挥发性化合物介导的植物-植食性昆虫-天敌三级营养级互作机制及应用

2021-05-07王冰李慧敏操海群王桂荣

中国农业科学 2021年8期

王冰，李慧敏,，操海群，王桂荣

王冰1，李慧敏1,2，操海群2，王桂荣1

1中国农业科学院植物保护研究所植物病虫害生物学国家重点实验室，北京 100193；2安徽农业大学植物保护学院，合肥 230036

农业生态系统中植物-植食性昆虫-天敌三级营养级间存在复杂的互作关系，挥发性化合物在三级营养级互作中发挥着重要作用。植食性昆虫能够以植物挥发物为化学线索精准地识别和定位寄主，而虫害诱导的挥发物作为关键的化学信息物质对于调控三级营养级关系起到不可或缺的作用，一直是该领域研究的重点和热点问题。另外，植物为传粉昆虫提供花粉或者花蜜，传粉昆虫可以通过识别花中挥发物寻找食物来源，在帮助植物传粉的同时有利于自身的生长发育与繁殖。近40年来，随着传统化学生态学研究的不断深入，特别是化学分析手段和灵敏度的不断提高以及电生理研究技术的广泛渗入，新的研究理念、研究手段快速形成与发展。在三级营养级互作的过程中，昆虫化学感受基因参与了对挥发性化合物的识别。因此，对昆虫化学感受基因的挖掘与功能鉴定将有助于解析昆虫化学感受的分子机制，研发更高效的昆虫行为调控产品并科学合理地应用于农业害虫的绿色防控，对于农田生态环境的保护具有十分重要的意义。本文综述了挥发性化合物对植食性昆虫、天敌昆虫与传粉昆虫行为的影响，详述了挥发物介导的三级营养级之间的互作机制与研究现状，以及在害虫绿色防控中的应用，并对未来重点研究的问题进行了展望。

虫害诱导的挥发物；植食性昆虫；天敌昆虫；三级营养级互作；传粉昆虫；气味受体

1980年，PRICE等[1]提出了植物-植食性昆虫-天敌昆虫三级营养级互作的理论，揭示了植物对植食性昆虫和天敌昆虫之间具有直接或间接、积极或消极等多方面影响。在错综复杂的信息网中，化学信息调节三者之间的相互作用以及相互影响，是昆虫与昆虫、昆虫与植物、甚至植物与植物之间特殊的“语言”，是农田生态系统的重要组成部分[2-4]。近40年来，随着传统化学生态学研究的不断深入，特别是化学分析手段和灵敏度的不断提高以及电生理研究技术的广泛渗入，新的研究理念、研究手段快速形成与发展[5-6]，使得三级营养级关系之间的化学“语言”逐渐被破译，如利马豆（）-二斑叶螨（）-智利小植绥螨（）[7-8]；番茄（）-美洲棉铃虫（）-短管赤眼蜂（）[9]等一些研究进展极大地推动了三级营养级关系在化学生态领域中的认知。本文对挥发性化合物介导的植食性昆虫、天敌昆虫与传粉昆虫行为的影响进行了综述，对挥发物在三级营养级之间的互作机制、研究现状及其应用进行了归纳与总结，以期为昆虫行为调控产品的研发以及害虫的绿色防控提供一定的借鉴作用和理论指导。

1 化学线索调控昆虫行为选择

在健康植物的生长发育过程中，植物能够持续不断地释放大量的挥发物，植食性昆虫能够以植物挥发物为化学线索，远距离识别和定位寄主，这不仅满足了植食性昆虫自身的营养需求，而且为寻找合适的产卵场所提供了必要条件[10-12]。当植物受到植食性昆虫或病原菌危害和侵袭后，会形成一定的防御机制来应对各种伤害。虫害诱导的植物挥发物（herbivore- induced plant volatile，HIPV）是一种特殊的植物“语言”，可以向植食性昆虫传递“警告”信号，亦可以向天敌昆虫发出“求救”信号，同时“告诫”临近植株危险的到来[2,13-14]。HIPV主要包括萜烯类化合物和绿叶挥发物（green leaf volatile，GLV），还包括少量的含氮、含硫化合物[15-17]。此外，昆虫种间和种内信息素对于同种或异种昆虫行为选择有一定的影响，尤其是植食性昆虫挥发物作为重要的化学线索影响着天敌昆虫的寄主定位。这些化学信号参与调控植物-植食性昆虫-天敌昆虫三级营养级关系之间的生态平衡。

1.1 植物挥发物对植食性昆虫的影响

植物挥发物对于植食性昆虫搜寻和定位寄主、产卵以及寻找配偶等生命活动具有重要意义[10,18]。在鳞翅目昆虫中已开展了系统的研究。例如，苹果蠹蛾（）幼虫能识别成熟的西洋梨（）释放的挥发物（反式）--法尼烯、（反式）-2-（顺式）-4-癸二烯酸甲酯、（反式）-2-（顺式）-4-癸二烯酸乙酯，并在行为上表现出明显的偏好性[19]。油菜（）的挥发物异硫氰酸烯丙酯、2, 5-己二醇、异戊酸叶醇酯、（顺式）-3-甲基丁酸-3-己烯酯不仅能强烈地激活小菜蛾（）触角的EAG反应，还能引起小菜蛾的定向飞行和着陆行为[20]。有研究显示，（顺式）-茉莉酮和1-戊醇是吸引棉铃虫（）幼虫的关键成分[21]。“Y”型嗅觉仪试验表明，烟草植物挥发物乙酸香叶酯对烟青虫（）雌蛾有显著的吸引作用，橙花叔醇能显著地吸引雌、雄蛾[22]。由此可见，寄主植物挥发物在鳞翅目昆虫定位寄主的过程中发挥着关键作用。

