付興飛，胡發(fā)廣，程金煥，李貴平，黃家雄

木霉菌防控農(nóng)業(yè)害蟲的研究綜述

付興飛，胡發(fā)廣，程金煥，李貴平*，黃家雄

（云南省農(nóng)業(yè)科學(xué)院 熱帶亞熱帶經(jīng)濟作物研究所，云南 保山 678000）

害蟲對農(nóng)作物的生產(chǎn)和儲藏構(gòu)成了巨大威脅，過去主要以化學(xué)防治來控制害蟲，導(dǎo)致環(huán)境污染和人體健康等負(fù)面效應(yīng)，由此，急需開發(fā)安全高效的生物替代劑。木霉菌不僅可以控制病原菌引起的病害，還可以通過寄生、產(chǎn)生殺蟲類次級代謝物、拒食化合物、驅(qū)避代謝產(chǎn)物直接防治害蟲或誘導(dǎo)植物激活系統(tǒng)性防御反應(yīng)、吸引天敵、寄生害蟲共生微生物間接防控害蟲，被認(rèn)為是未來可持續(xù)發(fā)展農(nóng)業(yè)中一種比較理想的微生物劑。對木霉菌防控農(nóng)業(yè)害蟲的直接和間接機制進(jìn)行綜述，并對木霉菌的研究和利用趨勢進(jìn)行展望。

木霉菌；昆蟲寄生；次級代謝物；揮發(fā)性有機化合物；真菌類殺蟲劑；農(nóng)業(yè)害蟲

昆蟲作為生態(tài)系統(tǒng)的重要組成部分，在營養(yǎng)循環(huán)[1]、種子傳播[2]、土壤改良[3]、生物擾動[4]、作物授粉[5]及病蟲害防控[6]等生態(tài)系統(tǒng)服務(wù)功能中發(fā)揮重要作用。在國際糧食日益緊張的全球背景下，了解昆蟲在農(nóng)業(yè)生態(tài)系統(tǒng)中的作用，對確保國家糧食安全和可持續(xù)發(fā)展戰(zhàn)略尤為關(guān)鍵。據(jù)統(tǒng)計，在北美洲，每年昆蟲在授粉及害蟲防控等生態(tài)系統(tǒng)服務(wù)功能的經(jīng)濟價值就高達(dá)570億美元[7]。而害蟲作為昆蟲群落重要類群之一，也給農(nóng)業(yè)安全生產(chǎn)和儲存造成了巨大壓力。在熱帶地區(qū)，每年70%的作物產(chǎn)量損失與害蟲相關(guān)聯(lián)[7]。害蟲與作物間的相互作用受多種生物和非生物因素影響。首先，昆蟲必須精準(zhǔn)識別寄主植物的特定化學(xué)信號；其次，植物也會形成不同的物理結(jié)構(gòu)或合成防御類化合物，抵御害蟲攻擊[8]；然而，害蟲的長期進(jìn)化顯然已經(jīng)適應(yīng)了寄主植物的這種防御反應(yīng)，如通過取食不同植物部位[9]。此外，微生物群落在昆蟲與植物相互作用中也扮演關(guān)鍵角色，昆蟲內(nèi)共生微生物有助于昆蟲對植物防御次級代謝物解毒，與植物相關(guān)聯(lián)的微生物則能夠激活植物系統(tǒng)性防御反應(yīng)來抵御害蟲攻擊[10-13]。

害蟲作為導(dǎo)致農(nóng)作物減產(chǎn)的重要因素，給作物的安全生產(chǎn)和存儲造成巨大負(fù)面影響。而部分特定害蟲在部分特定作物中的危害更為顯著，如鷹嘴豆[14]、番茄[15]、棉花[16]等受棉鈴蟲危害造成的損失更為嚴(yán)重；近年來，我國大范圍玉米產(chǎn)區(qū)，受草地貪夜蛾（）危害導(dǎo)致玉米減產(chǎn)或無產(chǎn)[17]。直到20世紀(jì)初，隨著化學(xué)藥劑的應(yīng)用才得以有效控制害蟲危害，但隨之環(huán)境污染、農(nóng)殘、次要害蟲上升等負(fù)面效應(yīng)也相繼報道[18]。由于害蟲導(dǎo)致的農(nóng)業(yè)損失和化學(xué)農(nóng)藥帶來的負(fù)面效應(yīng)，尋找新的害蟲防治替代品已成為可持續(xù)農(nóng)業(yè)發(fā)展的必然[19-20]。

