that in the control group, but there was no significant difference in food intake of the 3rd and 4th instars between the GM group and the control group. The ACP activity of the 4th and 5th instars in the GI group was significantly lower than that in the control group, and AKP activity of the 4th instar in the GI group was significantly higher than that in the control group, whereas the reverse was true for the 5th instar. On the other hand, the activities of these two detoxifying enzymes in the GM group were significantly higher than those in the control group.
ConclusionThe GI treatment enhances the growth of younger (3rd and 4th instars) L. dispar larvae, but not that of the mature (5th instar) larvae. The GM treatment increases the growth and development of L. dispar larvae, improves their food utilization efficiency, and stimulates their phosphatase activity, indicating that the spongy moth larvae might have a better adaptability to the GM-colonized Qingshan poplar trees. The effects of AMF on trees and herbivorous insects seem to be species-specific. GI colonization doesn’t affect Qingshan poplar’s resistance to the insect, while GM colonization reduces Qingshan poplar’s resistance to the insect.
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丛枝菌根真菌(arbuscular mycorrhiza fungi,AMF)属于球囊菌门(Glomeromycata),能够与超过80%的陆地植物形成共生关系[1]。AMF从植物中吸收碳水化合物[2],反过来为植物提供磷酸盐、铵和微量营养素等矿物质[3]。AMF在改善植物生长发育的同时已逐渐应用于经济型农作物害虫的综合防治,并且取得了一定的防治效益[4]。除此之外,AMF定殖是否可以提高林木的抗虫性已成当前研究的热点。
AMF对植食性昆虫的影响存在3种情况,即正效应(约占45%)、负效应(35%)、变化不定和无影响(20%)[5]。例如:Wang等[6]发现摩西管柄囊霉(Glomus mosseae,GM)定殖的长叶车前草(Plantago lanceolata)已被证明可以抑制甜菜夜蛾(Spodoptera exigua)幼虫的相对生长速率,并且通过昆虫的植食作用改变梓醇在环烯醚萜苷水平中所占的比例;而Khaitov等[7]发现GM定殖的菜豆(Phaseolus vulgaris)提高了二斑叶螨(Tetranychus urticae)的繁殖率;Minton等[8]通过研究烟草天蛾(Manduca sexta)取食根内根孢囊霉(Glomus intraradices,GI)定殖的东方龙葵(Solanum ptycanthum)时发现烟草天蛾的体重与对照组无显著差异。菌根定殖对植物抗虫性影响的多态性可能与AMF的种类、昆虫的取食方式、食性广度、寄主植物种类、植物的营养与次生物质代谢等方面有关[9]。此外,昆虫对寄主植物的化学防御具有反防御机制。通常,昆虫在取食植物时会根据食物的质量调节自身的适应能力,尤其在取食一些不利于自身的食物时,其解毒机制被激活[10]。其中,磷酸酯酶可以分为酸性磷酸酯酶(acid phosphatases,ACP)和碱性磷酸酯酶(alkaline phosphatases,AKP),是一种广泛存在于昆虫体内的重要解毒酶,具有代谢一些杀虫剂,解毒部分外源物质的作用[11−12]。
