木霉菌防控农业害虫的研究综述

付兴飞，胡发广，程金焕，李贵平，黄家雄

木霉菌防控农业害虫的研究综述

付兴飞，胡发广，程金焕，李贵平*，黄家雄

（云南省农业科学院 热带亚热带经济作物研究所，云南 保山 678000）

害虫对农作物的生产和储藏构成了巨大威胁，过去主要以化学防治来控制害虫，导致环境污染和人体健康等负面效应，由此，急需开发安全高效的生物替代剂。木霉菌不仅可以控制病原菌引起的病害，还可以通过寄生、产生杀虫类次级代谢物、拒食化合物、驱避代谢产物直接防治害虫或诱导植物激活系统性防御反应、吸引天敌、寄生害虫共生微生物间接防控害虫，被认为是未来可持续发展农业中一种比较理想的微生物剂。对木霉菌防控农业害虫的直接和间接机制进行综述，并对木霉菌的研究和利用趋势进行展望。

木霉菌；昆虫寄生；次级代谢物；挥发性有机化合物；真菌类杀虫剂；农业害虫

昆虫作为生态系统的重要组成部分，在营养循环[1]、种子传播[2]、土壤改良[3]、生物扰动[4]、作物授粉[5]及病虫害防控[6]等生态系统服务功能中发挥重要作用。在国际粮食日益紧张的全球背景下，了解昆虫在农业生态系统中的作用，对确保国家粮食安全和可持续发展战略尤为关键。据统计，在北美洲，每年昆虫在授粉及害虫防控等生态系统服务功能的经济价值就高达570亿美元[7]。而害虫作为昆虫群落重要类群之一，也给农业安全生产和储存造成了巨大压力。在热带地区，每年70%的作物产量损失与害虫相关联[7]。害虫与作物间的相互作用受多种生物和非生物因素影响。首先，昆虫必须精准识别寄主植物的特定化学信号；其次，植物也会形成不同的物理结构或合成防御类化合物，抵御害虫攻击[8]；然而，害虫的长期进化显然已经适应了寄主植物的这种防御反应，如通过取食不同植物部位[9]。此外，微生物群落在昆虫与植物相互作用中也扮演关键角色，昆虫内共生微生物有助于昆虫对植物防御次级代谢物解毒，与植物相关联的微生物则能够激活植物系统性防御反应来抵御害虫攻击[10-13]。

害虫作为导致农作物减产的重要因素，给作物的安全生产和存储造成巨大负面影响。而部分特定害虫在部分特定作物中的危害更为显著，如鹰嘴豆[14]、番茄[15]、棉花[16]等受棉铃虫危害造成的损失更为严重；近年来，我国大范围玉米产区，受草地贪夜蛾（）危害导致玉米减产或无产[17]。直到20世纪初，随着化学药剂的应用才得以有效控制害虫危害，但随之环境污染、农残、次要害虫上升等负面效应也相继报道[18]。由于害虫导致的农业损失和化学农药带来的负面效应，寻找新的害虫防治替代品已成为可持续农业发展的必然[19-20]。

1 真菌对害虫的控制

微生物既可作为病原菌导致植物发生病害，也可作为有效生物防控剂防治不同的农业病虫害[21-23]，如细菌[24]、病毒[25]、线虫[26]及真菌[22,27]等可通过产生毒素、杀虫类次级代谢物或直接寄生等达到抑制害虫的作用，并作为农业生物杀虫剂广泛应用。

真菌类群是生物技术和工业生产中广泛使用的微生物类群，在抗生素、抗癌药剂、工业酶生产中广泛应用；同时，也可作为植物病虫害生物控制剂、生物肥料或生物调节剂等[28-29]。在农业方面，由于环境友好型药剂需求量的逐年增加，近十年来真菌类杀虫剂已成为最广泛的应用之一，推广使用面积正逐年增加[30]。真菌作为寄生性微生物，也可作为昆虫病原菌，具有感染和杀死农业害虫的能力。目前，在农业领域研究中应用最广泛的有绿僵菌属（）、白僵菌属（）、拟青霉属（）和丛枝菌属（）等属的真菌[31-32]。通常，昆虫病原菌通过直接穿透角质层来感染害虫，而穿透角质层需要粘附素和溶解酶（几丁质酶、蛋白酶和脂肪酶），当病原菌克服昆虫免疫系统后，在昆虫体内寄生，最终从致死的宿主体内形成并传播新的分生孢子。在整个寄生过程中，病原真菌必须产生多种杀虫类次生代谢产物，才能够完成其完整的生命周期[31]。同时，部分昆虫病原真菌也可作为植物内生菌，在植物组织中存活并完成部分生命周期，而不会对宿主植物产生负面效应。在过去，许多种内生真菌被发现可以降低植食性害虫对植物的危害，这是由于不同作用机制导致，包括植物防御系统的激活，从初级代谢前体化合物中产生次级防御代谢产物的营养物质吸收增加或真菌杀虫代谢产物产生[33]。此外，在农业上使用真菌杀虫剂防治害虫时，分析真菌杀虫剂对天敌造成的危害也至关重要，这也符合农业害虫综合防控IPM发展的具体要求。