另外，一些特定寄主植物挥发物对鞘翅目、半翅目和双翅目等昆虫也具有引诱作用。例如蓝桉树（）植物挥发物莰烯、（+）--蒎烯和苯乙醇能够显著地吸引鞘翅目昆虫普来特象鼻虫（）[23]。芸香科植物挥发物-石竹烯、-石竹烯和（1）-（+）--蒎烯能显著地吸引半翅目昆虫柑橘木虱（）成虫[24-25]。葱属（）植物和侧耳属（）植物共有的挥发物柠檬烯对双翅目昆虫韭菜迟眼蕈蚊（）的3龄幼虫以及雌成虫具有显著的引诱作用[26]。

不同植食性昆虫对同种植物挥发物的行为反应存在着差异。以1-辛烯-3-醇对多种双翅目昆虫的作用为例，研究显示1-辛烯-3-醇对橘小实蝇（）雄蝇具有驱避作用，但是对已交配的雌虫却具有显著的引诱作用[27]。另外，1-辛烯-3-醇能增加斑翅果蝇（）的搜寻时间并降低雌蝇产卵量[28]。来源于蘑菇、三叶草以及牛呼吸气流中的1-辛烯-3-醇能够吸引按蚊属（）和伊蚊属（）的蚊类，但是对致倦库蚊（）却有显著的驱避作用[29-30]。寄主植物挥发物己醛、甲基丙基二硫醚、1-辛烯-3-醇对韭菜迟眼蕈蚊的3龄幼虫以及雌成虫具有驱避作用[26]。

在农田生态系统中，植食性昆虫往往通过对植物“化学语言”不同编码方式的识别而选择和定位寄主植物。多种化合物在环境空间中的组成决定了昆虫对植物的偏好性选择程度。例如，（顺式）-3-己烯醇、正己醇、苯甲醛、（反式）--法尼烯、水杨酸甲酯等15种蚕豆（）植株挥发物的混合物能够显著吸引蚕豆蚜（）[31]。另外，具有特定比例的混合物比单一组分更能引起昆虫强烈的定向行为。研究显示成熟芒果（）挥发物组分乙醇、醋酸和苯乙醇以1﹕22﹕5的比例混合比单一组分对黑腹果蝇（）的引诱作用更强[32]。以100﹕78﹕9比例混合的葡萄（）挥发物（反式）--石竹烯、4, 8-二甲基-1, 3, 7-壬三烯（DMNT）和（反式）--法尼烯能强烈地吸引葡萄花翅小卷蛾（），缺少其中的任何一种都会失去引诱效果[33-34]。麦麸发酵物棕榈酸乙酯、亚油酸乙酯、亚油酸甲酯和亚油酸以10﹕24﹕6﹕0.2的比例混合对家蝇（）的引诱效果显著高于单一组分，并显著提高产卵量[35]。因此，具有特定比例的混合物对于鳞翅目、鞘翅目、双翅目等多种植食性昆虫的搜寻、定位、产卵等生命活动具有重要意义，可为开发害虫引诱剂提供一定的理论参考。

1.2 虫害诱导的植物挥发物（HIPV）对昆虫的影响

1.2.1 植物的防御机制以及对植食性昆虫的影响在植物的生长周期中，经常受到大量植食性昆虫的危害。因此，植物在长期的进化过程中形成了多种高效的防御途径[36-39]，包括水杨酸（salicylic acid，SA）、茉莉酸（jasmonic acid，JA）、乙烯（ethene，ETH）等植物激素调节的信号转导途径[40-44]。植食性昆虫取食以及产卵等行为会诱导植物产生HIPV，是植物应对外来侵害的一种防御策略[2,13-14,45]。研究表明HIPV能够增强植物对植食性昆虫的防御反应。例如，草地贪夜蛾（）取食水稻（）释放挥发物吲哚能诱导未被取食的组织中丝裂原活化蛋白激酶OsMPK3的转运、积累和活化，增强以及多个茉莉酸合成基因的转录，而茉莉酸信号传导有利于植物防御，该研究解析了吲哚增强水稻对草地贪夜蛾防御反应的作用模式[17]。类似地，甜菜夜蛾（）危害玉米植株释放的绿叶挥发物（顺式）-3-己烯乙酸酯也能增加玉米植株茉莉酸的合成，从而启动植物对植食性昆虫的防御[16]。另外，昆虫的挥发物也能影响植物的防御反应。例如，双翅目秋麒麟瘿蝇（）雄虫释放的主要挥发物混合成分螺结缩长时间处理北美一枝黄花（），诱导黄花关键防御激素茉莉酸水平的增加，从而增强植物防御反应，降低对怀卵雌虫的吸引[46]。地下环境中生存的昆虫病原线虫挥发物苯甲醛、苯甲醇、苯乙酮、壬醛和吲哚能够促进植物的防御反应并且影响植食性昆虫的行为。研究显示昆虫病原线虫挥发物能够减少地上部植食性昆虫马铃薯甲虫（）幼虫对马铃薯叶片的取食，并且抑制马铃薯甲虫雌虫的产卵行为，这主要是由于马铃薯植株经过昆虫病原线虫挥发物的诱导后能产生更高水平的水杨酸和茉莉酸，从而使植株产生防御反应[47]。有些植食性昆虫利用HIPV操纵植物的防御反应，更适于自身的繁衍。研究显示烟粉虱（）诱导的马铃薯植物挥发物-月桂烯或-石竹烯能抑制临近植株的水杨酸防御途径，使临近植株更适于烟粉虱的生长发育[48]。地下害虫红胸律点跳甲（）幼虫取食乌桕（），释放2-乙基己醇和壬醛能吸引同种成虫取食地上部分的叶片，根部酚类次生防御物质含量降低，从而有利于幼虫的生长发育[49]。

