王冰，李慧敏,，操海群，王桂榮

揮發(fā)性化合物介導(dǎo)的植物-植食性昆蟲(chóng)-天敵三級(jí)營(yíng)養(yǎng)級(jí)互作機(jī)制及應(yīng)用

王冰1，李慧敏1,2，操海群2，王桂榮1

1中國(guó)農(nóng)業(yè)科學(xué)院植物保護(hù)研究所植物病蟲(chóng)害生物學(xué)國(guó)家重點(diǎn)實(shí)驗(yàn)室，北京 100193；2安徽農(nóng)業(yè)大學(xué)植物保護(hù)學(xué)院，合肥 230036

農(nóng)業(yè)生態(tài)系統(tǒng)中植物-植食性昆蟲(chóng)-天敵三級(jí)營(yíng)養(yǎng)級(jí)間存在復(fù)雜的互作關(guān)系，揮發(fā)性化合物在三級(jí)營(yíng)養(yǎng)級(jí)互作中發(fā)揮著重要作用。植食性昆蟲(chóng)能夠以植物揮發(fā)物為化學(xué)線索精準(zhǔn)地識(shí)別和定位寄主，而蟲(chóng)害誘導(dǎo)的揮發(fā)物作為關(guān)鍵的化學(xué)信息物質(zhì)對(duì)于調(diào)控三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系起到不可或缺的作用，一直是該領(lǐng)域研究的重點(diǎn)和熱點(diǎn)問(wèn)題。另外，植物為傳粉昆蟲(chóng)提供花粉或者花蜜，傳粉昆蟲(chóng)可以通過(guò)識(shí)別花中揮發(fā)物尋找食物來(lái)源，在幫助植物傳粉的同時(shí)有利于自身的生長(zhǎng)發(fā)育與繁殖。近40年來(lái)，隨著傳統(tǒng)化學(xué)生態(tài)學(xué)研究的不斷深入，特別是化學(xué)分析手段和靈敏度的不斷提高以及電生理研究技術(shù)的廣泛滲入，新的研究理念、研究手段快速形成與發(fā)展。在三級(jí)營(yíng)養(yǎng)級(jí)互作的過(guò)程中，昆蟲(chóng)化學(xué)感受基因參與了對(duì)揮發(fā)性化合物的識(shí)別。因此，對(duì)昆蟲(chóng)化學(xué)感受基因的挖掘與功能鑒定將有助于解析昆蟲(chóng)化學(xué)感受的分子機(jī)制，研發(fā)更高效的昆蟲(chóng)行為調(diào)控產(chǎn)品并科學(xué)合理地應(yīng)用于農(nóng)業(yè)害蟲(chóng)的綠色防控，對(duì)于農(nóng)田生態(tài)環(huán)境的保護(hù)具有十分重要的意義。本文綜述了揮發(fā)性化合物對(duì)植食性昆蟲(chóng)、天敵昆蟲(chóng)與傳粉昆蟲(chóng)行為的影響，詳述了揮發(fā)物介導(dǎo)的三級(jí)營(yíng)養(yǎng)級(jí)之間的互作機(jī)制與研究現(xiàn)狀，以及在害蟲(chóng)綠色防控中的應(yīng)用，并對(duì)未來(lái)重點(diǎn)研究的問(wèn)題進(jìn)行了展望。

蟲(chóng)害誘導(dǎo)的揮發(fā)物；植食性昆蟲(chóng)；天敵昆蟲(chóng)；三級(jí)營(yíng)養(yǎng)級(jí)互作；傳粉昆蟲(chóng)；氣味受體

1980年，PRICE等[1]提出了植物-植食性昆蟲(chóng)-天敵昆蟲(chóng)三級(jí)營(yíng)養(yǎng)級(jí)互作的理論，揭示了植物對(duì)植食性昆蟲(chóng)和天敵昆蟲(chóng)之間具有直接或間接、積極或消極等多方面影響。在錯(cuò)綜復(fù)雜的信息網(wǎng)中，化學(xué)信息調(diào)節(jié)三者之間的相互作用以及相互影響，是昆蟲(chóng)與昆蟲(chóng)、昆蟲(chóng)與植物、甚至植物與植物之間特殊的“語(yǔ)言”，是農(nóng)田生態(tài)系統(tǒng)的重要組成部分[2-4]。近40年來(lái)，隨著傳統(tǒng)化學(xué)生態(tài)學(xué)研究的不斷深入，特別是化學(xué)分析手段和靈敏度的不斷提高以及電生理研究技術(shù)的廣泛滲入，新的研究理念、研究手段快速形成與發(fā)展[5-6]，使得三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系之間的化學(xué)“語(yǔ)言”逐漸被破譯，如利馬豆（）-二斑葉螨（）-智利小植綏螨（）[7-8]；番茄（）-美洲棉鈴蟲(chóng)（）-短管赤眼蜂（）[9]等一些研究進(jìn)展極大地推動(dòng)了三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系在化學(xué)生態(tài)領(lǐng)域中的認(rèn)知。本文對(duì)揮發(fā)性化合物介導(dǎo)的植食性昆蟲(chóng)、天敵昆蟲(chóng)與傳粉昆蟲(chóng)行為的影響進(jìn)行了綜述，對(duì)揮發(fā)物在三級(jí)營(yíng)養(yǎng)級(jí)之間的互作機(jī)制、研究現(xiàn)狀及其應(yīng)用進(jìn)行了歸納與總結(jié)，以期為昆蟲(chóng)行為調(diào)控產(chǎn)品的研發(fā)以及害蟲(chóng)的綠色防控提供一定的借鑒作用和理論指導(dǎo)。

1 化學(xué)線索調(diào)控昆蟲(chóng)行為選擇

在健康植物的生長(zhǎng)發(fā)育過(guò)程中，植物能夠持續(xù)不斷地釋放大量的揮發(fā)物，植食性昆蟲(chóng)能夠以植物揮發(fā)物為化學(xué)線索，遠(yuǎn)距離識(shí)別和定位寄主，這不僅滿足了植食性昆蟲(chóng)自身的營(yíng)養(yǎng)需求，而且為尋找合適的產(chǎn)卵場(chǎng)所提供了必要條件[10-12]。當(dāng)植物受到植食性昆蟲(chóng)或病原菌危害和侵襲后，會(huì)形成一定的防御機(jī)制來(lái)應(yīng)對(duì)各種傷害。蟲(chóng)害誘導(dǎo)的植物揮發(fā)物（herbivore- induced plant volatile，HIPV）是一種特殊的植物“語(yǔ)言”，可以向植食性昆蟲(chóng)傳遞“警告”信號(hào)，亦可以向天敵昆蟲(chóng)發(fā)出“求救”信號(hào)，同時(shí)“告誡”臨近植株危險(xiǎn)的到來(lái)[2,13-14]。HIPV主要包括萜烯類化合物和綠葉揮發(fā)物（green leaf volatile，GLV），還包括少量的含氮、含硫化合物[15-17]。此外，昆蟲(chóng)種間和種內(nèi)信息素對(duì)于同種或異種昆蟲(chóng)行為選擇有一定的影響，尤其是植食性昆蟲(chóng)揮發(fā)物作為重要的化學(xué)線索影響著天敵昆蟲(chóng)的寄主定位。這些化學(xué)信號(hào)參與調(diào)控植物-植食性昆蟲(chóng)-天敵昆蟲(chóng)三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系之間的生態(tài)平衡。