1 真菌對害蟲的控制

微生物既可作為病原菌導(dǎo)致植物發(fā)生病害，也可作為有效生物防控劑防治不同的農(nóng)業(yè)病蟲害[21-23]，如細(xì)菌[24]、病毒[25]、線蟲[26]及真菌[22,27]等可通過產(chǎn)生毒素、殺蟲類次級代謝物或直接寄生等達(dá)到抑制害蟲的作用，并作為農(nóng)業(yè)生物殺蟲劑廣泛應(yīng)用。

真菌類群是生物技術(shù)和工業(yè)生產(chǎn)中廣泛使用的微生物類群，在抗生素、抗癌藥劑、工業(yè)酶生產(chǎn)中廣泛應(yīng)用；同時，也可作為植物病蟲害生物控制劑、生物肥料或生物調(diào)節(jié)劑等[28-29]。在農(nóng)業(yè)方面，由于環(huán)境友好型藥劑需求量的逐年增加，近十年來真菌類殺蟲劑已成為最廣泛的應(yīng)用之一，推廣使用面積正逐年增加[30]。真菌作為寄生性微生物，也可作為昆蟲病原菌，具有感染和殺死農(nóng)業(yè)害蟲的能力。目前，在農(nóng)業(yè)領(lǐng)域研究中應(yīng)用最廣泛的有綠僵菌屬（）、白僵菌屬（）、擬青霉屬（）和叢枝菌屬（）等屬的真菌[31-32]。通常，昆蟲病原菌通過直接穿透角質(zhì)層來感染害蟲，而穿透角質(zhì)層需要粘附素和溶解酶（幾丁質(zhì)酶、蛋白酶和脂肪酶），當(dāng)病原菌克服昆蟲免疫系統(tǒng)后，在昆蟲體內(nèi)寄生，最終從致死的宿主體內(nèi)形成并傳播新的分生孢子。在整個寄生過程中，病原真菌必須產(chǎn)生多種殺蟲類次生代謝產(chǎn)物，才能夠完成其完整的生命周期[31]。同時，部分昆蟲病原真菌也可作為植物內(nèi)生菌，在植物組織中存活并完成部分生命周期，而不會對宿主植物產(chǎn)生負(fù)面效應(yīng)。在過去，許多種內(nèi)生真菌被發(fā)現(xiàn)可以降低植食性害蟲對植物的危害，這是由于不同作用機制導(dǎo)致，包括植物防御系統(tǒng)的激活，從初級代謝前體化合物中產(chǎn)生次級防御代謝產(chǎn)物的營養(yǎng)物質(zhì)吸收增加或真菌殺蟲代謝產(chǎn)物產(chǎn)生[33]。此外，在農(nóng)業(yè)上使用真菌殺蟲劑防治害蟲時，分析真菌殺蟲劑對天敵造成的危害也至關(guān)重要，這也符合農(nóng)業(yè)害蟲綜合防控IPM發(fā)展的具體要求。

2 木霉菌在農(nóng)業(yè)生態(tài)系統(tǒng)中的應(yīng)用

全世界已鑒定木霉屬真菌約377種[34-35]，目前主要用于農(nóng)業(yè)生物防治劑和不同行業(yè)所需酶的生產(chǎn)[36]。近年，在其他行業(yè)的應(yīng)用也不斷增加，如作為植物生長和對非生物脅迫耐受性的促進(jìn)劑[37-38]、生物肥料[39]、生物技術(shù)基因源[40]等。