植食性昆虫识别HIPV后，“推断”寄主植物的适生情况以及是否存在竞争者，从而表现出一定的行为反馈[50]。为了提高同种后代的存活率，降低后代生存竞争，植食性昆虫往往会避免在已被危害的植物上定殖或产卵。例如，烟芽夜蛾（）雌蛾通过识别烟草（）在夜间释放的（顺式）-3-己烯丁酸、（顺式）-3-己烯乙酸酯等多种绿叶挥发物的混合物从而产生驱避行为，并且避免在植株上产卵[51]。类似地，海灰翅夜蛾（）取食棉花后，诱导的挥发物DMNT能抑制同种害虫对性信息素的选择，从而影响交配和产卵行为[52]。

VEYRAT等[53]研究表明，虫害诱导的玉米植株挥发物吲哚能提高海灰翅夜蛾幼虫的死亡率并降低其取食量，驱避雌成虫产卵，从而达到直接防御的作用。此外，虫害诱导的植物挥发物法尼烯的同分异构体（反式，反式）--法尼烯（49%）、（反式）--法尼烯（26%）、（顺式）--法尼烯（18%）以及（顺式，反式）--法尼烯（7%）能显著地抑制烟青虫雌虫的产卵行为[54]。虫害诱导的玉米植株挥发物（反式）--法尼烯对玉米蚜（）具有显著的驱避作用[55]。麦长管蚜（）危害小麦释放的3种诱导挥发物6-甲基-5-庚烯-2-酮、6-甲基-5-庚烯-2-醇和水杨酸甲酯对有翅蚜具有较好的驱避效果[56]。茶尺蠖（）幼虫取食后诱导的茶树挥发物苄腈和芳樟醇对同种未交配的雌、雄成虫具有显著的驱避作用[57]。HIPV对同一生态位的异种植食性昆虫也会产生一定的影响。例如，烟芽夜蛾危害烟草植株能诱导释放大量的烟碱，对同一植株上的西花蓟马（）产生忌避作用[58]。HIPV对某些植食性昆虫具有驱避作用是植物在长期的进化过程中产生的自身防御反应，以减少植食性昆虫的危害。

1.2.2 HIPV对天敌昆虫行为的影响植株被植食性昆虫危害后能产生一系列自身防御反应，释放多种诱导挥发物作为利他素以吸引植食性昆虫的自然天敌，从而间接地调控生态系统的组成结构[2,59-61]。最早报道的有关植物利用HIPV吸引天敌的证据显示，二斑叶螨危害利马豆释放的DMNT能吸引天敌智利小植绥螨[60,62]，从而形成间接防御。随着研究的深入，越来越多证据表明HIPV能够远距离地吸引植食性昆虫的天敌，尤其是寄生性天敌昆虫，研究较多的是鳞翅目昆虫危害玉米产生的HIPV对寄生蜂行为的影响。例如，甜菜夜蛾幼虫危害玉米植株释放的（顺式）-3-己烯乙酸酯、（顺式）-3-己烯醇和芳樟醇等11种虫害诱导的混合挥发物，对幼虫寄生蜂缘腹盘绒茧蜂（）有显著的引诱作用[63]。草地贪夜蛾取食玉米植株1—2 h后，释放的绿叶挥发物（顺式）-3-己烯醛、（反式）-2-己烯醛、（反式）-3-己烯醇和（顺式）-3-己烯乙酸酯与少量单萜芳樟醇和-月桂烯混合显著地吸引卵寄生蜂短管赤眼蜂，而危害玉米12 h后的植株却失去了对短管赤眼蜂的引诱作用，表明该寄生蜂更易被新鲜伤口产生的挥发物所吸引[64]。此外，草地贪夜蛾危害玉米产生的-蒎烯和-古巴烯的混合物对卵寄生蜂岛甲腹茧蜂（）有极显著的引诱作用，是主要的活性成分[65]。由此可见，虫害诱导的玉米植株挥发物通过不同活性成分的组合模式能吸引多种寄生蜂前来定位猎物的幼虫或卵，从而发挥生物控害的效果。

HIPV对害虫的间接防御作用具有普遍性。“Y”型嗅觉仪试验显示，棉铃虫幼虫危害反枝苋（）诱导产生的植物挥发物6-甲基-5-庚烯-2-酮和-榄香烯可以显著地吸引雌性中红侧沟茧蜂（），有利于棉铃虫绿色防控产品的开发与应用[66]。半翅目昆虫红圆蚧（）危害柑橘后诱导产生的D-柠檬烯和-罗勒烯是吸引天敌昆虫印巴黄蚜小蜂（）的主要化合物，在红圆蚧的生物防治中发挥着重要作用[67]。已有的研究表明植物防御过程中产生的萜烯类化合物DMNT和TMTT是天敌昆虫重要的利他素，利用转基因的方法使水稻释放DMNT和TMTT能显著地吸引水稻害虫的天敌二化螟绒茧蜂（），起到对害虫的间接防御作用，为培育新型抗虫品种提供了新思路[68]。