1.1 植物揮發(fā)物對(duì)植食性昆蟲(chóng)的影響

植物揮發(fā)物對(duì)于植食性昆蟲(chóng)搜尋和定位寄主、產(chǎn)卵以及尋找配偶等生命活動(dòng)具有重要意義[10,18]。在鱗翅目昆蟲(chóng)中已開(kāi)展了系統(tǒng)的研究。例如，蘋(píng)果蠹蛾（）幼蟲(chóng)能識(shí)別成熟的西洋梨（）釋放的揮發(fā)物（反式）--法尼烯、（反式）-2-（順式）-4-癸二烯酸甲酯、（反式）-2-（順式）-4-癸二烯酸乙酯，并在行為上表現(xiàn)出明顯的偏好性[19]。油菜（）的揮發(fā)物異硫氰酸烯丙酯、2, 5-己二醇、異戊酸葉醇酯、（順式）-3-甲基丁酸-3-己烯酯不僅能強(qiáng)烈地激活小菜蛾（）觸角的EAG反應(yīng)，還能引起小菜蛾的定向飛行和著陸行為[20]。有研究顯示，（順式）-茉莉酮和1-戊醇是吸引棉鈴蟲(chóng)（）幼蟲(chóng)的關(guān)鍵成分[21]?！癥”型嗅覺(jué)儀試驗(yàn)表明，煙草植物揮發(fā)物乙酸香葉酯對(duì)煙青蟲(chóng)（）雌蛾有顯著的吸引作用，橙花叔醇能顯著地吸引雌、雄蛾[22]。由此可見(jiàn)，寄主植物揮發(fā)物在鱗翅目昆蟲(chóng)定位寄主的過(guò)程中發(fā)揮著關(guān)鍵作用。

另外，一些特定寄主植物揮發(fā)物對(duì)鞘翅目、半翅目和雙翅目等昆蟲(chóng)也具有引誘作用。例如藍(lán)桉樹(shù)（）植物揮發(fā)物莰烯、（+）--蒎烯和苯乙醇能夠顯著地吸引鞘翅目昆蟲(chóng)普來(lái)特象鼻蟲(chóng)（）[23]。蕓香科植物揮發(fā)物-石竹烯、-石竹烯和（1）-（+）--蒎烯能顯著地吸引半翅目昆蟲(chóng)柑橘木虱（）成蟲(chóng)[24-25]。蔥屬（）植物和側(cè)耳屬（）植物共有的揮發(fā)物檸檬烯對(duì)雙翅目昆蟲(chóng)韭菜遲眼蕈蚊（）的3齡幼蟲(chóng)以及雌成蟲(chóng)具有顯著的引誘作用[26]。

不同植食性昆蟲(chóng)對(duì)同種植物揮發(fā)物的行為反應(yīng)存在著差異。以1-辛烯-3-醇對(duì)多種雙翅目昆蟲(chóng)的作用為例，研究顯示1-辛烯-3-醇對(duì)橘小實(shí)蠅（）雄蠅具有驅(qū)避作用，但是對(duì)已交配的雌蟲(chóng)卻具有顯著的引誘作用[27]。另外，1-辛烯-3-醇能增加斑翅果蠅（）的搜尋時(shí)間并降低雌蠅產(chǎn)卵量[28]。來(lái)源于蘑菇、三葉草以及牛呼吸氣流中的1-辛烯-3-醇能夠吸引按蚊屬（）和伊蚊屬（）的蚊類，但是對(duì)致倦庫(kù)蚊（）卻有顯著的驅(qū)避作用[29-30]。寄主植物揮發(fā)物己醛、甲基丙基二硫醚、1-辛烯-3-醇對(duì)韭菜遲眼蕈蚊的3齡幼蟲(chóng)以及雌成蟲(chóng)具有驅(qū)避作用[26]。

在農(nóng)田生態(tài)系統(tǒng)中，植食性昆蟲(chóng)往往通過(guò)對(duì)植物“化學(xué)語(yǔ)言”不同編碼方式的識(shí)別而選擇和定位寄主植物。多種化合物在環(huán)境空間中的組成決定了昆蟲(chóng)對(duì)植物的偏好性選擇程度。例如，（順式）-3-己烯醇、正己醇、苯甲醛、（反式）--法尼烯、水楊酸甲酯等15種蠶豆（）植株揮發(fā)物的混合物能夠顯著吸引蠶豆蚜（）[31]。另外，具有特定比例的混合物比單一組分更能引起昆蟲(chóng)強(qiáng)烈的定向行為。研究顯示成熟芒果（）揮發(fā)物組分乙醇、醋酸和苯乙醇以1﹕22﹕5的比例混合比單一組分對(duì)黑腹果蠅（）的引誘作用更強(qiáng)[32]。以100﹕78﹕9比例混合的葡萄（）揮發(fā)物（反式）--石竹烯、4, 8-二甲基-1, 3, 7-壬三烯（DMNT）和（反式）--法尼烯能強(qiáng)烈地吸引葡萄花翅小卷蛾（），缺少其中的任何一種都會(huì)失去引誘效果[33-34]。麥麩發(fā)酵物棕櫚酸乙酯、亞油酸乙酯、亞油酸甲酯和亞油酸以10﹕24﹕6﹕0.2的比例混合對(duì)家蠅（）的引誘效果顯著高于單一組分，并顯著提高產(chǎn)卵量[35]。因此，具有特定比例的混合物對(duì)于鱗翅目、鞘翅目、雙翅目等多種植食性昆蟲(chóng)的搜尋、定位、產(chǎn)卵等生命活動(dòng)具有重要意義，可為開(kāi)發(fā)害蟲(chóng)引誘劑提供一定的理論參考。

1.2 蟲(chóng)害誘導(dǎo)的植物揮發(fā)物（HIPV）對(duì)昆蟲(chóng)的影響

1.2.1 植物的防御機(jī)制以及對(duì)植食性昆蟲(chóng)的影響 在植物的生長(zhǎng)周期中，經(jīng)常受到大量植食性昆蟲(chóng)的危害。因此，植物在長(zhǎng)期的進(jìn)化過(guò)程中形成了多種高效的防御途徑[36-39]，包括水楊酸（salicylic acid，SA）、茉莉酸（jasmonic acid，JA）、乙烯（ethene，ETH）等植物激素調(diào)節(jié)的信號(hào)轉(zhuǎn)導(dǎo)途徑[40-44]。植食性昆蟲(chóng)取食以及產(chǎn)卵等行為會(huì)誘導(dǎo)植物產(chǎn)生HIPV，是植物應(yīng)對(duì)外來(lái)侵害的一種防御策略[2,13-14,45]。研究表明HIPV能夠增強(qiáng)植物對(duì)植食性昆蟲(chóng)的防御反應(yīng)。例如，草地貪夜蛾（）取食水稻（）釋放揮發(fā)物吲哚能誘導(dǎo)未被取食的組織中絲裂原活化蛋白激酶OsMPK3的轉(zhuǎn)運(yùn)、積累和活化，增強(qiáng)以及多個(gè)茉莉酸合成基因的轉(zhuǎn)錄，而茉莉酸信號(hào)傳導(dǎo)有利于植物防御，該研究解析了吲哚增強(qiáng)水稻對(duì)草地貪夜蛾防御反應(yīng)的作用模式[17]。類似地，甜菜夜蛾（）危害玉米植株釋放的綠葉揮發(fā)物（順式）-3-己烯乙酸酯也能增加玉米植株茉莉酸的合成，從而啟動(dòng)植物對(duì)植食性昆蟲(chóng)的防御[16]。另外，昆蟲(chóng)的揮發(fā)物也能影響植物的防御反應(yīng)。例如，雙翅目秋麒麟癭蠅（）雄蟲(chóng)釋放的主要揮發(fā)物混合成分螺結(jié)縮長(zhǎng)時(shí)間處理北美一枝黃花（），誘導(dǎo)黃花關(guān)鍵防御激素茉莉酸水平的增加，從而增強(qiáng)植物防御反應(yīng)，降低對(duì)懷卵雌蟲(chóng)的吸引[46]。地下環(huán)境中生存的昆蟲(chóng)病原線蟲(chóng)揮發(fā)物苯甲醛、苯甲醇、苯乙酮、壬醛和吲哚能夠促進(jìn)植物的防御反應(yīng)并且影響植食性昆蟲(chóng)的行為。研究顯示昆蟲(chóng)病原線蟲(chóng)揮發(fā)物能夠減少地上部植食性昆蟲(chóng)馬鈴薯甲蟲(chóng)（）幼蟲(chóng)對(duì)馬鈴薯葉片的取食，并且抑制馬鈴薯甲蟲(chóng)雌蟲(chóng)的產(chǎn)卵行為，這主要是由于馬鈴薯植株經(jīng)過(guò)昆蟲(chóng)病原線蟲(chóng)揮發(fā)物的誘導(dǎo)后能產(chǎn)生更高水平的水楊酸和茉莉酸，從而使植株產(chǎn)生防御反應(yīng)[47]。有些植食性昆蟲(chóng)利用HIPV操縱植物的防御反應(yīng)，更適于自身的繁衍。研究顯示煙粉虱（）誘導(dǎo)的馬鈴薯植物揮發(fā)物-月桂烯或-石竹烯能抑制臨近植株的水楊酸防御途徑，使臨近植株更適于煙粉虱的生長(zhǎng)發(fā)育[48]。地下害蟲(chóng)紅胸律點(diǎn)跳甲（）幼蟲(chóng)取食烏桕（），釋放2-乙基己醇和壬醛能吸引同種成蟲(chóng)取食地上部分的葉片，根部酚類次生防御物質(zhì)含量降低，從而有利于幼蟲(chóng)的生長(zhǎng)發(fā)育[49]。