木霉菌與植物相互作用主要表現(xiàn)為根部內(nèi)生真菌，受水楊酸SA介導(dǎo)的植物防御反應(yīng)，木霉菌只能定植于植物的最外層，從而阻止病原菌到達(dá)維管束，表現(xiàn)為系統(tǒng)性病原體[41-42]。通過這種方式，木霉菌也可以激活植物的系統(tǒng)性防御反應(yīng)，抵御害蟲和病原體的攻擊[42]。目前，應(yīng)用最多的就是將木霉菌孢子用于作物種子或繁殖體的包衣劑，播種或移栽期間通過灌溉和拌土等方式達(dá)到最大化的成功定植，以控制病蟲害[43-44]。木霉菌基因組比較分析也表明了根際真菌病原菌的大量存在，加上分泌豐富的營養(yǎng)物質(zhì)，導(dǎo)致木霉菌最終與根系相互作用，定植于根部[45-46]。木霉菌寄生需要多個信號來形成寄生的特異性結(jié)構(gòu)和產(chǎn)生必要的酶，通常木霉菌通過識別病原體細(xì)胞壁寡甲殼素寡糖；然后，開始以一種針對性的方式向化學(xué)信號方向生長；菌絲接觸后，木霉菌菌絲纏繞在病原體菌絲周圍，開始分泌細(xì)胞壁降解酶（幾丁質(zhì)酶、-1, 3-葡聚糖酶）；隨著病原菌細(xì)胞壁的降解形成空隙，木霉菌通過空隙從真菌體內(nèi)獲取生長所必須的營養(yǎng)物質(zhì)[47-48]。此外，木霉菌還能寄生線蟲的卵、第1齡幼蟲[49-50]及昆蟲的全周期，甚至還可以抑制人體某些病害[51]。

3 木霉菌對害蟲的直接防控

木霉菌通過寄生或產(chǎn)生殺蟲次級代謝產(chǎn)物、拒食化合物和驅(qū)避代謝產(chǎn)物直接防控害蟲。與其他害蟲病原菌作用機制基本一致，木霉菌可以主動寄生昆蟲，并直接從昆蟲體內(nèi)獲取各種營養(yǎng)物質(zhì)。絕大多數(shù)木霉菌的研究仍處于室內(nèi)研發(fā)階段，研究結(jié)果表明：木霉菌針對不同害蟲及不同作用時間，對害蟲的控制效率有差異。如：長枝木霉（）和哈茨木霉（）分別寄生于B型煙粉虱（）和熱帶臭蟲（），5 d內(nèi)均可導(dǎo)致40%的害蟲死亡[52]，14 d后死亡率超過90%[53]；同樣，不同種類木霉菌15 d后可導(dǎo)致90%椰子二疣犀甲（）死亡[54]。此外，將長枝木霉孢子液噴施后，既可提高茄子56%的產(chǎn)量，還可導(dǎo)致50%茄黃斑螟（）死亡[55]。而多種木霉菌均可產(chǎn)生殺蟲類次級代謝物，并將其釋放到環(huán)境中降低害蟲危害，如深綠木霉（）[56]。研究最多的哈茨木霉產(chǎn)生代謝物peptaibols類抗菌肽（小陽離子肽家族）[57]在抑制病原體生長方面非常有效，在蘿卜、豌豆及番茄等作物上應(yīng)用對赤擬谷盜（）、棉蚜（）[58]等害蟲的致死率高達(dá)100%；木霉菌還能產(chǎn)生揮發(fā)性殺蟲類次級代謝物，如6-戊基-α-吡喃酮，在48 h內(nèi)對葉螨的致死率高達(dá)100%[59]。木霉菌產(chǎn)生的殺蟲類次生代謝物對飛蝗[60]、食心蟲（）和粉紅色棉鈴蟲（）[7]均有顯著的直接防控作用。

另一方面，綠色木霉（）、桔綠木霉（）和深綠木霉也可產(chǎn)生拒食性化合物，如幾丁質(zhì)酶致使鱗翅目幼蟲取食量降低，從而導(dǎo)致外米綴蛾（）[61]、棉鈴蟲[62]和家蠶（）[63]在7 d內(nèi)死亡率達(dá)50%；而其他具有拒食活性化合物如游離脂肪酸亞油酸甲酯和亞油酸，對半翅目昆蟲也有抑制作用[64]；此外，木霉硒納米顆粒作為斜紋夜蛾（）幼蟲的拒食劑，可顯著降低斜紋夜蛾的種群[65]；深綠木霉通過水楊酸JA介導(dǎo)增加了玉米根部萜烯和6-戊基-2H-吡喃-2-酮的排放，而6-戊基-2H-吡喃-2-酮作為草地貪夜蛾的1種抗食性代謝物可明顯減少草地貪夜蛾對玉米的取食[66]。

