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Research progress in the control of plant diseases by the combination of Bacillus and fungicides

花匠小妙招
2024-11-14 15:22

黄慧婧, 罗坤. 芽孢杆菌与杀菌剂复配防治植物病害的研究进展[J]. 微生物学通报, 2021, 48(3): 938-947.

HUANG Huijing, LUO Kun. Research progress in the control of plant diseases by the combination of Bacillus and fungicides[J]. Microbiology China, 2021, 48(3): 938-947.

芽孢杆菌与杀菌剂复配防治植物病害的研究进展

湖南农业大学植物保护学院湖南长沙 410128

收稿日期: 2020-05-07; 接受日期: 2020-06-23; 网络首发日期: 2020-10-20

基金项目: 湖南省烟草公司长沙市公司科技项目(20-21A05)

摘要: 芽孢杆菌属包含多种植物病原物的拮抗菌，可广泛用于植物病害防治。然而单独利用生防菌进行生物防治常由于环境因素影响而无法达到较好的防治效果，可通过与低剂量杀菌剂复配使用来提高防治效率。本文对生防芽孢杆菌与杀菌剂复配使用进行植物病害综合防治的研究现状、防效、研究方法等进行综述，芽孢杆菌与杀菌剂复配使用不仅保障了防治效果，还大大减少了化学农药的施用。

关键词: 生防菌杀菌剂芽孢杆菌植物病害农药减量化

Research progress in the control of plant diseases by the combination of Bacillus and fungicides

HUANG Huijing , LUO Kun

College of Plant Protection, Hunan Agricultural University, Changsha, Hunan 410128, China

Received: 07-05-2020; Accepted: 23-06-2020; Published online: 20-10-2020

Foundation item: Science-Technology Project of Hunan Tobacco Company Changsha Branch (20-21A05)

Abstract: Bacillus spp. contains a variety of antagonistic bacterias of plant pathogens, which can be widely used in the control of plant diseases. However, the use of biocontrol bacteria alone for biological control is often unable to achieve a better control effect due to the influence of environmental factors, and the control efficiency can be improved by combined use with low-dose fungicides. The research status, control effects and research methods of integrated control of plant diseases by the combination of biocontrol Bacillus and fungicides were reviewed in this paper. The combined use of Bacillus and fungicides can not only ensure the control effect, but also can greatly reduce the application of chemical pesticides.

Keywords: biocontrol bacteria fungicides Bacillus plant diseases pesticide reduction

植物病害带来的巨大经济损失一直影响着我国农业发展，植物病害防治是我国农业生产中一项重要的工作。目前，化学防治依然是防治植物病害的主要方式。随着化学药剂的大规模施用，环境污染与日俱增，病原微生物抗性的产生不可避免，同时食品安全问题日益受到关注。随着农药减量化观点的提出，生物防治的作用更加受到期待。植物病害的拮抗微生物对其具有抗生作用、竞争作用、重寄生作用、诱导植物系统抗性等拮抗机制[1]。利用拮抗菌防治植物病害具有安全环保、对病原菌高度特异性等优点[2]，有利于可持续发展。在植物病害的生防菌中，木霉属(Trichoderma spp.)、芽孢杆菌属(Bacillus spp.)、假单胞菌属(Pseudomonas spp.)等较为常见[3]。除此之外，还有一些不常见的生防菌也正在被不断研究，例如罗坤等[4]筛选出的一株伯克氏属(Burkholderia sp.)拮抗细菌对番茄青枯病的防治具有重要意义。

芽孢杆菌属生防菌对多种植物病原物具有拮抗效应，可用于多种植物病害的防治工作。然而，由于受环境条件的多变性和土壤系统的复杂性影响，单用生物防治难以有效防治植物病害[5]。生防菌与杀菌剂复配使用可弥补二者各自的局限性和弊端，成为一种切实可行且环境友好的防治方法。生防菌与杀菌剂的相容可通过耐药生防菌株的选育来实现，获得耐药菌株可用含药培养基对特定杀菌剂的天然耐药性拮抗菌株进行筛选[6]，或通过紫外线诱变[7]等多种方式。利用生防菌与杀菌剂共同作用，可有效实现对植物病害的综合防治。