植食性昆蟲(chóng)識(shí)別HIPV后，“推斷”寄主植物的適生情況以及是否存在競(jìng)爭(zhēng)者，從而表現(xiàn)出一定的行為反饋[50]。為了提高同種后代的存活率，降低后代生存競(jìng)爭(zhēng)，植食性昆蟲(chóng)往往會(huì)避免在已被危害的植物上定殖或產(chǎn)卵。例如，煙芽夜蛾（）雌蛾通過(guò)識(shí)別煙草（）在夜間釋放的（順式）-3-己烯丁酸、（順式）-3-己烯乙酸酯等多種綠葉揮發(fā)物的混合物從而產(chǎn)生驅(qū)避行為，并且避免在植株上產(chǎn)卵[51]。類似地，海灰翅夜蛾（）取食棉花后，誘導(dǎo)的揮發(fā)物DMNT能抑制同種害蟲(chóng)對(duì)性信息素的選擇，從而影響交配和產(chǎn)卵行為[52]。

VEYRAT等[53]研究表明，蟲(chóng)害誘導(dǎo)的玉米植株揮發(fā)物吲哚能提高?；页嵋苟暧紫x(chóng)的死亡率并降低其取食量，驅(qū)避雌成蟲(chóng)產(chǎn)卵，從而達(dá)到直接防御的作用。此外，蟲(chóng)害誘導(dǎo)的植物揮發(fā)物法尼烯的同分異構(gòu)體（反式，反式）--法尼烯（49%）、（反式）--法尼烯（26%）、（順式）--法尼烯（18%）以及（順式，反式）--法尼烯（7%）能顯著地抑制煙青蟲(chóng)雌蟲(chóng)的產(chǎn)卵行為[54]。蟲(chóng)害誘導(dǎo)的玉米植株揮發(fā)物（反式）--法尼烯對(duì)玉米蚜（）具有顯著的驅(qū)避作用[55]。麥長(zhǎng)管蚜（）危害小麥釋放的3種誘導(dǎo)揮發(fā)物6-甲基-5-庚烯-2-酮、6-甲基-5-庚烯-2-醇和水楊酸甲酯對(duì)有翅蚜具有較好的驅(qū)避效果[56]。茶尺蠖（）幼蟲(chóng)取食后誘導(dǎo)的茶樹(shù)揮發(fā)物芐腈和芳樟醇對(duì)同種未交配的雌、雄成蟲(chóng)具有顯著的驅(qū)避作用[57]。HIPV對(duì)同一生態(tài)位的異種植食性昆蟲(chóng)也會(huì)產(chǎn)生一定的影響。例如，煙芽夜蛾危害煙草植株能誘導(dǎo)釋放大量的煙堿，對(duì)同一植株上的西花薊馬（）產(chǎn)生忌避作用[58]。HIPV對(duì)某些植食性昆蟲(chóng)具有驅(qū)避作用是植物在長(zhǎng)期的進(jìn)化過(guò)程中產(chǎn)生的自身防御反應(yīng)，以減少植食性昆蟲(chóng)的危害。

1.2.2 HIPV對(duì)天敵昆蟲(chóng)行為的影響 植株被植食性昆蟲(chóng)危害后能產(chǎn)生一系列自身防御反應(yīng)，釋放多種誘導(dǎo)揮發(fā)物作為利他素以吸引植食性昆蟲(chóng)的自然天敵，從而間接地調(diào)控生態(tài)系統(tǒng)的組成結(jié)構(gòu)[2,59-61]。最早報(bào)道的有關(guān)植物利用HIPV吸引天敵的證據(jù)顯示，二斑葉螨危害利馬豆釋放的DMNT能吸引天敵智利小植綏螨[60,62]，從而形成間接防御。隨著研究的深入，越來(lái)越多證據(jù)表明HIPV能夠遠(yuǎn)距離地吸引植食性昆蟲(chóng)的天敵，尤其是寄生性天敵昆蟲(chóng)，研究較多的是鱗翅目昆蟲(chóng)危害玉米產(chǎn)生的HIPV對(duì)寄生蜂行為的影響。例如，甜菜夜蛾幼蟲(chóng)危害玉米植株釋放的（順式）-3-己烯乙酸酯、（順式）-3-己烯醇和芳樟醇等11種蟲(chóng)害誘導(dǎo)的混合揮發(fā)物，對(duì)幼蟲(chóng)寄生蜂緣腹盤(pán)絨繭蜂（）有顯著的引誘作用[63]。草地貪夜蛾取食玉米植株1—2 h后，釋放的綠葉揮發(fā)物（順式）-3-己烯醛、（反式）-2-己烯醛、（反式）-3-己烯醇和（順式）-3-己烯乙酸酯與少量單萜芳樟醇和-月桂烯混合顯著地吸引卵寄生蜂短管赤眼蜂，而危害玉米12 h后的植株卻失去了對(duì)短管赤眼蜂的引誘作用，表明該寄生蜂更易被新鮮傷口產(chǎn)生的揮發(fā)物所吸引[64]。此外，草地貪夜蛾危害玉米產(chǎn)生的-蒎烯和-古巴烯的混合物對(duì)卵寄生蜂島甲腹繭蜂（）有極顯著的引誘作用，是主要的活性成分[65]。由此可見(jiàn)，蟲(chóng)害誘導(dǎo)的玉米植株揮發(fā)物通過(guò)不同活性成分的組合模式能吸引多種寄生蜂前來(lái)定位獵物的幼蟲(chóng)或卵，從而發(fā)揮生物控害的效果。

HIPV對(duì)害蟲(chóng)的間接防御作用具有普遍性?！癥”型嗅覺(jué)儀試驗(yàn)顯示，棉鈴蟲(chóng)幼蟲(chóng)危害反枝莧（）誘導(dǎo)產(chǎn)生的植物揮發(fā)物6-甲基-5-庚烯-2-酮和-欖香烯可以顯著地吸引雌性中紅側(cè)溝繭蜂（），有利于棉鈴蟲(chóng)綠色防控產(chǎn)品的開(kāi)發(fā)與應(yīng)用[66]。半翅目昆蟲(chóng)紅圓蚧（）危害柑橘后誘導(dǎo)產(chǎn)生的D-檸檬烯和-羅勒烯是吸引天敵昆蟲(chóng)印巴黃蚜小蜂（）的主要化合物，在紅圓蚧的生物防治中發(fā)揮著重要作用[67]。已有的研究表明植物防御過(guò)程中產(chǎn)生的萜烯類化合物DMNT和TMTT是天敵昆蟲(chóng)重要的利他素，利用轉(zhuǎn)基因的方法使水稻釋放DMNT和TMTT能顯著地吸引水稻害蟲(chóng)的天敵二化螟絨繭蜂（），起到對(duì)害蟲(chóng)的間接防御作用，為培育新型抗蟲(chóng)品種提供了新思路[68]。