2 木霉菌在农业生态系统中的应用

全世界已鉴定木霉属真菌约377种[34-35]，目前主要用于农业生物防治剂和不同行业所需酶的生产[36]。近年，在其他行业的应用也不断增加，如作为植物生长和对非生物胁迫耐受性的促进剂[37-38]、生物肥料[39]、生物技术基因源[40]等。

木霉菌与植物相互作用主要表现为根部内生真菌，受水杨酸SA介导的植物防御反应，木霉菌只能定植于植物的最外层，从而阻止病原菌到达维管束，表现为系统性病原体[41-42]。通过这种方式，木霉菌也可以激活植物的系统性防御反应，抵御害虫和病原体的攻击[42]。目前，应用最多的就是将木霉菌孢子用于作物种子或繁殖体的包衣剂，播种或移栽期间通过灌溉和拌土等方式达到最大化的成功定植，以控制病虫害[43-44]。木霉菌基因组比较分析也表明了根际真菌病原菌的大量存在，加上分泌丰富的营养物质，导致木霉菌最终与根系相互作用，定植于根部[45-46]。木霉菌寄生需要多个信号来形成寄生的特异性结构和产生必要的酶，通常木霉菌通过识别病原体细胞壁寡甲壳素寡糖；然后，开始以一种针对性的方式向化学信号方向生长；菌丝接触后，木霉菌菌丝缠绕在病原体菌丝周围，开始分泌细胞壁降解酶（几丁质酶、-1, 3-葡聚糖酶）；随着病原菌细胞壁的降解形成空隙，木霉菌通过空隙从真菌体内获取生长所必须的营养物质[47-48]。此外，木霉菌还能寄生线虫的卵、第1龄幼虫[49-50]及昆虫的全周期，甚至还可以抑制人体某些病害[51]。

3 木霉菌对害虫的直接防控

木霉菌通过寄生或产生杀虫次级代谢产物、拒食化合物和驱避代谢产物直接防控害虫。与其他害虫病原菌作用机制基本一致，木霉菌可以主动寄生昆虫，并直接从昆虫体内获取各种营养物质。绝大多数木霉菌的研究仍处于室内研发阶段，研究结果表明：木霉菌针对不同害虫及不同作用时间，对害虫的控制效率有差异。如：长枝木霉（）和哈茨木霉（）分别寄生于B型烟粉虱（）和热带臭虫（），5 d内均可导致40%的害虫死亡[52]，14 d后死亡率超过90%[53]；同样，不同种类木霉菌15 d后可导致90%椰子二疣犀甲（）死亡[54]。此外，将长枝木霉孢子液喷施后，既可提高茄子56%的产量，还可导致50%茄黄斑螟（）死亡[55]。而多种木霉菌均可产生杀虫类次级代谢物，并将其释放到环境中降低害虫危害，如深绿木霉（）[56]。研究最多的哈茨木霉产生代谢物peptaibols类抗菌肽（小阳离子肽家族）[57]在抑制病原体生长方面非常有效，在萝卜、豌豆及番茄等作物上应用对赤拟谷盗（）、棉蚜（）[58]等害虫的致死率高达100%；木霉菌还能产生挥发性杀虫类次级代谢物，如6-戊基-α-吡喃酮，在48 h内对叶螨的致死率高达100%[59]。木霉菌产生的杀虫类次生代谢物对飞蝗[60]、食心虫（）和粉红色棉铃虫（）[7]均有显著的直接防控作用。

另一方面，绿色木霉（）、桔绿木霉（）和深绿木霉也可产生拒食性化合物，如几丁质酶致使鳞翅目幼虫取食量降低，从而导致外米缀蛾（）[61]、棉铃虫[62]和家蚕（）[63]在7 d内死亡率达50%；而其他具有拒食活性化合物如游离脂肪酸亚油酸甲酯和亚油酸，对半翅目昆虫也有抑制作用[64]；此外，木霉硒纳米颗粒作为斜纹夜蛾（）幼虫的拒食剂，可显著降低斜纹夜蛾的种群[65]；深绿木霉通过水杨酸JA介导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-酮作为草地贪夜蛾的1种抗食性代谢物可明显减少草地贪夜蛾对玉米的取食[66]。