捕食性天敌昆虫同样能够识别环境中的多种HIPV，从而快速定位猎物。有研究显示，麦长管蚜危害小麦诱导产生的（顺式）-3-己烯乙酸酯对黑带食蚜蝇（）具有显著的引诱作用，水杨酸甲酯能够特异性地吸引异色瓢虫（），这些化合物在调控麦长管蚜的种群消长中发挥着重要作用[69]。单一或混合组分的HIPV对不同种天敌昆虫的引诱效果存在差异。例如，田间试验结果表明虫害诱导挥发物罗勒烯对四条小食蚜蝇（）具有明显的引诱作用[70]，嗅觉行为试验显示低浓度的单一组分水杨酸甲酯能够显著地吸引对多异瓢虫（）[71]。单一组分（顺式）-3-己烯乙酸酯对七星瓢虫（）具有引诱作用[70]。而（顺式）-3-己烯乙酸酯和水杨酸甲酯的混合物比单一组分对食螨瓢虫（）的引诱作用更强[72]。杂食性天敌昆虫矮小长脊盲蝽（）能够识别桃蚜（）取食茄子叶片产生的（反式）--法尼烯和TMTT等HIPV的混合物，从而偏好性地选择有蚜虫定殖的茄子植株[73]。

植物地上部分HIPV可以吸引捕食性或寄生性天敌昆虫寻找猎物，植物地下根系分泌的化学信息素也能吸引天敌，从而定位寄主。有研究显示昆虫病原线虫能识别玉米根萤叶甲（）幼虫危害玉米根部释放的（反式）--石竹烯，对这种化学线索识别的特异性使其精准定位猎物[74]。

1.3 花的挥发物参与昆虫行为调控

植物与传粉昆虫之间的相互作用在维持大多数陆地生态系统功能完整性中发挥着重要作用[75]。大约75%的农作物种类以及88%的开花植物都需要传粉昆虫授粉从而增加作物产量[76-78]。反之，植物为传粉昆虫提供花粉或花蜜，传粉昆虫可以通过识别花中挥发物寻找食物来源，在帮助植物传粉的同时有利于传粉昆虫自身的生长发育与繁殖[79-81]。花的挥发物是吸引传粉昆虫的重要化学信号。为了研究花香的演变与昆虫化学交流的关联性，SCHIESTL[82]分析了来源于96种植物和87种昆虫中的71种最常见的花香挥发性有机化合物的发生、共性和进化模式，研究显示植物和昆虫产生的挥发性有机化合物有87%的重叠，其中芳香族化合物在被子植物中进化出信号功能，主要用于吸引传粉媒介。

传粉昆虫的嗅觉系统在识别花挥发物的过程中发挥着重要作用[83-84]。花的挥发物由花的不同结构和部位散发，传粉昆虫可以通过识别挥发物差异定位花的不同部位。在无花蜜的植物中，花药是植物提供给访花昆虫的主要报偿。SOLÍS-MONTERO等[81]研究表明，刺萼龙葵（）传粉型花药挥发物丁香酚、-古巴烯和甲基丁香酚，以及取食型花药挥发物苯甲酸甲酯、苯甲酸乙酯、（反式）--法尼烯、-癸内酯和（反式）-金合欢醇均能显著地吸引东方熊蜂（）前来访花，选择行为试验表明东方熊峰更加偏好选择取食型花药。另外，研究发现刺萼龙葵取食型花药和传粉型花药的挥发物均能引起一种麦蜂（）的触角电位反应[81]。有研究表明菊科植物丝路蓟（）花的挥发物苯乙醛、水杨酸甲酯、2-甲氧基苯甲酸甲酯是引起黑带食蚜蝇触角电位反应的主要成分[83]。田间调查试验表明，神后鸢尾（）主要的传粉昆虫为熊蜂（）和意大利蜜蜂（），其次为黑带食蚜蝇。神后鸢尾花的挥发物以1, 4-对苯二甲醚、苯乙醇和2-甲氧基苯甲醛等芳香化合物为主，推测是吸引传粉昆虫前来取食和访花的主要化学线索[85]。此外，蜜蜂和食蚜蝇等传粉昆虫在柠檬烯释放量较高的甜叶菊（）上访问数量最多[86]。牡丹草属植物花的挥发物主要为烃类化合物、脂肪酸、长链的醇、醛类和少量芳香族化合物，能够吸引双翅目、膜翅目和鞘翅目昆虫[77]。另外，花挥发物也能吸引夜行性访花昆虫。比如，含有芳樟醇和（反式）--罗勒烯等巴西香可可（）花挥发物的混合物能吸引夜行性传粉昆虫隧蜂（）[87]。夜行性盲蝽（）能识别花挥发物（顺式）-茉莉酮，从而定位寄主万年青属植物，并将其作为取食和交配场所[88]。另外，花挥发物也能引起一些植食性昆虫的电生理反应或行为反应。例如，大叶醉鱼草（）的花挥发物苯甲醛、茶香酮、2, 2, 6-三甲基-1, 4-环己二酮、氧化异佛尔酮、（反式，反式）--法尼烯等能引起甘蓝尺蠖（）的触角电位反应[89]。诱捕试验表明，花挥发的混合物-月桂烯与苯乙醛能显著地吸引大豆尺蠖（）[90]。

一些植物可以通过模拟并释放昆虫的信息素组分吸引传粉昆虫，从而增加植物自身的传粉。疏花火烧兰（）可以挥发一些类似于蚜虫报警信息素组分的萜烯类化合物，例如-蒎烯、-蒎烯、-月桂烯和-水芹烯等利他素，从而吸引黑带食蚜蝇前来产卵，有助于为其传粉[91-93]。澳大利亚兰花（）可以释放一种与雌性黄蜂（）性信息素组分2-乙基-5-丙基-1, 3-环己二酮相同的化合物以吸引传粉昆虫授粉[94-95]。在长期进化过程中，植物发展的这种“欺骗”行为有助于自身的生存和繁衍。