捕食性天敵昆蟲(chóng)同樣能夠識(shí)別環(huán)境中的多種HIPV，從而快速定位獵物。有研究顯示，麥長(zhǎng)管蚜危害小麥誘導(dǎo)產(chǎn)生的（順式）-3-己烯乙酸酯對(duì)黑帶食蚜蠅（）具有顯著的引誘作用，水楊酸甲酯能夠特異性地吸引異色瓢蟲(chóng)（），這些化合物在調(diào)控麥長(zhǎng)管蚜的種群消長(zhǎng)中發(fā)揮著重要作用[69]。單一或混合組分的HIPV對(duì)不同種天敵昆蟲(chóng)的引誘效果存在差異。例如，田間試驗(yàn)結(jié)果表明蟲(chóng)害誘導(dǎo)揮發(fā)物羅勒烯對(duì)四條小食蚜蠅（）具有明顯的引誘作用[70]，嗅覺(jué)行為試驗(yàn)顯示低濃度的單一組分水楊酸甲酯能夠顯著地吸引對(duì)多異瓢蟲(chóng)（）[71]。單一組分（順式）-3-己烯乙酸酯對(duì)七星瓢蟲(chóng)（）具有引誘作用[70]。而（順式）-3-己烯乙酸酯和水楊酸甲酯的混合物比單一組分對(duì)食螨瓢蟲(chóng)（）的引誘作用更強(qiáng)[72]。雜食性天敵昆蟲(chóng)矮小長(zhǎng)脊盲蝽（）能夠識(shí)別桃蚜（）取食茄子葉片產(chǎn)生的（反式）--法尼烯和TMTT等HIPV的混合物，從而偏好性地選擇有蚜蟲(chóng)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敵昆蟲(chóng)尋找獵物，植物地下根系分泌的化學(xué)信息素也能吸引天敵，從而定位寄主。有研究顯示昆蟲(chóng)病原線蟲(chóng)能識(shí)別玉米根螢葉甲（）幼蟲(chóng)危害玉米根部釋放的（反式）--石竹烯，對(duì)這種化學(xué)線索識(shí)別的特異性使其精準(zhǔn)定位獵物[74]。

1.3 花的揮發(fā)物參與昆蟲(chóng)行為調(diào)控

植物與傳粉昆蟲(chóng)之間的相互作用在維持大多數(shù)陸地生態(tài)系統(tǒng)功能完整性中發(fā)揮著重要作用[75]。大約75%的農(nóng)作物種類以及88%的開(kāi)花植物都需要傳粉昆蟲(chóng)授粉從而增加作物產(chǎn)量[76-78]。反之，植物為傳粉昆蟲(chóng)提供花粉或花蜜，傳粉昆蟲(chóng)可以通過(guò)識(shí)別花中揮發(fā)物尋找食物來(lái)源，在幫助植物傳粉的同時(shí)有利于傳粉昆蟲(chóng)自身的生長(zhǎng)發(fā)育與繁殖[79-81]。花的揮發(fā)物是吸引傳粉昆蟲(chóng)的重要化學(xué)信號(hào)。為了研究花香的演變與昆蟲(chóng)化學(xué)交流的關(guān)聯(lián)性，SCHIESTL[82]分析了來(lái)源于96種植物和87種昆蟲(chóng)中的71種最常見(jiàn)的花香揮發(fā)性有機(jī)化合物的發(fā)生、共性和進(jìn)化模式，研究顯示植物和昆蟲(chóng)產(chǎn)生的揮發(fā)性有機(jī)化合物有87%的重疊，其中芳香族化合物在被子植物中進(jìn)化出信號(hào)功能，主要用于吸引傳粉媒介。

傳粉昆蟲(chóng)的嗅覺(jué)系統(tǒng)在識(shí)別花揮發(fā)物的過(guò)程中發(fā)揮著重要作用[83-84]?；ǖ膿]發(fā)物由花的不同結(jié)構(gòu)和部位散發(fā)，傳粉昆蟲(chóng)可以通過(guò)識(shí)別揮發(fā)物差異定位花的不同部位。在無(wú)花蜜的植物中，花藥是植物提供給訪花昆蟲(chóng)的主要報(bào)償。SOLíS-MONTERO等[81]研究表明，刺萼龍葵（）傳粉型花藥揮發(fā)物丁香酚、-古巴烯和甲基丁香酚，以及取食型花藥揮發(fā)物苯甲酸甲酯、苯甲酸乙酯、（反式）--法尼烯、-癸內(nèi)酯和（反式）-金合歡醇均能顯著地吸引東方熊蜂（）前來(lái)訪花，選擇行為試驗(yàn)表明東方熊峰更加偏好選擇取食型花藥。另外，研究發(fā)現(xiàn)刺萼龍葵取食型花藥和傳粉型花藥的揮發(fā)物均能引起一種麥蜂（）的觸角電位反應(yīng)[81]。有研究表明菊科植物絲路薊（）花的揮發(fā)物苯乙醛、水楊酸甲酯、2-甲氧基苯甲酸甲酯是引起黑帶食蚜蠅觸角電位反應(yīng)的主要成分[83]。田間調(diào)查試驗(yàn)表明，神后鳶尾（）主要的傳粉昆蟲(chóng)為熊蜂（）和意大利蜜蜂（），其次為黑帶食蚜蠅。神后鳶尾花的揮發(fā)物以1, 4-對(duì)苯二甲醚、苯乙醇和2-甲氧基苯甲醛等芳香化合物為主，推測(cè)是吸引傳粉昆蟲(chóng)前來(lái)取食和訪花的主要化學(xué)線索[85]。此外，蜜蜂和食蚜蠅等傳粉昆蟲(chóng)在檸檬烯釋放量較高的甜葉菊（）上訪問(wèn)數(shù)量最多[86]。牡丹草屬植物花的揮發(fā)物主要為烴類化合物、脂肪酸、長(zhǎng)鏈的醇、醛類和少量芳香族化合物，能夠吸引雙翅目、膜翅目和鞘翅目昆蟲(chóng)[77]。另外，花揮發(fā)物也能吸引夜行性訪花昆蟲(chóng)。比如，含有芳樟醇和（反式）--羅勒烯等巴西香可可（）花揮發(fā)物的混合物能吸引夜行性傳粉昆蟲(chóng)隧蜂（）[87]。夜行性盲蝽（）能識(shí)別花揮發(fā)物（順式）-茉莉酮，從而定位寄主萬(wàn)年青屬植物，并將其作為取食和交配場(chǎng)所[88]。另外，花揮發(fā)物也能引起一些植食性昆蟲(chóng)的電生理反應(yīng)或行為反應(yīng)。例如，大葉醉魚(yú)草（）的花揮發(fā)物苯甲醛、茶香酮、2, 2, 6-三甲基-1, 4-環(huán)己二酮、氧化異佛爾酮、（反式，反式）--法尼烯等能引起甘藍(lán)尺蠖（）的觸角電位反應(yīng)[89]。誘捕試驗(yàn)表明，花揮發(fā)的混合物-月桂烯與苯乙醛能顯著地吸引大豆尺蠖（）[90]。