此外，研究表明哈茨木霉、綠色木霉、橘綠木霉等揮發(fā)性有機化合物VOCs起到驅(qū)避害蟲的作用，有效降低了害蟲對植物資源的危害。通過真菌孢子在土壤中的應(yīng)用，因木霉菌產(chǎn)生的驅(qū)避代謝產(chǎn)物導(dǎo)致臺灣乳白蟻（）不能進(jìn)行筑巢[67]；在貯藏大豆種子中施用木霉菌孢子，也能使菜豆象（）對大豆種子的損耗減少達(dá)10%[68]。

4 木霉菌對害蟲的間接防控

木霉菌可以激活植物系統(tǒng)防御反應(yīng)、吸引天敵和寄生昆蟲共生微生物，間接的作為植物內(nèi)生真菌或真菌的重寄生真菌。微生物與植物間的相互作用觸發(fā)了植物的2種防御機制，保護(hù)植物免受危害。第1種為系統(tǒng)獲得抗性SAR，這種機制由局部感染觸發(fā)，在整個植物中提供對不同病原體生物的長期抗性，這與致病相關(guān)蛋白PR的合成相關(guān)聯(lián)，PR由編碼水楊酸SA生物合成相關(guān)酶的基因上調(diào)介導(dǎo)[69]；第2種為誘導(dǎo)系統(tǒng)抗性ISR，與茉莉酸JA和乙烯et的合成有關(guān)，由轉(zhuǎn)錄因子MYC2和ERF介導(dǎo)[70-71]，這種抗性誘導(dǎo)了一種啟動狀態(tài)，當(dāng)受到病原體攻擊時增強了植物防御基因的表達(dá)[72]。木霉菌誘導(dǎo)植物進(jìn)入防御反應(yīng)啟動狀態(tài)后，植物對病原體的攻擊反應(yīng)更快，防御也更強，這主要是通過降低效應(yīng)物觸發(fā)敏感性和增強效應(yīng)物觸發(fā)免疫實現(xiàn)的[73]。與其他微生物相同，木霉菌在植物根部定植，能夠激活植物系統(tǒng)性防御反應(yīng)，從而對病原菌和害蟲的防御，這主要由植物激素水楊酸SA和茉莉酸JA介導(dǎo)[74-75]。綠色木霉和甘氏木霉分別激活系統(tǒng)性植物防御系統(tǒng)，可使綠龜甲（）[76]和擬尺蠖（）[77]的攝食量分別減少25%。在番茄植株中，通過哈茨木霉激活在SA介導(dǎo)的防御系統(tǒng)，可以導(dǎo)致35%的B型煙粉虱死亡率[41]。深綠木霉可使棉葉片產(chǎn)生蛋白酶抑制劑，導(dǎo)致棉鈴蟲等鱗翅目幼蟲25 d內(nèi)達(dá)100%死亡率[78]。類似地，在蘭花屬植物中JA介導(dǎo)反應(yīng)刺激葉片中的鞣質(zhì)、根皮鞣質(zhì)、類黃酮、甾體、糖苷和生物堿的產(chǎn)生，從而阻止粉蚧（spp.）的取食[7]。