开花植物释放的化合物具有动态节律性[96-97]。花的个体发育阶段以及花性别差异导致其释放的挥发物对传粉昆虫和植食性访花昆虫的引诱作用也存在一定的分化。THEIS等研究发现雌雄异株的丝路蓟雄蕊和雌蕊花的挥发物在开花初期和花期均以芳香族化合物为主，但是雄蕊花大多吸引鞘翅目金龟甲和半翅目盲蝽等植食性访花昆虫，而雌蕊花大多吸引蜜蜂和集蜂科的传粉昆虫。而雌雄同株的美洲近缘种蓟属植物同样在开花初期和花期大量释放芳香族化合物，对植食性访花昆虫和传粉昆虫均具有引诱作用，其中对凤蝶等传粉昆虫的引诱效果最好。无论是雌雄异株的丝路蓟还是雌雄同株的在开花末期单萜的释放量显著提高，但对访花昆虫的引诱作用明显下降[98]。ZHOU等揭示了渐狭叶烟草（）的花在夜间释放的挥发物（反式）--香柠檬烯吸引烟草天蛾（）成虫进行传粉，而日间烟草的叶片释放的同一化合物作为一种HIPV用于吸引烟草天蛾幼虫的天敌，这种植物挥发物释放的时空变化策略有助于解决同为传粉昆虫和植食性害虫的困境，同时为传粉昆虫和植食性昆虫对花香信号与植物防御之间形成的协同进化机制提供了遗传证据[99]。植物繁殖方式不同也影响植物对传粉昆虫的吸引。HABER等研究表明，远亲繁殖的玄参科植物猴面花（）挥发物中的一个关键组分（反式）--香柑油烯的释放量显著高于近亲繁殖的量，传粉昆虫东方熊蜂能够识别这种释放量的差异对远亲繁殖的种类完成授粉过程[100]。因此，花挥发物的来源、植物繁殖类型、花的个体发育阶段与花性别差异在访花昆虫与植物互作中都发挥着重要作用。

1.4 植食性昆虫与天敌之间的化学联系

天敌昆虫可以通过植食性昆虫挥发物以及性信息素组分等化学线索寻找和定位猎物[101]。具有代表性的案例是蚜虫天敌对蚜虫蜜露挥发物和蚜虫报警信息素等化学线索的精准识别。LEROY等研究表明，巢菜修尾蚜（）蜜露挥发物3-羟基-2-丁酮、3-甲基-2-丁烯醛、3-甲基-1-丁醇和柠檬烯可以显著地吸引七星瓢虫[102]，这些化合物的鉴定为巢菜修尾蚜的生物防治提供了重要的化学线索。另一研究显示蚜虫报警信息素（反式）--法尼烯能被黑带食蚜蝇识别并诱导产卵行为[103-104]。周氏啮小蜂（）是一种寄生在美国白蛾（）蛹中的内寄生蜂，“Y”型嗅觉仪试验表明美国白蛾蛹的挥发物1-十二烯能引起已交配的周氏啮小蜂强烈的定向选择，这一结果为揭示蛹寄生机制提供了分子依据[105]。

另外，植食性昆虫释放的性信息素可以作为天敌昆虫定位寄主的重要化学线索[106-107]。例如雌性麦蛾茧蜂（）能识别雄性寄主大蜡螟（）释放的性信息素混合物壬醛和十一醛，并以此作为寻找产卵场所的直接线索[108]。ZHU等研究表明豌豆蚜（）性信息素组分（1R, 4aS, 7S, 7aR）-荆芥醇能够显著吸引金眼草蛉（）成虫，有利于其迅速定位猎物[109-110]。由此可见，天敌昆虫对于植食性昆虫释放的化学线索的识别具有普遍性和特异性，然而目前对于识别的分子机制并不十分清楚。

2 昆虫化学感受基因参与化学线索的识别

随着转录组和基因组等测序技术的飞速发展，研究人员已经鉴定出大量的昆虫化学感受基因。主要的嗅觉基因包括气味结合蛋白（odorant binding protein，OBP）、化学感受蛋白（chemosensory protein，CSP）、气味受体（odorant receptor，OR）、离子型受体（ionotropic receptor，IR）、感觉神经元膜蛋白（sensory neuron membrane protein，SNMP）等，参与了外周嗅觉系统信号的转导[111-112]。外部气味分子通过触角极孔进入感器淋巴液，通过气味结合蛋白将其运输至神经元树突膜后，释放气味分子的同时激活气味受体，将化学信号转变为电信号并传递到更高级的神经中枢，从而指导昆虫行为[113-114]。在这个过程中，气味结合蛋白和气味受体的功能获得了广泛的研究，为解析昆虫触角外周神经系统嗅觉识别的分子机制奠定了基础。