一些植物可以通過(guò)模擬并釋放昆蟲(chóng)的信息素組分吸引傳粉昆蟲(chóng)，從而增加植物自身的傳粉。疏花火燒蘭（）可以揮發(fā)一些類似于蚜蟲(chóng)報(bào)警信息素組分的萜烯類化合物，例如-蒎烯、-蒎烯、-月桂烯和-水芹烯等利他素，從而吸引黑帶食蚜蠅前來(lái)產(chǎn)卵，有助于為其傳粉[91-93]。澳大利亞蘭花（）可以釋放一種與雌性黃蜂（）性信息素組分2-乙基-5-丙基-1, 3-環(huán)己二酮相同的化合物以吸引傳粉昆蟲(chóng)授粉[94-95]。在長(zhǎng)期進(jìn)化過(guò)程中，植物發(fā)展的這種“欺騙”行為有助于自身的生存和繁衍。

開(kāi)花植物釋放的化合物具有動(dòng)態(tài)節(jié)律性[96-97]?；ǖ膫€(gè)體發(fā)育階段以及花性別差異導(dǎo)致其釋放的揮發(fā)物對(duì)傳粉昆蟲(chóng)和植食性訪花昆蟲(chóng)的引誘作用也存在一定的分化。THEIS等研究發(fā)現(xiàn)雌雄異株的絲路薊雄蕊和雌蕊花的揮發(fā)物在開(kāi)花初期和花期均以芳香族化合物為主，但是雄蕊花大多吸引鞘翅目金龜甲和半翅目盲蝽等植食性訪花昆蟲(chóng)，而雌蕊花大多吸引蜜蜂和集蜂科的傳粉昆蟲(chóng)。而雌雄同株的美洲近緣種薊屬植物同樣在開(kāi)花初期和花期大量釋放芳香族化合物，對(duì)植食性訪花昆蟲(chóng)和傳粉昆蟲(chóng)均具有引誘作用，其中對(duì)鳳蝶等傳粉昆蟲(chóng)的引誘效果最好。無(wú)論是雌雄異株的絲路薊還是雌雄同株的在開(kāi)花末期單萜的釋放量顯著提高，但對(duì)訪花昆蟲(chóng)的引誘作用明顯下降[98]。ZHOU等揭示了漸狹葉煙草（）的花在夜間釋放的揮發(fā)物（反式）--香檸檬烯吸引煙草天蛾（）成蟲(chóng)進(jìn)行傳粉，而日間煙草的葉片釋放的同一化合物作為一種HIPV用于吸引煙草天蛾幼蟲(chóng)的天敵，這種植物揮發(fā)物釋放的時(shí)空變化策略有助于解決同為傳粉昆蟲(chóng)和植食性害蟲(chóng)的困境，同時(shí)為傳粉昆蟲(chóng)和植食性昆蟲(chóng)對(duì)花香信號(hào)與植物防御之間形成的協(xié)同進(jìn)化機(jī)制提供了遺傳證據(jù)[99]。植物繁殖方式不同也影響植物對(duì)傳粉昆蟲(chóng)的吸引。HABER等研究表明，遠(yuǎn)親繁殖的玄參科植物猴面花（）揮發(fā)物中的一個(gè)關(guān)鍵組分（反式）--香柑油烯的釋放量顯著高于近親繁殖的量，傳粉昆蟲(chóng)東方熊蜂能夠識(shí)別這種釋放量的差異對(duì)遠(yuǎn)親繁殖的種類完成授粉過(guò)程[100]。因此，花揮發(fā)物的來(lái)源、植物繁殖類型、花的個(gè)體發(fā)育階段與花性別差異在訪花昆蟲(chóng)與植物互作中都發(fā)揮著重要作用。

1.4 植食性昆蟲(chóng)與天敵之間的化學(xué)聯(lián)系

天敵昆蟲(chóng)可以通過(guò)植食性昆蟲(chóng)揮發(fā)物以及性信息素組分等化學(xué)線索尋找和定位獵物[101]。具有代表性的案例是蚜蟲(chóng)天敵對(duì)蚜蟲(chóng)蜜露揮發(fā)物和蚜蟲(chóng)報(bào)警信息素等化學(xué)線索的精準(zhǔn)識(shí)別。LEROY等研究表明，巢菜修尾蚜（）蜜露揮發(fā)物3-羥基-2-丁酮、3-甲基-2-丁烯醛、3-甲基-1-丁醇和檸檬烯可以顯著地吸引七星瓢蟲(chóng)[102]，這些化合物的鑒定為巢菜修尾蚜的生物防治提供了重要的化學(xué)線索。另一研究顯示蚜蟲(chóng)報(bào)警信息素（反式）--法尼烯能被黑帶食蚜蠅識(shí)別并誘導(dǎo)產(chǎn)卵行為[103-104]。周氏嚙小蜂（）是一種寄生在美國(guó)白蛾（）蛹中的內(nèi)寄生蜂，“Y”型嗅覺(jué)儀試驗(yàn)表明美國(guó)白蛾蛹的揮發(fā)物1-十二烯能引起已交配的周氏嚙小蜂強(qiáng)烈的定向選擇，這一結(jié)果為揭示蛹寄生機(jī)制提供了分子依據(jù)[105]。

另外，植食性昆蟲(chóng)釋放的性信息素可以作為天敵昆蟲(chóng)定位寄主的重要化學(xué)線索[106-107]。例如雌性麥蛾繭蜂（）能識(shí)別雄性寄主大蠟螟（）釋放的性信息素混合物壬醛和十一醛，并以此作為尋找產(chǎn)卵場(chǎng)所的直接線索[108]。ZHU等研究表明豌豆蚜（）性信息素組分（1R, 4aS, 7S, 7aR）-荊芥醇能夠顯著吸引金眼草蛉（）成蟲(chóng)，有利于其迅速定位獵物[109-110]。由此可見(jiàn)，天敵昆蟲(chóng)對(duì)于植食性昆蟲(chóng)釋放的化學(xué)線索的識(shí)別具有普遍性和特異性，然而目前對(duì)于識(shí)別的分子機(jī)制并不十分清楚。

2 昆蟲(chóng)化學(xué)感受基因參與化學(xué)線索的識(shí)別

隨著轉(zhuǎn)錄組和基因組等測(cè)序技術(shù)的飛速發(fā)展，研究人員已經(jīng)鑒定出大量的昆蟲(chóng)化學(xué)感受基因。主要的嗅覺(jué)基因包括氣味結(jié)合蛋白（odorant binding protein，OBP）、化學(xué)感受蛋白（chemosensory protein，CSP）、氣味受體（odorant receptor，OR）、離子型受體（ionotropic receptor，IR）、感覺(jué)神經(jīng)元膜蛋白（sensory neuron membrane protein，SNMP）等，參與了外周嗅覺(jué)系統(tǒng)信號(hào)的轉(zhuǎn)導(dǎo)[111-112]。外部氣味分子通過(guò)觸角極孔進(jìn)入感器淋巴液，通過(guò)氣味結(jié)合蛋白將其運(yùn)輸至神經(jīng)元樹(shù)突膜后，釋放氣味分子的同時(shí)激活氣味受體，將化學(xué)信號(hào)轉(zhuǎn)變?yōu)殡娦盘?hào)并傳遞到更高級(jí)的神經(jīng)中樞，從而指導(dǎo)昆蟲(chóng)行為[113-114]。在這個(gè)過(guò)程中，氣味結(jié)合蛋白和氣味受體的功能獲得了廣泛的研究，為解析昆蟲(chóng)觸角外周神經(jīng)系統(tǒng)嗅覺(jué)識(shí)別的分子機(jī)制奠定了基礎(chǔ)。