此外，研究表明哈茨木霉、绿色木霉、橘绿木霉等挥发性有机化合物VOCs起到驱避害虫的作用，有效降低了害虫对植物资源的危害。通过真菌孢子在土壤中的应用，因木霉菌产生的驱避代谢产物导致台湾乳白蚁（）不能进行筑巢[67]；在贮藏大豆种子中施用木霉菌孢子，也能使菜豆象（）对大豆种子的损耗减少达10%[68]。

4 木霉菌对害虫的间接防控

木霉菌可以激活植物系统防御反应、吸引天敌和寄生昆虫共生微生物，间接的作为植物内生真菌或真菌的重寄生真菌。微生物与植物间的相互作用触发了植物的2种防御机制，保护植物免受危害。第1种为系统获得抗性SAR，这种机制由局部感染触发，在整个植物中提供对不同病原体生物的长期抗性，这与致病相关蛋白PR的合成相关联，PR由编码水杨酸SA生物合成相关酶的基因上调介导[69]；第2种为诱导系统抗性ISR，与茉莉酸JA和乙烯et的合成有关，由转录因子MYC2和ERF介导[70-71]，这种抗性诱导了一种启动状态，当受到病原体攻击时增强了植物防御基因的表达[72]。木霉菌诱导植物进入防御反应启动状态后，植物对病原体的攻击反应更快，防御也更强，这主要是通过降低效应物触发敏感性和增强效应物触发免疫实现的[73]。与其他微生物相同，木霉菌在植物根部定植，能够激活植物系统性防御反应，从而对病原菌和害虫的防御，这主要由植物激素水杨酸SA和茉莉酸JA介导[74-75]。绿色木霉和甘氏木霉分别激活系统性植物防御系统，可使绿龟甲（）[76]和拟尺蠖（）[77]的摄食量分别减少25%。在番茄植株中，通过哈茨木霉激活在SA介导的防御系统，可以导致35%的B型烟粉虱死亡率[41]。深绿木霉可使棉叶片产生蛋白酶抑制剂，导致棉铃虫等鳞翅目幼虫25 d内达100%死亡率[78]。类似地，在兰花属植物中JA介导反应刺激叶片中的鞣质、根皮鞣质、类黄酮、甾体、糖苷和生物碱的产生，从而阻止粉蚧（spp.）的取食[7]。

植物或大量与植物相关的生物群体间往往需要多营养级的协同作用，包括植食性昆虫和土壤微生物，木霉菌作为营养级的重要组成部分[79]，木霉菌根部定植激活植物的系统防御反应导致次生防御代谢产物在植物组织中积累。其中，一些代谢物可能具有趋避性的挥发性有机化合物，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），可使草地贪夜蛾对玉米叶片的消耗减少75%[79]；此外，木霉菌定植植物根系后也会产生针对害虫的间接防御反应，此时植物会释放有机化合物吸引害虫的寄生蜂或捕食者，如6-戊基-α-吡咯烷酮和4-戊基-α-吡咯烷酮均对寄生蜂黑唇姬蜂（）具有引诱作用[79]，深绿木霉诱导玉米产生单-C10和C15倍半萜及其他挥发性有机化合物释放，吸引黑唇姬蜂雌虫[66]。通过在番茄根部定植诱导SA介导的系统抗性，哈茨木霉、长枝木霉及深绿木霉在25 d内可导致100%的马铃薯蚜虫个体死亡，这是由于植物产生的挥发性有机化合物如水杨酸甲酯MeSA，吸引了特定的寄生蜂（）[80]和捕食蚜虫的盲蝽象（）[81]。对于其他蚜虫来说，田间条件下的哈茨木霉引起JA介导的系统抗性，产生释放有机化合物（Z）-3-己烯-1-醇，吸引蚜虫天敌异色瓢虫（），使害虫种群数量减少22%[82]。类似针对葡萄园中不同种类的桃金娘和瓢虫，木霉菌引起JA介导的VOCs产生，从而吸引半翅目拟蝇科寄生蜂[83]；受木霉菌诱导植物多种防御反应相关基因的转录变化，导致前期参与防御反应的基因上调或编码保护酶（蛋白酶抑制剂、苏氨酸脱氨酶、亮氨酸氨基肽酶、精氨酸酶及多酚氧化酶）在防御级联下游被激活，最终改变了番茄的代谢途径，导致挥发性有机化合物VOCs的产生和释放吸引了阿尔蚜茧蜂（），降低了斜纹夜蛾、大戟长管蚜（）的危害[78]。