2.1 气味结合蛋白参与化学线索的识别

气味结合蛋白联系着气味受体与气味分子之间的相互作用。目前，通过转录组或者基因组测序已经鉴定了包括鳞翅目、双翅目、鞘翅目、半翅目[115-121]等许多种植食性昆虫的气味结合蛋白基因。其中，对在鳞翅目昆虫中较为保守的性信息素结合蛋白（pheromone binding protein，PBP）和普通气味结合蛋白（general odorant binding protein，GOBP）的功能已经开展了广泛的研究[122-128]。例如桃小食心虫（）的性信息素结合蛋白CsasPBP3能特异性结合两种性信息素成分（顺式）-7-二十烯-11-酮和（顺式）-7-十九烯-11-酮，而普通气味结合蛋白CsasGOBP1对这两种信息素组分结合力最强，同时也能结合植物挥发物，CsasGOBP2偏好结合植物挥发物，表明CsasPBP和CsasGOBP分别在识别性信息素和寄主植物挥发物的过程中发挥着不同的作用[129]。有研究显示，经典的气味结合蛋白也能结合性信息素组分，例如甜菜夜蛾的SexiOBP7除了可以结合苯乙酮和金合欢醇等寄主植物挥发物以外，对甜菜夜蛾的主要性信息素组分（顺式，反式）-9, 12-十四碳二烯醇醋酸酯的结合能力最好，推测SexiOBP7可能参与性信息素识别或相关行为[130]。现有的研究显示大多数昆虫气味结合蛋白均能结合寄主植物挥发物，例如鳞翅目昆虫二化螟（）的CsupOBP8能高度结合植物挥发物-紫罗酮、橙花叔醇、金合欢醇和2-己酮[131]；半翅目昆虫柑橘木虱的DcitOBP1对-石竹烯、-石竹烯、-水芹烯和（1R）-（+）--蒎烯等寄主植物挥发物具有高亲和力，并且对这些化合物具有强烈的行为趋向性[25]；双翅目韭菜迟眼蕈蚊的BodoOBP1和BodoOBP2均能结合寄主植物挥发物二丙基三硫醚[132]；鞘翅目华北大黑鳃金龟（）的HoblOBP13和HoblOBP9分别对（反式）-2-己烯醇和苯乙醇具有高亲和力[133]。

有关天敌昆虫嗅觉编码机制的研究还比较匮乏。尽管通过组学分析已经鉴定出了许多寄生性天敌以及捕食性天敌的化学感受基因，但是对于基因的功能则研究较少[3,134-142]。对鳞翅目昆虫的寄生性天敌中红侧沟茧蜂的研究发现，7个气味结合蛋白能够识别具有不同化学构象和官能团的配体，其中MmedOBP2、MmedOBP4和MmedOBP6能结合萜烯类化合物，并且后两者对含有十五碳的萜烯类化合物有较好的亲和性，推断这些气味结合蛋白对中红侧沟茧蜂搜寻和定位寄主具有一定的作用[143]。对捕食性天敌中华通草蛉（）气味结合蛋白功能的研究结果显示，CsinOBP1和CsinOBP10结合谱较广并且是结合萜烯类化合物的两个关键气味结合蛋白，CsinOBP1不仅能结合植物挥发物金合欢醇、己酸、（顺式）-3-己烯酯、香叶基丙酮、-紫罗兰酮、2-十三烷酮和（反式）-橙花叔醇，还能结合蚜虫报警信息素成分（反式）--法尼烯，这为寄主搜寻和定位提供了直接证据[144]。

2.2 气味受体功能研究进展

气味受体是外周神经系统中接收嗅觉识别信号的关键因素，其功能鉴定对于解析嗅觉编码机制十分重要[145-146]。目前，研究人员对于鳞翅目夜蛾科昆虫性信息素识别机制的研究较为广泛，夜蛾科昆虫的性信息素受体（pheromone receptor，PR）在进化上较为保守，一些研究揭示了性信息素受体的功能在蛾类求偶交配等生理活动中发挥着重要作用。例如，棉铃虫性信息素受体HarmOR13能特异性识别性信息素主要成分（顺式）-11-十六碳烯醛，HarmOR6识别性信息素组分（顺式）-9-十六碳烯醛和（顺式）-9-十四碳烯醛，HarmOR16主要被次要组分（顺式）-11-十六碳烯醇激活[147]。随后，利用CRISPR/Cas9技术敲除雄性棉铃虫气味受体HarmOR16，发现OR16突变体提前与未成熟的雌性交配，明确了棉铃虫次要性信息素成分作为性信息素拮抗剂参与调控棉铃虫的最优交配时机[148]。最近的研究显示鳞翅目近缘种棉铃虫和烟青虫的同源性信息素受体OR14b跨膜结构域上两个氨基酸位点分化决定了功能差异，阐明了性信息素受体结构与功能之间的关系[149]。这些研究为解析棉铃虫识别性信息素的外周编码和物种形成机制提供了证据。此外，对烟青虫[150-151]、烟芽夜蛾[152]、斜纹夜蛾（）[153]、甜菜夜蛾[154]以及海灰翅夜蛾[155-156]等许多夜蛾科昆虫的性信息素受体功能开展了研究并取得了一定的进展。

植食性昆虫普通气味受体的激活是对寄主植物挥发物最初的信号识别与接收，参与调控昆虫的行为选择。体外功能研究显示一些寄主植物挥发物能够激活植食性昆虫的气味受体。例如斜纹夜蛾的气味受体SlituOR12能专一性识别植物挥发物（顺式）-3-己烯乙酸酯[157]。（顺式）-3-己烯乙酸酯能够激活绿盲蝽（）气味受体AlucOR28，可能参与调控绿盲蝽趋花行为[158]。对雌性绿盲蝽具有引诱作用的植物挥发物（反式）-2-己烯醛能够激活绿盲蝽雌性触角高表达的气味受体AlucOR46[159]。另外，研究显示引起棉铃虫成虫触角EAG反应的6种结构相似的植物挥发物香叶醇、-香茅醇、3, 7-二甲基-3-辛醇、（-）-芳樟醇、芳樟醇和（反式）-2-己烯乙酸酯均能激活鳞翅目夜蛾科3个近缘种棉铃虫、烟青虫和烟芽夜蛾的同源气味受体HarmOR12、HassOR12和HvirOR12[160]。一些研究证据显示单一气味受体的激活与植食性昆虫行为选择相关联。体内和体外功能研究表明豌豆蚜气味受体ApisOR5能被蚜虫报警信息素组分（反式）--法尼烯及其类似物乙酸香叶酯激活，通过RNAi技术基因沉默该受体后，豌豆蚜的跌落行为下降，证实ApisOR5通道的激活与蚜虫驱避行为相关，为筛选蚜虫驱避剂提供了理论依据[161]。对烟青虫气味受体和神经元的功能研究显示HassOR40以及短毛形感器中的B神经元能特异性识别3种结构类似的烟草挥发物乙酸香叶酯、香叶醇和橙花叔醇，并且橙花叔醇能显著地引起雌、雄虫的吸引行为，这种利用反向化学生态学理念以气味受体和神经元的功能鉴定为基础的高通量筛选可以极大地提高害虫行为调控产品的开发效率[22]。另外，鳞翅目昆虫的幼虫是主要的植食者，同样利用灵敏的嗅觉系统感受寄主植物挥发物。研究显示月桂烯、（顺式）-茉莉酮、苯乙醛和1-戊醇的混合物对棉铃虫1龄幼虫具有显著的引诱作用，其中（顺式）-茉莉酮和1-戊醇是混合物中的必要组分，可以激活在棉铃虫幼虫的同一嗅觉神经元上表达的OR41和OR52，初步阐明了棉铃虫幼虫寄主识别的神经和分子机制[21]。2020年，最新的研究发现烟青虫气味受体HassOR31在雌虫产卵器中高表达，能够感受顺-3-己烯基丁酯等12种寄主植物气味分子，明确了HassOR31参与产卵选择行为[162]。