植物或大量與植物相關(guān)的生物群體間往往需要多營養(yǎng)級的協(xié)同作用，包括植食性昆蟲和土壤微生物，木霉菌作為營養(yǎng)級的重要組成部分[79]，木霉菌根部定植激活植物的系統(tǒng)防御反應(yīng)導(dǎo)致次生防御代謝產(chǎn)物在植物組織中積累。其中，一些代謝物可能具有趨避性的揮發(fā)性有機化合物，如萜烯（1-辛-3-醇、6-戊基-α-吡咯烷酮和4-戊基-α-吡咯烷酮等），可使草地貪夜蛾對玉米葉片的消耗減少75%[79]；此外，木霉菌定植植物根系后也會產(chǎn)生針對害蟲的間接防御反應(yīng)，此時植物會釋放有機化合物吸引害蟲的寄生蜂或捕食者，如6-戊基-α-吡咯烷酮和4-戊基-α-吡咯烷酮均對寄生蜂黑唇姬蜂（）具有引誘作用[79]，深綠木霉誘導(dǎo)玉米產(chǎn)生單-C10和C15倍半萜及其他揮發(fā)性有機化合物釋放，吸引黑唇姬蜂雌蟲[66]。通過在番茄根部定植誘導(dǎo)SA介導(dǎo)的系統(tǒng)抗性，哈茨木霉、長枝木霉及深綠木霉在25 d內(nèi)可導(dǎo)致100%的馬鈴薯蚜蟲個體死亡，這是由于植物產(chǎn)生的揮發(fā)性有機化合物如水楊酸甲酯MeSA，吸引了特定的寄生蜂（）[80]和捕食蚜蟲的盲蝽象（）[81]。對于其他蚜蟲來說，田間條件下的哈茨木霉引起JA介導(dǎo)的系統(tǒng)抗性，產(chǎn)生釋放有機化合物（Z）-3-己烯-1-醇，吸引蚜蟲天敵異色瓢蟲（），使害蟲種群數(shù)量減少22%[82]。類似針對葡萄園中不同種類的桃金娘和瓢蟲，木霉菌引起JA介導(dǎo)的VOCs產(chǎn)生，從而吸引半翅目擬蠅科寄生蜂[83]；受木霉菌誘導(dǎo)植物多種防御反應(yīng)相關(guān)基因的轉(zhuǎn)錄變化，導(dǎo)致前期參與防御反應(yīng)的基因上調(diào)或編碼保護(hù)酶（蛋白酶抑制劑、蘇氨酸脫氨酶、亮氨酸氨基肽酶、精氨酸酶及多酚氧化酶）在防御級聯(lián)下游被激活，最終改變了番茄的代謝途徑，導(dǎo)致?lián)]發(fā)性有機化合物VOCs的產(chǎn)生和釋放吸引了阿爾蚜繭蜂（），降低了斜紋夜蛾、大戟長管蚜（）的危害[78]。

為防治害蟲，木霉菌寄生昆蟲共生真菌的特性也可以利用。光滑足距小蠹（）是危害榛子（）的重要害蟲，雌蟲在寄主植物木質(zhì)部形成通道，幼蟲和成蟲都只能以這些木腐菌為食，因此，它們需要這種共生營養(yǎng)關(guān)系才能生存，榛子枝接種哈茨木霉, 棘胞木霉（）和深綠木霉通過直接寄生共生真菌顯著減少光滑足距小蠹的數(shù)量[84]。切葉蟻是熱帶和亞熱帶農(nóng)林生態(tài)系統(tǒng)中一種重要的經(jīng)濟害蟲，這些螞蟻利用葉片碎片培養(yǎng)真菌，木霉菌在體外對昆蟲共生真菌（）[85]和（sp.）的寄生作用已得到證實。從離體培養(yǎng)結(jié)果來看，（）在小麥麩皮上寄生共生真菌（）導(dǎo)致40 d內(nèi)100%的螞蟻因饑餓而死亡[86]。

此外，木霉菌可以作為昆蟲腸道微生物群的有效拮抗劑?？凳夏久梗ǎ┛墒箒喼抻衩酌c道菌群減少，最終導(dǎo)致亞洲玉米螟第4齡幼蟲12 d內(nèi)達(dá)30%死亡率[87]。最近，相關(guān)研究表明哈茨木霉會導(dǎo)致玉米釋放揮發(fā)性有機化合物（Z）-3-己烯-1-醇，該化合物也可作為植食性昆蟲的拮抗劑[88]。