青山杨(Populus pseudo-cathayana × P. deltoides)幼苗−舞毒蛾(Lymantria dispar)幼虫互作系统,由于青山杨幼苗的速生特性[13−14]和舞毒蛾幼虫的发育特性[15−16],是分析木本植物对昆虫抗性的极好模型。本研究以1年生青山杨和舞毒蛾幼虫为研究对象,对青山杨分别接种根内根孢囊霉(GI)和摩西管柄囊霉(GM),通过舞毒蛾幼虫的生长发育、食物利用和解毒酶活性分析GI或GM定殖对青山杨抗虫性的影响,进而为研究AMF对林业害虫的防治提供理论基础。
1. 材料与方法
1.1 试验材料与试剂
供试菌株:根内根孢囊霉(菌株号BJ09)和摩西管柄囊霉(菌株号GZ01A)(由甘肃省农业科学院提供)通过宿主玉米(Zea mays)和三叶草(Trifolium pratense)扩繁完成,菌剂中包含孢子、菌丝、根段和沙子,其中孢子含量15个/g。
供试植物:1年生青山杨扦插苗(为避免自然环境中菌根侵染样本植株干扰试验研究结果,故供试植物选择1年生青山杨扦插苗)。
供试土壤:草炭土、蛭石、沙子体积比为1∶1∶1,混合后在121 ℃下高压灭菌2 h。
供试昆虫:舞毒蛾卵块采自东北林业大学校园,饲料购自中国林业科学院森林生态环境与保护研究所。
供试试剂盒:总蛋白(TP)、酸性磷酸酯酶(ACP)、碱性磷酸酯酶(AKP)测定试剂盒购自南京建成生物工程研究所。
1.2 主要仪器与设备
高压蒸汽灭菌器,普和希株式会社生物医疗公司(MLS-3781L-PC);光照培养箱,东京理化器械株式会社(MTI-202B);电子分析天平,赛多利斯科学仪器有限公司(QYINTIX224-1CN);高速离心机,长沙湘智离心机仪器有限公司(TGL22M);电热恒温水浴锅,上海森信实验仪器有限公司(DK-S26);紫外可见光分光光度计,安玛西亚中国有限公司(ULtrospec5300pro)。
1.3 试验方法
1.3.1 杨树苗的培养及接菌处理
试验前将花盆用0.3%KMnO4溶液浸泡2 h进行消毒处理,每盆装入1.3 kg灭菌土壤,放置于东北林业大学育种苗圃温室。试验设置1个对照(CK)组和2个处理组,处理组分别接入丛枝菌根菌GI和GM,每1.3 kg土壤混入菌剂20 g,CK组不加菌剂。每盆移栽1株青山杨扦插苗,每组300盆,共计900盆,定期浇水除草。在开始饲喂昆虫前(青山杨扦插苗栽植80 d后),从每组随机各选取5株样树,每株至少选取50小段须根根样,根据Phillips等[17]方法测定菌根定殖率。
1.3.2 舞毒蛾幼虫饲养
舞毒蛾卵经10%甲醛溶液浸泡消毒,消除病毒的影响。置于恒温培养箱孵化,温度(25 ± 1) ℃,湿度为(70 ± 1)%,光周期16L∶8D(光照/黑暗时间为8 h/16 h)。待幼虫孵出后用人工饲料喂养至2龄[18]。将刚蜕皮的2龄幼虫分为3组,每组90头,分别摘取栽植80 d后的处理组和对照组叶片进行喂养,每2 d更换一次叶片,观察幼虫的生长发育状况。每组的3、4、5龄幼虫各取30头,测量其体重、体长、头壳宽。用电子分析天平称量每头幼虫体重,将幼虫放在1 mm网格纸上测定幼虫体长和头壳宽,并拍照保存图像。
1.3.3 舞毒蛾幼虫食物利用测定
在幼虫开始进入3龄、4龄、5龄时,分别从3组中各选取蜕皮不超过24 h的幼虫24头,并将每组所选的幼虫分为3个重复,继续用对应组的叶片饲养48 h,测定各重复组取食前鲜叶、取食后残叶和幼虫粪便的质量(湿质量);计算取食量、食物消耗率、转化率和利用率[19]。
I48=(mI−mF)/(1−L/mI) 式中:I48为48 h幼虫取食量,g;mI为取食前叶片鲜质量,g;mF为取食后叶片鲜质量,g; L为对照叶片失水量,g。
EAD=I48/mE×100% 式中:EAD为食物消耗率,%;mE为排粪质量,g。
ECI=(mBF−mBI)/(I48−mE)×100% 式中:ECI为食物转化率,%;mBF为取食后幼虫体重,g;mBI为取食前幼虫体重,g。
ECD=(mBF−mBI)/I48×100% 式中:ECD为食物利用率,%。
1.3.4 解毒酶活力测定
试验期间收集各处理组新蜕皮的4龄和5龄幼虫放置于−40 ℃冰箱备用。取3头相同处理的舞毒蛾同龄幼虫放置于玻璃匀浆器中,加入5 mL预冷的生理盐水(0.90%NaCl),在冰浴条件下充分研磨成匀浆后倒入10 mL离心管中,于4 ℃条件下10 000 r/min下离心10 min,上清液即为酶提取液[20]。采用试剂盒测定解毒酶ACP和AKP活力,每组测3个重复。酶液中组织蛋白含量采用总蛋白测定试剂盒(TP)进行测定。酶活计算公式:酸性磷酸酯酶(U/g) = (测定OD值/标准OD值) × 标准管含酚的量/(待测样本蛋白浓度 × 取样量);碱性磷酸酯酶(金氏单位/g) = (测定OD值/标准OD值) × 标准管含酚的量/(待测样本蛋白浓度 × 取样量)。
1.4 数据处理与分析
各龄期舞毒蛾图像使用Image J-v1.8.0软件测量体长和头壳宽,采用SPSS 19.0对舞毒蛾幼虫体重、体长、头壳宽、取食量、食物消耗率、食物转化率、食物利用率、ACP活性、AKP活性进行单因素方差分析,以LSD法进行多重比较。使用Excel 2016统计数据的平均值和标准误差并做图。
2. 结果与分析
2.1 青山杨根部GI和GM的定殖率