2.1 氣味結(jié)合蛋白參與化學(xué)線索的識(shí)別

氣味結(jié)合蛋白聯(lián)系著氣味受體與氣味分子之間的相互作用。目前，通過(guò)轉(zhuǎn)錄組或者基因組測(cè)序已經(jīng)鑒定了包括鱗翅目、雙翅目、鞘翅目、半翅目[115-121]等許多種植食性昆蟲(chóng)的氣味結(jié)合蛋白基因。其中，對(duì)在鱗翅目昆蟲(chóng)中較為保守的性信息素結(jié)合蛋白（pheromone binding protein，PBP）和普通氣味結(jié)合蛋白（general odorant binding protein，GOBP）的功能已經(jīng)開(kāi)展了廣泛的研究[122-128]。例如桃小食心蟲(chóng)（）的性信息素結(jié)合蛋白CsasPBP3能特異性結(jié)合兩種性信息素成分（順式）-7-二十烯-11-酮和（順式）-7-十九烯-11-酮，而普通氣味結(jié)合蛋白CsasGOBP1對(duì)這兩種信息素組分結(jié)合力最強(qiáng)，同時(shí)也能結(jié)合植物揮發(fā)物，CsasGOBP2偏好結(jié)合植物揮發(fā)物，表明CsasPBP和CsasGOBP分別在識(shí)別性信息素和寄主植物揮發(fā)物的過(guò)程中發(fā)揮著不同的作用[129]。有研究顯示，經(jīng)典的氣味結(jié)合蛋白也能結(jié)合性信息素組分，例如甜菜夜蛾的SexiOBP7除了可以結(jié)合苯乙酮和金合歡醇等寄主植物揮發(fā)物以外，對(duì)甜菜夜蛾的主要性信息素組分（順式，反式）-9, 12-十四碳二烯醇醋酸酯的結(jié)合能力最好，推測(cè)SexiOBP7可能參與性信息素識(shí)別或相關(guān)行為[130]?，F(xiàn)有的研究顯示大多數(shù)昆蟲(chóng)氣味結(jié)合蛋白均能結(jié)合寄主植物揮發(fā)物，例如鱗翅目昆蟲(chóng)二化螟（）的CsupOBP8能高度結(jié)合植物揮發(fā)物-紫羅酮、橙花叔醇、金合歡醇和2-己酮[131]；半翅目昆蟲(chóng)柑橘木虱的DcitOBP1對(duì)-石竹烯、-石竹烯、-水芹烯和（1R）-（+）--蒎烯等寄主植物揮發(fā)物具有高親和力，并且對(duì)這些化合物具有強(qiáng)烈的行為趨向性[25]；雙翅目韭菜遲眼蕈蚊的BodoOBP1和BodoOBP2均能結(jié)合寄主植物揮發(fā)物二丙基三硫醚[132]；鞘翅目華北大黑鰓金龜（）的HoblOBP13和HoblOBP9分別對(duì)（反式）-2-己烯醇和苯乙醇具有高親和力[133]。

有關(guān)天敵昆蟲(chóng)嗅覺(jué)編碼機(jī)制的研究還比較匱乏。盡管通過(guò)組學(xué)分析已經(jīng)鑒定出了許多寄生性天敵以及捕食性天敵的化學(xué)感受基因，但是對(duì)于基因的功能則研究較少[3,134-142]。對(duì)鱗翅目昆蟲(chóng)的寄生性天敵中紅側(cè)溝繭蜂的研究發(fā)現(xiàn)，7個(gè)氣味結(jié)合蛋白能夠識(shí)別具有不同化學(xué)構(gòu)象和官能團(tuán)的配體，其中MmedOBP2、MmedOBP4和MmedOBP6能結(jié)合萜烯類化合物，并且后兩者對(duì)含有十五碳的萜烯類化合物有較好的親和性，推斷這些氣味結(jié)合蛋白對(duì)中紅側(cè)溝繭蜂搜尋和定位寄主具有一定的作用[143]。對(duì)捕食性天敵中華通草蛉（）氣味結(jié)合蛋白功能的研究結(jié)果顯示，CsinOBP1和CsinOBP10結(jié)合譜較廣并且是結(jié)合萜烯類化合物的兩個(gè)關(guān)鍵氣味結(jié)合蛋白，CsinOBP1不僅能結(jié)合植物揮發(fā)物金合歡醇、己酸、（順式）-3-己烯酯、香葉基丙酮、-紫羅蘭酮、2-十三烷酮和（反式）-橙花叔醇，還能結(jié)合蚜蟲(chóng)報(bào)警信息素成分（反式）--法尼烯，這為寄主搜尋和定位提供了直接證據(jù)[144]。

2.2 氣味受體功能研究進(jìn)展

氣味受體是外周神經(jīng)系統(tǒng)中接收嗅覺(jué)識(shí)別信號(hào)的關(guān)鍵因素，其功能鑒定對(duì)于解析嗅覺(jué)編碼機(jī)制十分重要[145-146]。目前，研究人員對(duì)于鱗翅目夜蛾科昆蟲(chóng)性信息素識(shí)別機(jī)制的研究較為廣泛，夜蛾科昆蟲(chóng)的性信息素受體（pheromone receptor，PR）在進(jìn)化上較為保守，一些研究揭示了性信息素受體的功能在蛾類求偶交配等生理活動(dòng)中發(fā)揮著重要作用。例如，棉鈴蟲(chóng)性信息素受體HarmOR13能特異性識(shí)別性信息素主要成分（順式）-11-十六碳烯醛，HarmOR6識(shí)別性信息素組分（順式）-9-十六碳烯醛和（順式）-9-十四碳烯醛，HarmOR16主要被次要組分（順式）-11-十六碳烯醇激活[147]。隨后，利用CRISPR/Cas9技術(shù)敲除雄性棉鈴蟲(chóng)氣味受體HarmOR16，發(fā)現(xiàn)OR16突變體提前與未成熟的雌性交配，明確了棉鈴蟲(chóng)次要性信息素成分作為性信息素拮抗劑參與調(diào)控棉鈴蟲(chóng)的最優(yōu)交配時(shí)機(jī)[148]。最近的研究顯示鱗翅目近緣種棉鈴蟲(chóng)和煙青蟲(chóng)的同源性信息素受體OR14b跨膜結(jié)構(gòu)域上兩個(gè)氨基酸位點(diǎn)分化決定了功能差異，闡明了性信息素受體結(jié)構(gòu)與功能之間的關(guān)系[149]。這些研究為解析棉鈴蟲(chóng)識(shí)別性信息素的外周編碼和物種形成機(jī)制提供了證據(jù)。此外，對(duì)煙青蟲(chóng)[150-151]、煙芽夜蛾[152]、斜紋夜蛾（）[153]、甜菜夜蛾[154]以及海灰翅夜蛾[155-156]等許多夜蛾科昆蟲(chóng)的性信息素受體功能開(kāi)展了研究并取得了一定的進(jìn)展。