目前，在天敌昆虫，尤其是鳞翅目幼虫寄生性天敌昆虫中有少数气味受体的功能得到鉴定。例如（顺式）-茉莉酮作为一种HIPV能特异性地激活齿唇姬蜂（）雌虫触角高表达的气味受体CchlOR62，选择行为试验表明该化合物能够显著地吸引交配后的齿唇姬蜂雌虫及其猎物棉铃虫幼虫，并且（顺式）-茉莉酮能显著地提高齿唇姬蜂雌虫的寄生效率，该研究初步解析了寄生蜂识别HIPV的嗅觉机制，为发展寄生蜂生物防控策略提供了理论依据[163]。另有研究显示，寄主挥发物-石竹烯、十一烷、（反式）--金合欢烯、（+）-香橙烯和（顺式）-3-己烯醇能够显著引诱平腹小蜂（）产卵。利用RNAi技术沉默气味受体后，平腹小蜂对-石竹烯和（反式）--金合欢烯的EAG反应显著降低，并且-石竹烯和（反式）--金合欢烯对平腹小峰的产卵引诱效果消失，表明AjapOR35可能参与调控平腹小蜂产卵行为[164]。天敌昆虫化学感受基因对于HIPV和猎物挥发物的识别尤为重要，是调控天敌昆虫寄主定位和产卵选择行为的重要靶标。目前对于天敌昆虫化学感受基因的功能研究还比较匮乏，是今后研究的一个重要方向。

3 应用

挥发性次生代谢物质调节植物与其他生物之间的作用一直被认为是可持续农作物保护的机遇。近年来，挥发物调节三级营养级关系已经成功地应用于农业生产[165]。目前，常见的田间防控策略包括气味诱芯的释放以调控昆虫的行为、诱导改变植物的引诱效果、培育新品种以促进挥发物的释放、间作套种（即推拉策略）等。但总的来说主要是利用各种化学信息素调节昆虫的行为。这些应用策略并不是独立起作用的，而是通过各种手段的综合应用以达到最优效果[2]。

3.1 化学信息素调控昆虫行为

田间直接施用合成的挥发性昆虫行为调控产品在诱杀、驱避害虫或吸引天敌方面已经取得了成功[166-168]。已商品化的昆虫行为调控产品大部分是针对植食性昆虫研制而成，其中引诱产品中以鳞翅目昆虫的性信息素及其类似物居多。利用挥发性化合物吸引天敌的应用已经有了成功案例，例如含有水杨酸甲酯的混合组分可以吸引草蛉等捕食性天敌昆虫，利用水杨酸甲酯和其他引诱成分复配的引诱剂已经得到商业化推广[169]。目前，国内外对于天敌昆虫行为调控产品的开发与应用仍然具有极大的发展潜力。而驱避剂产品在市场上的占比较低，主要用于防治蚊类和蚜虫等。

越来越多的证据表明，植物内源激素是植物诱导防御的重要信号物质，参与直接和间接的防御过程。例如，外施茉莉酸可以诱导番茄或水稻产生HIPV引起间接防御作用，提高对寄生蜂的吸引力，从而达到自然控害的效果[170-171]。然而这一结果在田间并没有得到广泛地证实。（顺式）-茉莉酮是一种挥发性植物激素，已在田间开展了应用研究，成功用于诱导大豆植物间接防御反应从而吸引卵寄生蜂[172]。化学遗传学筛选显示，阔叶杂草的除草剂2, 4-二氯苯氧基乙酸作为一种生长素的同系物可以极大地促进水稻对优势种卵寄生蜂的吸引[173]。

3.2 转基因作物应用

了解挥发性化合物介导的防御信号传导过程不仅可以使用标记辅助分子育种，而且可以通过识别信号的生物合成功能基因和调控基因促进育种程序。当这些信号是次生代谢物或与之相关的化合物时，转基因明显是一条更直接的途径。培育转基因新品种以驱避害虫或吸引天敌可能是进行害虫生物防治简单有效的方法之一[174-175]。蚜虫报警信息素对蚜虫的驱避效果显而易见，如果利用转基因技术从农作物中释放蚜虫报警信息素，将极大地降低蚜虫危害[176-177]。BEALE等[178]研究证实了拟南芥对桃蚜抑制以及提高寄生蜂搜寻能力的原理，并在十字花科植物中进行了验证。Bruce等[179]在实验室利用转基因方法在小麦中共表达（反式）--法尼烯和法呢基二磷酸前体的合成酶基因与质体靶向的氨基酸序列，证实了该小麦品种显著驱蚜并且提高寄生蜂的搜寻效率，但是在两年的田间试验中却没有达到相似的结果。