由图1可知AMF在青山杨根系中侵染定殖成功,图中可看到丛枝、泡囊和菌丝结构。在青山杨扦插苗栽植80 d后,其根部GI和GM定殖率如图2所示。GI定殖率为62.1%,GM定殖率为60.8%,未在CK组中检测到菌根定殖。
图 2 栽植80 d后青山杨扦插苗根部GI、GM的定殖率CK.对照;GI.根内根孢囊霉;GM.摩西管柄囊酶。不同小写字母表示不同处理之间差异显著(P < 0.05)。数据均为平均值 ± 标准差(n = 5)。下同。CK, control; GI, Glomus intraradices; GM, Glomus mosseae. Different lowercase letters indicate significant difference among varied groups (P < 0.05). The data annotation in the picture is average value ± SD (n = 5). The same below.Figure 2. Colonization rate of GI and GM at 80 d after planting2.2 GI、GM定殖青山杨对舞毒蛾幼虫体重的影响
舞毒蛾幼虫取食GI或GM定殖的青山杨叶片对其体重的影响如图3所示。3龄幼虫体重,GI和GM组均显著高于CK组(P < 0.05),同时GI组显著高于GM组(P < 0.05)。4龄幼虫体重,GI、GM组均显著高于CK组(P < 0.05),但GI组和GM组差异不显著(P > 0.05)。5龄幼虫体重,GI组与CK组差异不显著,GM组显著高于CK组(P < 0.05)。
图 3 各试验组舞毒蛾幼虫的体重数据均为平均值 ± 标准差(n = 30);不同小写字母表示同一龄期不同组之间差异显著(P < 0.05)。下同。 The data annotation in the picture is average value ± SD (n = 30); different lowercase letters indicate that there is significant difference among different groups at the same age (P < 0.05). The same below.Figure 3. Larvae body mass of spongy moth in each treatment group2.3 GI、GM定殖青山杨对舞毒蛾幼虫体长和头壳宽的影响
舞毒蛾幼虫取食GI或GM定殖的青山杨叶片对其体长和头壳宽的影响分别见图4和图5。3龄幼虫体长,GI组显著高于CK组和GM组(P < 0.05),GM组与CK差异不显著(P > 0.05)。4龄幼虫体长各组之间均不显著(P > 0.05)。5龄幼虫体长,GI组与CK组差异不显著(P > 0.05),GM组显著高于CK组和GI组(P < 0.05)。3龄幼虫头壳宽,GI组显著高于CK组和GM组(P < 0.05),GM组与CK差异不显著(P > 0.05)。4龄GI组与CK组和GM组差异均不显著(P > 0.05),GM组显著高于CK组(P < 0.05),5龄GI组和CK组差异不显著(P > 0.05),GM组显著高于CK组和GI组(P < 0.05)。
2.4 GI、GM定殖青山杨对舞毒蛾幼虫取食量的影响
GI或GM定殖的青山杨叶片对舞毒蛾幼虫取食量的影响如图6所示。3龄幼虫取食量,GI组显著高于CK组(P < 0.05),GM组与CK组和GI组差异均不显著(P > 0.05);4龄幼虫取食量,GI组显著低于CK组和GM组(P < 0.05),GM组与CK组差异不显著(P > 0.05)。5龄幼虫取食量,GI组显著低于CK组和GM组(P < 0.05),GM组显著高于CK组(P < 0.05)。
2.5 GI、GM定殖青山杨对舞毒蛾幼虫食物消耗率的影响
取食GI或GM处理的青山杨叶片对舞毒蛾幼虫食物消耗率的影响如图7所示。3龄幼虫食物消耗率,GI组显著高于GM组和CK组(P < 0.05),GM组与CK组差异不显著(P > 0.05);4龄幼虫食物消耗率,GI组与CK组差异不显著(P > 0.05),GM组显著高于CK组和GI组(P < 0.05);5龄幼虫食物消耗率,各处理组间差异均不显著(P > 0.05)。
2.6 GI、GM定殖青山杨对舞毒蛾幼虫食物转化率的影响
取食GI或GM定殖的青山杨叶片对舞毒蛾幼虫食物转化率的影响如图8所示。3龄幼虫食物转化率,GI组与CK组差异不显著(P > 0.05),GM组显著高于GI组与CK组(P < 0.05);4龄幼虫食物转化率各处理组和对照组差异均不显著(P > 0.05);5龄幼虫食物转化率,GI组与CK组和GM组差异均不显著(P > 0.05),GM组显著高于CK组(P < 0.05)。
2.7 GI、GM定殖青山杨叶片对舞毒蛾幼虫食物利用率的影响
取食GI或GM定殖的青山杨叶片对舞毒蛾幼虫食物利用率的影响如图9所示。GI组食物利用率,3龄时显著高于CK组(P < 0.05),4龄和5龄时GI组和CK组食物利用率差异不显著(P > 0.05)。GM组食物利用率,3龄、4龄显著高于CK组和GI组(P < 0.05),5龄显著高于CK组(P < 0.05),与GI组差异不显著(P > 0.05)。