1 杀菌剂复配的协同作用

在防治植物病害时，当2种或2种以上处理共同作用的防效大于它们各自单独作用的防效之和时，这些处理方式之间具有协同作用(增效作用)。国内外已有大量利用协同作用复配药剂的成功案例。Colby曾介绍常用于评价除草剂复配协同作用的Gowing法并将其简化，同样适用于杀菌剂复配所产生效应的判断：当2种杀菌剂复配时该模型为“E=X+Y−XY/100”，其中X为a剂量的药剂A单独使用时对病原菌的防效，Y为b剂量的药剂B单独使用时对病原菌的防效，计算所得E为预期防效；当实际防效大于E时，2种杀菌剂之间具有协同作用，反之为拮抗作用[8]。Wadely提出的增效系数法也常用于评价复配杀菌剂中不同药剂间的互作：增效系数(SR)=EC50(exp)/EC50(obs)，EC50(exp)=(x+y)/ [x/EC50(x)+y/EC50(y)]；其中x、y分别为药剂X、药剂Y的浓度，EC50(x)、EC50(y)分别为药剂X和药剂Y的半最大效应浓度，EC50(exp)、EC50(obs)分别为复配药剂的预期半最大效应浓度与实际半最大效应浓度；当SR > 1.5时混配药剂中的不同药剂间表现为协同作用，0.5≤SR≤1.5时表现为相加作用，SR < 0.5时则表现为拮抗作用[9]。此外，共毒系数法[10]、Horsfall法[11]、等效线法[12]等也可用于杀菌剂复配效果的评价。利用生防菌与杀菌剂之间的协同作用可提高对植物病害的防治效率，一方面使生防菌的防治效果更加稳定，另一方面可显著减少农药用量[13]，实现防效与环保的双赢。

2 芽孢杆菌在植物病害防治中常见的作用机制

从国内外学者的大量研究中可了解到生防芽孢杆菌具有多样的防病机制，可通过一种或多种防病机制作用于植物病害。如表 1所示，这些作用机制实现的防病效果与杀菌剂的防病效果有些相同，有些与之互补。

表 1　芽孢杆菌与杀菌剂的作用机制Table 1　Mechanisms of action of Bacillus and fungicides

防治因子
Factors of prevention 作用机制
Mechanisms of action 对病原物
To the pathogens 对寄主植物
To the host plants 杀菌剂
Fungicides 影响细胞壁结构[14]，破坏细胞膜通透性[15]
By affecting the structure of the cell wall[14] and destroying the permeability of the cell membrane[15]
抑制毒素形成[16]
By inhibiting the formation of toxins[16]
影响必需蛋白的合成[17]
By affecting the synthesis of essential proteins[17]
抑制呼吸代谢与能量合成[18]
By inhibiting respiratory metabolism and energy synthesis[18] 诱导系统抗性(诱导病程相关蛋白的合成[19])
By inducing systemic resistance (by inducing the synthesis of pathogenesis-related proteins[19])
降低植物对病原菌的敏感程度[20]
By reducing the sensitivity of plants to pathogens 生防芽孢杆菌
Biocontrol Bacillus 竞争作用
Competitive effect
抗生作用
Antibiosis诱导系统抗性
Induced systemic resistance, ISR
促进植物生长
Growth-promotion effect

在芽孢杆菌对各种植物病害的抑制作用中，竞争作用、抗生作用、促进植物生长和诱导系统抗性(Induced Systemic Resistance，ISR)是比较常见的防病机制。