作物差异导致的HIPV种类变异使得对天敌昆虫的引诱作用造成分化。例如，不同玉米品系释放的HIPV存在明显的差异，导致天敌对植食性昆虫的寄生率产生一定的影响[180-181]。因此，在选择转基因植物合成靶标基因时应考虑到合成挥发性化合物是否具有特异性和共性，以提高害虫综合治理的效率。

3.3 种植方式的改变——推-拉策略

自从1990年MILLER等提出推-拉策略的理论，并将此策略应用于防治洋葱蝇（）以来[182]，推-拉策略得到了广泛地关注，该理论充分地将特殊植物挥发物和植物种植方式结合起来，利用间作套种的方式防治农业害虫，已在田间得到成功应用[165,183-184]。在非洲将玉米和糖蜜草（）间作，可以有效地驱避（推）鳞翅目蛀茎类害虫，并对寄生蜂具有引诱作用（拉），使得对蛀茎害虫幼虫的寄生率显著提高[185]。推-拉策略也已成功扩展到其他谷类作物[186]，但需要进一步鉴定、繁殖、培育有引诱作用或者驱避作用的植物，并且植物之间地下部分的相互作用不容忽视。此外，这种策略还可以通过灵活地应用抗聚集信息素、报警信息素、产卵忌避素、拒食剂等驱避剂以及聚集信息素、性信息素、产卵刺激素等引诱剂调控昆虫行为，以达到对植食性昆虫进行绿色、高效防控的目的。另一种方法是间作对病原微生物或植食性昆虫易感的特定植物品种，诱导释放HIPV并对临近植物释放防御信号，同时能强烈地吸引有益的节肢动物。易感植物可作为有效生物防治因子的繁殖地，也可用于早期害虫的监测。

4 展望

挥发性化合物在植物、植食性昆虫与天敌昆虫三级营养级关系的相互作用中具有重要的作用。本文综述了挥发物介导的三营养级间的互作机制以及国内外学者在该研究领域中的贡献和重要进展，概括了部分已鉴定的重要植物挥发物对植食性昆虫、天敌昆虫以及传粉昆虫的生态调控作用（表1）。值得一提的是，我国学者在昆虫化学感受基因的鉴定与功能研究方面开展了大量的工作，阐释了一些重要农业昆虫感受化学信号从而产生求偶、交配、寄主定位以及产卵等重要生理行为的生化机制，我国昆虫化学生态学研究的整体水平从研究技术与手段到研究平台的建设与利用等方面均获得了极大的提升，这为进一步开发具有自主知识产权的昆虫行为调控产品打下了基础。

表1 挥发性化合物在三级营养级关系中的生态调控作用

续表1 Continued table 1

引诱作用Attraction effect◆；驱避作用Repellent effect ★；引起的EAG反应EAG response●

虽然挥发物介导植物与昆虫之间互作关系的研究有了一些突破性进展，但是目前在农业生产的应用方面还存在着一定的局限性，例如，有大量的研究表明这些化合物具有引诱或驱避植食性昆虫、吸引天敌昆虫等调节昆虫行为的作用，但如何把这些化学信息素进行整合加工进而商业化生产，并科学地应用于实际的害虫综合治理过程中还有待于进一步的系统性研究。另外，在三级营养级关系中的许多作用机理还不清楚，尤其是植物与昆虫之间的互作机制、植物挥发物与昆虫激素协同作用的分子机制、天敌昆虫化学感受分子机制等相关研究还比较匮乏。因此，需要利用多种研究手段和策略进行深入地探索与实践，以期为发展绿色、安全和高效的昆虫行为调控技术提供理论参考。

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Mechanisms and Applications of plant-herbivore-natural enemy Tritrophic Interactions Mediated by Volatile organic Compounds

WANG Bing1, LI HuiMin1,2, CAO HaiQun2, WANG GuiRong1

1State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193;2College of Plant Protection, Anhui Agricultural University, Hefei 230036

The complicated interaction among plant, herbivore, and natural enemy is widespread in an agroecosystem. Volatile organic compounds (VOCs) play an important role in tritrophic interactions. Herbivores precisely distinguish and locate host plant through the emission of chemical cues. It is a research priority and highlight that herbivore-induced plant volatiles (HIPVs) acting as a key chemical cue play an indispensable role in regulating interactions. Moreover, floral attractants are the chemical cues used by pollinators to locate flowers and the food reward such as pollen and nectar that flowering plants offer, and they help to increase the probability of pollination and their development and fecundity. Over the last four decades, the novel research concepts and techniques are rapidly developed with the deep progress of traditional chemical ecology, especially improving in method and sensibility of chemical analysis, and widespread penetration of electrophysiological techniques. In tritrophic interactions, a large of chemosensory genes of insects involve in the process of chemoreception to VOCs. Hence, the discovery of putative chemosensory genes and further functional characterizations give the way for elucidating the molecular basis of chemoreception, and developing high-efficiency behavior regulation products for reasonable and environmentally friendly control of agricultural pest. It matters a great deal to the agroecosystem protection. This article summarized behavioural effects of herbivore, natural enemy and pollinator to VOCs, and illustrated mechanism and research status of tritrophic interactions mediated by VOCs, and reviewed applications in environmentally friendly prevention and control of insect pests. The last part is to look into the future of key issues.

herbivore-induced plant volatile; herbivore; natural enemy; tritrophic interaction; pollinator; odorant receptor