5 展 望

農(nóng)業(yè)害蟲作為農(nóng)作物減產(chǎn)的重要因素，過去一直依賴化學(xué)殺蟲劑來降低害蟲危害，對生態(tài)環(huán)境和食品安全造成了巨大壓力，開發(fā)和利用環(huán)保型生物制劑已成為可持續(xù)農(nóng)業(yè)發(fā)展的重要趨勢。目前，多種真菌類防治劑應(yīng)用于農(nóng)業(yè)有害生物防控試驗中，均獲得比較理想的防控試驗效果，但在實際生產(chǎn)應(yīng)用中使用份額占比還比較小，這與農(nóng)業(yè)種植和生產(chǎn)者對化學(xué)農(nóng)藥長期使用形成依賴性及對新型生物農(nóng)藥認(rèn)識不足和接受程度低有關(guān)。近年來，伴隨著真菌類殺蟲劑使用率逐年上升，化學(xué)殺蟲劑使用率開始呈現(xiàn)下降趨勢，如木霉菌，由于其對植物病原真菌的寄生等作用機制，作為生物防治劑在農(nóng)業(yè)有害生物防治上被廣泛研究和應(yīng)用。近年來，研究表明木霉菌對農(nóng)業(yè)害蟲具有比較理想的防控效果，對多種農(nóng)業(yè)害蟲室內(nèi)防控效率高達(dá)100%，其作用方式具有直接寄生、產(chǎn)生殺蟲次級代謝物、拒食化合物和驅(qū)避代謝產(chǎn)物的直接防控作用，也具有通過激活植物系統(tǒng)防御反應(yīng)、吸引天敵、抑制害蟲生長和寄生害蟲共生微生物的間接防控作用，因此，木霉菌類生物制劑被認(rèn)為是一種比較理想的生物防治劑。

然而，值得注意的是用木霉菌作為真菌類殺蟲劑進(jìn)行的絕大多數(shù)試驗研究結(jié)果，都是在可調(diào)控的室內(nèi)實驗條件下進(jìn)行的，實際生產(chǎn)應(yīng)用效果需在田間進(jìn)行更多的試驗調(diào)查來加以驗證。木霉菌等真菌類生物防治劑在野外應(yīng)用較少的原因，可能是野外實地應(yīng)用試驗的防控效果不明顯或與室內(nèi)試驗結(jié)果差異顯著，因此，關(guān)于木霉菌野外應(yīng)用的報道較少。這也間接說明可調(diào)控的室內(nèi)實驗條件，不能準(zhǔn)確地反映野外田間的土壤質(zhì)地、溫濕變化和附生微生物群落等條件。此外，還應(yīng)開展平行試驗來驗證木霉菌對天敵或非有害昆蟲及本地昆蟲內(nèi)生真菌的安全性，這也符合農(nóng)業(yè)害蟲綜合防控IPM發(fā)展的具體要求。

綜上所述，利用木霉菌的直接和間接防控效果，有望成為農(nóng)業(yè)有害生物綠色防控的重要可持續(xù)替代品，但其作為農(nóng)業(yè)有害生物的生物防治劑對非有害生物的影響，仍需更多的野外和田間試驗加以驗證。

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A Review of the Research ofin Controlling Agricultural Pests

FU Xingfei, HU Faguang, CHEN Jinhuan, LI Guiping*, HUANG Jiaxiong

（Institute of Tropical and Subtropical Cash Crops, Yunnan Academy of Agricultural Sciences, Baoshan, Yunnan 678000, China）

Pests cause a great harm to the production and storage of crops. In the past, chemicals were mainly used to control pests. However, with the recognition of negative effects of environmental pollution and human health, it is urgent to develop a safe and efficient biological substitute.can control the diseases caused by pathogenic bacteria, and can also directly control pests by parasitizing, producing insecticidal secondary metabolites and antifeedant compounds, as well as driving away metabolites, or indirectly control pests by inducing plants to activate systemic defense response, attract natural enemies, parasitic pests and symbiotic microorganisms. So,is considered to be an ideal microbial agent in sustainable agriculture in the future. This paper reviews the direct and indirect mechanisms ofin controlling agricultural pests, and looks forward to the research and utilization trend of.

; insect parasitism; secondary metabolites; volatile organic compounds; mycopesticides; agricultural pest

S476.1

A

2095-3704（2022）03-0266-09

付興飛, 胡發(fā)廣, 程金煥, 等. 木霉菌防控農(nóng)業(yè)害蟲的研究綜述[J]. 生物災(zāi)害科學(xué), 2022, 45(3): 266-274.

10.3969/j.issn.2095-3704.2022.03.45

2022-06-08

2022-07-04

國家重點研發(fā)計劃咖啡可可產(chǎn)業(yè)鏈一體化示范項目（2020YFD1001202）和云南省隆陽區(qū)咖啡產(chǎn)業(yè)科技特派團項目（202004BI090136）

付興飛（1992—），男，碩士生，主要從事熱帶亞熱帶經(jīng)濟作物病蟲害綜合防控研究，1161003575@qq.com；*通信作者：李貴平，副研究員，lgp7007@163.com。