2.8 GI、GM定殖青山杨对舞毒蛾幼虫ACP和AKP酶活性的影响
舞毒蛾幼虫取食GI或GM定殖的青山杨对其ACP和AKP的影响如图10和图11所示。ACP活性,4龄和5龄幼虫GI组显著低于CK组和GM组(P < 0.05),GM组显著高于CK组(P < 0.05)。AKP活性,4龄幼虫GI组显著高于CK组(P < 0.05),GM组显著高于CK组和GI组(P < 0.05);5龄幼虫GI组显著低于CK组(P < 0.05),GM组显著高于CK组和GI组(P < 0.05)。
3. 结论与讨论
菌根定殖下植物对植食性昆虫的生长影响不尽相同[21−22]。本研究GI定殖的青山杨对舞毒蛾幼虫的生长发育影响呈阶段特异性,表现为:在3、4龄时呈促进作用,5龄呈中性作用。而GM定殖的青山杨对舞毒蛾幼虫的生长发育表现出一种促进效应,表现为:体重、取食量增加,食物转化率、食物利用率提高。这表明植物对昆虫的生长受菌根的种类特异性影响。
食物消耗率、食物转换率、食物利用率是表示植食性昆虫对寄主植物取食利用效率的重要营养参数[23]。菌根定殖可能通过改变植物的物质代谢影响昆虫的食物利用。Selvaraj等[24]发现,接种GI的黑吉豆(Vigna mungo)降低了斜纹夜蛾(Spodoptera litura)的食物转化率与食物利用效率,抑制了幼虫的生长。这与我们的发现不同,本研究中GM组舞毒蛾幼虫食物转化率、食物利用率显著提高,这与其体重增长趋势一致,舞毒蛾幼虫生长受到促进的原因可能是GM提高了青山杨叶片的营养,增强了舞毒蛾幼虫的嗜食性。而在GI定殖下的青山杨对舞毒蛾4、5龄幼虫的食物利用和生长表现出一种中性效应,这就凸显了菌根定殖植物后对植食性昆虫影响的特异性。
目前,大量研究指出,在多种植食性昆虫中,ACP、AKP活性的增强对于提高昆虫应对胁迫压力的能力至关重要[25−26]。姜礅[27]研究发现,在Zn胁迫下,4龄和5龄舞毒蛾幼虫体内的ACP、AKP活性均显著高于对照,发育历期没有被延长,解毒酶ACP和AKP能积极响应舞毒蛾幼虫抵御Zn的胁迫。本研究发现,GI组幼虫ACP活性受到抑制,AKP活性在4龄时高于对照但在5龄时AKP低于对照,这可能是GI组幼虫生长发育在4龄后不再显著增长的原因。GM组幼虫ACP与AKP活性均得到显著促进且幼虫生长发育良好,说明舞毒蛾幼虫体内的解毒酶能积极响应取食接种GM的青山杨后的解毒过程。
同样的菌种对不同树种抗虫性的影响也呈不同的趋势。武帅[28]研究了GI和GM分别定殖银中杨(Populus alba × P. berolinensis)后对舞毒蛾的影响,结果发现:GI和GM均能提高银中杨叶片的防御蛋白活性和次生代谢物含量,但对舞毒蛾的影响却不相同,GI定殖对舞毒蛾的生长发育有促进作用,而GM定殖则抑制了舞毒蛾的生长与取食。而在本研究中,GI定殖对青山杨的抗虫性起中性作用;GM定殖降低了青山杨的抗虫性。表明AMF对植物和植食性昆虫的影响具有种类特异性。本研究结果为今后针对不同树种的AMF菌种选择和植食性昆虫生态防治提供了理论依据。
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图 2 栽植80 d后青山杨扦插苗根部GI、GM的定殖率
CK.对照;GI.根内根孢囊霉;GM.摩西管柄囊酶。不同小写字母表示不同处理之间差异显著(P < 0.05)。数据均为平均值 ± 标准差(n = 5)。下同。CK, control; GI, Glomus intraradices; GM, Glomus mosseae. Different lowercase letters indicate significant difference among varied groups (P < 0.05). The data annotation in the picture is average value ± SD (n = 5). The same below.
Figure 2. Colonization rate of GI and GM at 80 d after planting
图 3 各试验组舞毒蛾幼虫的体重
数据均为平均值 ± 标准差(n = 30);不同小写字母表示同一龄期不同组之间差异显著(P < 0.05)。下同。 The data annotation in the picture is average value ± SD (n = 30); different lowercase letters indicate that there is significant difference among different groups at the same age (P < 0.05). The same below.
Figure 3. Larvae body mass of spongy moth in each treatment group
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