植食性昆蟲(chóng)普通氣味受體的激活是對(duì)寄主植物揮發(fā)物最初的信號(hào)識(shí)別與接收，參與調(diào)控昆蟲(chóng)的行為選擇。體外功能研究顯示一些寄主植物揮發(fā)物能夠激活植食性昆蟲(chóng)的氣味受體。例如斜紋夜蛾的氣味受體SlituOR12能專一性識(shí)別植物揮發(fā)物（順式）-3-己烯乙酸酯[157]。（順式）-3-己烯乙酸酯能夠激活綠盲蝽（）氣味受體AlucOR28，可能參與調(diào)控綠盲蝽趨花行為[158]。對(duì)雌性綠盲蝽具有引誘作用的植物揮發(fā)物（反式）-2-己烯醛能夠激活綠盲蝽雌性觸角高表達(dá)的氣味受體AlucOR46[159]。另外，研究顯示引起棉鈴蟲(chóng)成蟲(chóng)觸角EAG反應(yīng)的6種結(jié)構(gòu)相似的植物揮發(fā)物香葉醇、-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鱗翅目夜蛾科3個(gè)近緣種棉鈴蟲(chóng)、煙青蟲(chóng)和煙芽夜蛾的同源氣味受體HarmOR12、HassOR12和HvirOR12[160]。一些研究證據(jù)顯示單一氣味受體的激活與植食性昆蟲(chóng)行為選擇相關(guān)聯(lián)。體內(nèi)和體外功能研究表明豌豆蚜氣味受體ApisOR5能被蚜蟲(chóng)報(bào)警信息素組分（反式）--法尼烯及其類似物乙酸香葉酯激活，通過(guò)RNAi技術(shù)基因沉默該受體后，豌豆蚜的跌落行為下降，證實(shí)ApisOR5通道的激活與蚜蟲(chóng)驅(qū)避行為相關(guān)，為篩選蚜蟲(chóng)驅(qū)避劑提供了理論依據(jù)[161]。對(duì)煙青蟲(chóng)氣味受體和神經(jīng)元的功能研究顯示HassOR40以及短毛形感器中的B神經(jīng)元能特異性識(shí)別3種結(jié)構(gòu)類似的煙草揮發(fā)物乙酸香葉酯、香葉醇和橙花叔醇，并且橙花叔醇能顯著地引起雌、雄蟲(chóng)的吸引行為，這種利用反向化學(xué)生態(tài)學(xué)理念以氣味受體和神經(jīng)元的功能鑒定為基礎(chǔ)的高通量篩選可以極大地提高害蟲(chóng)行為調(diào)控產(chǎn)品的開(kāi)發(fā)效率[22]。另外，鱗翅目昆蟲(chóng)的幼蟲(chóng)是主要的植食者，同樣利用靈敏的嗅覺(jué)系統(tǒng)感受寄主植物揮發(fā)物。研究顯示月桂烯、（順式）-茉莉酮、苯乙醛和1-戊醇的混合物對(duì)棉鈴蟲(chóng)1齡幼蟲(chóng)具有顯著的引誘作用，其中（順式）-茉莉酮和1-戊醇是混合物中的必要組分，可以激活在棉鈴蟲(chóng)幼蟲(chóng)的同一嗅覺(jué)神經(jīng)元上表達(dá)的OR41和OR52，初步闡明了棉鈴蟲(chóng)幼蟲(chóng)寄主識(shí)別的神經(jīng)和分子機(jī)制[21]。2020年，最新的研究發(fā)現(xiàn)煙青蟲(chóng)氣味受體HassOR31在雌蟲(chóng)產(chǎn)卵器中高表達(dá)，能夠感受順-3-己烯基丁酯等12種寄主植物氣味分子，明確了HassOR31參與產(chǎn)卵選擇行為[162]。

目前，在天敵昆蟲(chóng)，尤其是鱗翅目幼蟲(chóng)寄生性天敵昆蟲(chóng)中有少數(shù)氣味受體的功能得到鑒定。例如（順式）-茉莉酮作為一種HIPV能特異性地激活齒唇姬蜂（）雌蟲(chóng)觸角高表達(dá)的氣味受體CchlOR62，選擇行為試驗(yàn)表明該化合物能夠顯著地吸引交配后的齒唇姬蜂雌蟲(chóng)及其獵物棉鈴蟲(chóng)幼蟲(chóng)，并且（順式）-茉莉酮能顯著地提高齒唇姬蜂雌蟲(chóng)的寄生效率，該研究初步解析了寄生蜂識(shí)別HIPV的嗅覺(jué)機(jī)制，為發(fā)展寄生蜂生物防控策略提供了理論依據(jù)[163]。另有研究顯示，寄主揮發(fā)物-石竹烯、十一烷、（反式）--金合歡烯、（+）-香橙烯和（順式）-3-己烯醇能夠顯著引誘平腹小蜂（）產(chǎn)卵。利用RNAi技術(shù)沉默氣味受體后，平腹小蜂對(duì)-石竹烯和（反式）--金合歡烯的EAG反應(yīng)顯著降低，并且-石竹烯和（反式）--金合歡烯對(duì)平腹小峰的產(chǎn)卵引誘效果消失，表明AjapOR35可能參與調(diào)控平腹小蜂產(chǎn)卵行為[164]。天敵昆蟲(chóng)化學(xué)感受基因?qū)τ贖IPV和獵物揮發(fā)物的識(shí)別尤為重要，是調(diào)控天敵昆蟲(chóng)寄主定位和產(chǎn)卵選擇行為的重要靶標(biāo)。目前對(duì)于天敵昆蟲(chóng)化學(xué)感受基因的功能研究還比較匱乏，是今后研究的一個(gè)重要方向。

3 應(yīng)用

揮發(fā)性次生代謝物質(zhì)調(diào)節(jié)植物與其他生物之間的作用一直被認(rèn)為是可持續(xù)農(nóng)作物保護(hù)的機(jī)遇。近年來(lái)，揮發(fā)物調(diào)節(jié)三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系已經(jīng)成功地應(yīng)用于農(nóng)業(yè)生產(chǎn)[165]。目前，常見(jiàn)的田間防控策略包括氣味誘芯的釋放以調(diào)控昆蟲(chóng)的行為、誘導(dǎo)改變植物的引誘效果、培育新品種以促進(jìn)揮發(fā)物的釋放、間作套種（即推拉策略）等。但總的來(lái)說(shuō)主要是利用各種化學(xué)信息素調(diào)節(jié)昆蟲(chóng)的行為。這些應(yīng)用策略并不是獨(dú)立起作用的，而是通過(guò)各種手段的綜合應(yīng)用以達(dá)到最優(yōu)效果[2]。

3.1 化學(xué)信息素調(diào)控昆蟲(chóng)行為

田間直接施用合成的揮發(fā)性昆蟲(chóng)行為調(diào)控產(chǎn)品在誘殺、驅(qū)避害蟲(chóng)或吸引天敵方面已經(jīng)取得了成功[166-168]。已商品化的昆蟲(chóng)行為調(diào)控產(chǎn)品大部分是針對(duì)植食性昆蟲(chóng)研制而成，其中引誘產(chǎn)品中以鱗翅目昆蟲(chóng)的性信息素及其類似物居多。利用揮發(fā)性化合物吸引天敵的應(yīng)用已經(jīng)有了成功案例，例如含有水楊酸甲酯的混合組分可以吸引草蛉等捕食性天敵昆蟲(chóng)，利用水楊酸甲酯和其他引誘成分復(fù)配的引誘劑已經(jīng)得到商業(yè)化推廣[169]。目前，國(guó)內(nèi)外對(duì)于天敵昆蟲(chóng)行為調(diào)控產(chǎn)品的開(kāi)發(fā)與應(yīng)用仍然具有極大的發(fā)展?jié)摿?。而?qū)避劑產(chǎn)品在市場(chǎng)上的占比較低，主要用于防治蚊類和蚜蟲(chóng)等。

越來(lái)越多的證據(jù)表明，植物內(nèi)源激素是植物誘導(dǎo)防御的重要信號(hào)物質(zhì)，參與直接和間接的防御過(guò)程。例如，外施茉莉酸可以誘導(dǎo)番茄或水稻產(chǎn)生HIPV引起間接防御作用，提高對(duì)寄生蜂的吸引力，從而達(dá)到自然控害的效果[170-171]。然而這一結(jié)果在田間并沒(méi)有得到廣泛地證實(shí)。（順式）-茉莉酮是一種揮發(fā)性植物激素，已在田間開(kāi)展了應(yīng)用研究，成功用于誘導(dǎo)大豆植物間接防御反應(yīng)從而吸引卵寄生蜂[172]?；瘜W(xué)遺傳學(xué)篩選顯示，闊葉雜草的除草劑2, 4-二氯苯氧基乙酸作為一種生長(zhǎng)素的同系物可以極大地促進(jìn)水稻對(duì)優(yōu)勢(shì)種卵寄生蜂的吸引[173]。