为防治害虫，木霉菌寄生昆虫共生真菌的特性也可以利用。光滑足距小蠹（）是危害榛子（）的重要害虫，雌虫在寄主植物木质部形成通道，幼虫和成虫都只能以这些木腐菌为食，因此，它们需要这种共生营养关系才能生存，榛子枝接种哈茨木霉, 棘胞木霉（）和深绿木霉通过直接寄生共生真菌显著减少光滑足距小蠹的数量[84]。切叶蚁是热带和亚热带农林生态系统中一种重要的经济害虫，这些蚂蚁利用叶片碎片培养真菌，木霉菌在体外对昆虫共生真菌（）[85]和（sp.）的寄生作用已得到证实。从离体培养结果来看，（）在小麦麸皮上寄生共生真菌（）导致40 d内100%的蚂蚁因饥饿而死亡[86]。

此外，木霉菌可以作为昆虫肠道微生物群的有效拮抗剂。康氏木霉（）可使亚洲玉米螟肠道菌群减少，最终导致亚洲玉米螟第4龄幼虫12 d内达30%死亡率[87]。最近，相关研究表明哈茨木霉会导致玉米释放挥发性有机化合物（Z）-3-己烯-1-醇，该化合物也可作为植食性昆虫的拮抗剂[88]。

5 展 望

农业害虫作为农作物减产的重要因素，过去一直依赖化学杀虫剂来降低害虫危害，对生态环境和食品安全造成了巨大压力，开发和利用环保型生物制剂已成为可持续农业发展的重要趋势。目前，多种真菌类防治剂应用于农业有害生物防控试验中，均获得比较理想的防控试验效果，但在实际生产应用中使用份额占比还比较小，这与农业种植和生产者对化学农药长期使用形成依赖性及对新型生物农药认识不足和接受程度低有关。近年来，伴随着真菌类杀虫剂使用率逐年上升，化学杀虫剂使用率开始呈现下降趋势，如木霉菌，由于其对植物病原真菌的寄生等作用机制，作为生物防治剂在农业有害生物防治上被广泛研究和应用。近年来，研究表明木霉菌对农业害虫具有比较理想的防控效果，对多种农业害虫室内防控效率高达100%，其作用方式具有直接寄生、产生杀虫次级代谢物、拒食化合物和驱避代谢产物的直接防控作用，也具有通过激活植物系统防御反应、吸引天敌、抑制害虫生长和寄生害虫共生微生物的间接防控作用，因此，木霉菌类生物制剂被认为是一种比较理想的生物防治剂。

然而，值得注意的是用木霉菌作为真菌类杀虫剂进行的绝大多数试验研究结果，都是在可调控的室内实验条件下进行的，实际生产应用效果需在田间进行更多的试验调查来加以验证。木霉菌等真菌类生物防治剂在野外应用较少的原因，可能是野外实地应用试验的防控效果不明显或与室内试验结果差异显著，因此，关于木霉菌野外应用的报道较少。这也间接说明可调控的室内实验条件，不能准确地反映野外田间的土壤质地、温湿变化和附生微生物群落等条件。此外，还应开展平行试验来验证木霉菌对天敌或非有害昆虫及本地昆虫内生真菌的安全性，这也符合农业害虫综合防控IPM发展的具体要求。

综上所述，利用木霉菌的直接和间接防控效果，有望成为农业有害生物绿色防控的重要可持续替代品，但其作为农业有害生物的生物防治剂对非有害生物的影响，仍需更多的野外和田间试验加以验证。

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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

付兴飞, 胡发广, 程金焕, 等. 木霉菌防控农业害虫的研究综述[J]. 生物灾害科学, 2022, 45(3): 266-274.

10.3969/j.issn.2095-3704.2022.03.45

2022-06-08

2022-07-04

国家重点研发计划咖啡可可产业链一体化示范项目（2020YFD1001202）和云南省隆阳区咖啡产业科技特派团项目（202004BI090136）

付兴飞（1992—），男，硕士生，主要从事热带亚热带经济作物病虫害综合防控研究，1161003575@qq.com；*通信作者：李贵平，副研究员，lgp7007@163.com。