3.2 轉(zhuǎn)基因作物應(yīng)用

了解揮發(fā)性化合物介導(dǎo)的防御信號(hào)傳導(dǎo)過(guò)程不僅可以使用標(biāo)記輔助分子育種，而且可以通過(guò)識(shí)別信號(hào)的生物合成功能基因和調(diào)控基因促進(jìn)育種程序。當(dāng)這些信號(hào)是次生代謝物或與之相關(guān)的化合物時(shí)，轉(zhuǎn)基因明顯是一條更直接的途徑。培育轉(zhuǎn)基因新品種以驅(qū)避害蟲(chóng)或吸引天敵可能是進(jìn)行害蟲(chóng)生物防治簡(jiǎn)單有效的方法之一[174-175]。蚜蟲(chóng)報(bào)警信息素對(duì)蚜蟲(chóng)的驅(qū)避效果顯而易見(jiàn)，如果利用轉(zhuǎn)基因技術(shù)從農(nóng)作物中釋放蚜蟲(chóng)報(bào)警信息素，將極大地降低蚜蟲(chóng)危害[176-177]。BEALE等[178]研究證實(shí)了擬南芥對(duì)桃蚜抑制以及提高寄生蜂搜尋能力的原理，并在十字花科植物中進(jìn)行了驗(yàn)證。Bruce等[179]在實(shí)驗(yàn)室利用轉(zhuǎn)基因方法在小麥中共表達(dá)（反式）--法尼烯和法呢基二磷酸前體的合成酶基因與質(zhì)體靶向的氨基酸序列，證實(shí)了該小麥品種顯著驅(qū)蚜并且提高寄生蜂的搜尋效率，但是在兩年的田間試驗(yàn)中卻沒(méi)有達(dá)到相似的結(jié)果。

作物差異導(dǎo)致的HIPV種類變異使得對(duì)天敵昆蟲(chóng)的引誘作用造成分化。例如，不同玉米品系釋放的HIPV存在明顯的差異，導(dǎo)致天敵對(duì)植食性昆蟲(chóng)的寄生率產(chǎn)生一定的影響[180-181]。因此，在選擇轉(zhuǎn)基因植物合成靶標(biāo)基因時(shí)應(yīng)考慮到合成揮發(fā)性化合物是否具有特異性和共性，以提高害蟲(chóng)綜合治理的效率。

3.3 種植方式的改變——推-拉策略

自從1990年MILLER等提出推-拉策略的理論，并將此策略應(yīng)用于防治洋蔥蠅（）以來(lái)[182]，推-拉策略得到了廣泛地關(guān)注，該理論充分地將特殊植物揮發(fā)物和植物種植方式結(jié)合起來(lái)，利用間作套種的方式防治農(nóng)業(yè)害蟲(chóng)，已在田間得到成功應(yīng)用[165,183-184]。在非洲將玉米和糖蜜草（）間作，可以有效地驅(qū)避（推）鱗翅目蛀莖類害蟲(chóng)，并對(duì)寄生蜂具有引誘作用（拉），使得對(duì)蛀莖害蟲(chóng)幼蟲(chóng)的寄生率顯著提高[185]。推-拉策略也已成功擴(kuò)展到其他谷類作物[186]，但需要進(jìn)一步鑒定、繁殖、培育有引誘作用或者驅(qū)避作用的植物，并且植物之間地下部分的相互作用不容忽視。此外，這種策略還可以通過(guò)靈活地應(yīng)用抗聚集信息素、報(bào)警信息素、產(chǎn)卵忌避素、拒食劑等驅(qū)避劑以及聚集信息素、性信息素、產(chǎn)卵刺激素等引誘劑調(diào)控昆蟲(chóng)行為，以達(dá)到對(duì)植食性昆蟲(chóng)進(jìn)行綠色、高效防控的目的。另一種方法是間作對(duì)病原微生物或植食性昆蟲(chóng)易感的特定植物品種，誘導(dǎo)釋放HIPV并對(duì)臨近植物釋放防御信號(hào)，同時(shí)能強(qiáng)烈地吸引有益的節(jié)肢動(dòng)物。易感植物可作為有效生物防治因子的繁殖地，也可用于早期害蟲(chóng)的監(jiān)測(cè)。

4 展望

揮發(fā)性化合物在植物、植食性昆蟲(chóng)與天敵昆蟲(chóng)三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系的相互作用中具有重要的作用。本文綜述了揮發(fā)物介導(dǎo)的三營(yíng)養(yǎng)級(jí)間的互作機(jī)制以及國(guó)內(nèi)外學(xué)者在該研究領(lǐng)域中的貢獻(xiàn)和重要進(jìn)展，概括了部分已鑒定的重要植物揮發(fā)物對(duì)植食性昆蟲(chóng)、天敵昆蟲(chóng)以及傳粉昆蟲(chóng)的生態(tài)調(diào)控作用（表1）。值得一提的是，我國(guó)學(xué)者在昆蟲(chóng)化學(xué)感受基因的鑒定與功能研究方面開(kāi)展了大量的工作，闡釋了一些重要農(nóng)業(yè)昆蟲(chóng)感受化學(xué)信號(hào)從而產(chǎn)生求偶、交配、寄主定位以及產(chǎn)卵等重要生理行為的生化機(jī)制，我國(guó)昆蟲(chóng)化學(xué)生態(tài)學(xué)研究的整體水平從研究技術(shù)與手段到研究平臺(tái)的建設(shè)與利用等方面均獲得了極大的提升，這為進(jìn)一步開(kāi)發(fā)具有自主知識(shí)產(chǎn)權(quán)的昆蟲(chóng)行為調(diào)控產(chǎn)品打下了基礎(chǔ)。

表1 揮發(fā)性化合物在三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系中的生態(tài)調(diào)控作用

續(xù)表1 Continued table 1

續(xù)表1 Continued table 1

引誘作用Attraction effect◆；驅(qū)避作用Repellent effect ★；引起的EAG反應(yīng)EAG response●

雖然揮發(fā)物介導(dǎo)植物與昆蟲(chóng)之間互作關(guān)系的研究有了一些突破性進(jìn)展，但是目前在農(nóng)業(yè)生產(chǎn)的應(yīng)用方面還存在著一定的局限性，例如，有大量的研究表明這些化合物具有引誘或驅(qū)避植食性昆蟲(chóng)、吸引天敵昆蟲(chóng)等調(diào)節(jié)昆蟲(chóng)行為的作用，但如何把這些化學(xué)信息素進(jìn)行整合加工進(jìn)而商業(yè)化生產(chǎn)，并科學(xué)地應(yīng)用于實(shí)際的害蟲(chóng)綜合治理過(guò)程中還有待于進(jìn)一步的系統(tǒng)性研究。另外，在三級(jí)營(yíng)養(yǎng)級(jí)關(guān)系中的許多作用機(jī)理還不清楚，尤其是植物與昆蟲(chóng)之間的互作機(jī)制、植物揮發(fā)物與昆蟲(chóng)激素協(xié)同作用的分子機(jī)制、天敵昆蟲(chóng)化學(xué)感受分子機(jī)制等相關(guān)研究還比較匱乏。因此，需要利用多種研究手段和策略進(jìn)行深入地探索與實(shí)踐，以期為發(fā)展綠色、安全和高效的昆蟲(chóng)行為調(diào)控技術(shù)提供理論參考。

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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

10.3864/j.issn.0578-1752.2021.08.007

2020-05-27；

2020-07-06

國(guó)家重點(diǎn)研發(fā)計(jì)劃政府間國(guó)際科技創(chuàng)新合作重點(diǎn)專項(xiàng)（2019YFE0105800）、國(guó)家自然科學(xué)基金杰出青年基金項(xiàng)目（31725023）、國(guó)家自然科學(xué)基金國(guó)際（地區(qū)）合作與交流項(xiàng)目（31861133019）、國(guó)家自然科學(xué)基金創(chuàng)新研究群體項(xiàng)目（31621064）

王冰，E-mail：bwang@ippcaas.cn。李慧敏，E-mail：1092883329@qq.com。王冰和李慧敏為同等貢獻(xiàn)作者。通信作者王桂榮，E-mail：wangguirong@caas.cn

（責(zé)任編輯 岳梅）