2.1 竞争作用

竞争作用是生防类芽孢杆菌常见的一种拮抗机制。生防菌可通过夺取营养和占据优势空间位点阻止病原菌从植物的自然孔口和伤口入侵，干扰病原菌在植物体内与根际的定殖。刘丁在研究萎缩芽孢杆菌(B. atrophaeus)对黄曲霉(Aspergillus flavus)的抑制机理中发现，无菌上清液与高压灭菌后培养液的抑菌率(分别为27.10%与19.19%)明显低于培养原液与菌体悬浮液的抑菌率(分别为79.80%与71.72%)，说明在萎缩芽孢杆菌对黄曲霉的拮抗关系中存在明显的竞争作用[21]。一些生防菌能通过形成生物膜来夺取病原菌入侵所必需的侵染位点，使植物免受病害侵袭。Luo等2018年在研究工业生防菌多粘芽孢杆菌(B. polymyxa) HY96-2菌株的生防机理时，发现其具有能通过调控群体感应引起生物膜形成的LuxS基因[22]。还有一些拮抗菌能产生嗜铁素，大量夺取病原菌生长环境中的铁离子，致使病原菌无法成功定殖。陈思宇在水稻纹枯病拮抗菌的筛选与研究中，得到的11株拮抗菌(其中10株均为芽孢杆菌属)都能产生嗜铁素[23]，可见产生嗜铁素是生防芽孢杆菌一种常见的拮抗机制。王涤非等从柿树根部分离出一株地衣芽孢杆菌，通过铬天青S (Chrome Azurol S，CAS)平板检测发现其具有较强的产嗜铁素能力，有望用于生物防治[24]。

2.2 抗生作用

生防芽孢杆菌的代谢产物中通常存在多种溶菌物质与抗菌物质，包括核糖体合成的抗菌蛋白(几丁质酶、葡聚糖酶、细菌素等)与非核糖体合成的抗生素(包括伊枯草菌素、芬枯草菌素、枯草菌脂肽)等[25]。Maachia等研究得出，枯草芽孢杆菌B27与B29菌株能产生β-1, 3葡聚糖酶与几丁质酶，参与病原菌的溶解，对葡萄灰霉病与白粉病具有良好的防控效果[26]。除了产生细胞壁降解酶，脂肽类抗生素也是生防芽孢杆菌常见的代谢产物。Nikolić等以乙酸乙酯萃取法对2株解淀粉芽孢杆菌(B. amyloliquefaciens)与一株短小芽孢杆菌(B. pumil)培养上清液中的脂肽进行提取，所得脂肽粗提物(Crude Lipopeptide Extracts，CLEs)对丁香假单胞菌(Pseudomonas syringae)有明显抑制作用[27]。Dimkić等在实验中证实这3株芽孢杆菌培养上清液的CLEs主要由表面活性素、丰源素A和伊枯草菌素A组成[28]。一些能分泌多种次生代谢产物的芽孢杆菌已成功商业化，例如能产生抗菌脂肽(表面活性物质、伊枯草菌素、丰源素)、聚酮(大乳蛋白、杆菌烯和艰难素)和挥发物(3-羟基丁酮/2, 3-丁二醇)的解淀粉芽孢杆菌FZB42菌株[29]。

2.3 促进植物生长

一些生防菌在抑制病原菌的同时，还能合成多种生长激素类物质促进植物生长。芽孢杆菌的代谢物中常见的促生物质有吲哚乙酸(Indoleacetic Acid，IAA)、脱落酸(Abscisic Acid，ABA)、细胞分裂素(Cytokinins)、赤霉素(Gibberellin，GA3)和亚精胺(Sperdimine)等[30]。Valenzuela-Ruiz等分离出一株对小麦根腐病具有潜在生防作用的副地衣芽孢杆菌(B. paralicheniformis) TRQ65菌株并对其基因组进行测序，发现其不仅有合成抗生素的相关基因，还具备合成生长素的能力，通过盆栽试验验证其促生作用确实存在[31]。除了合成生长激素，一些芽孢杆菌还能以解钾、解磷、固氮[32]的途径实现对植物的促生作用，或通过诱导植物生长相关基因表达等方式[33]促进植物生长。

2.4 诱导系统抗性(Induced Systemic Resistance, ISR)

随着对植物诱导抗性的不断深入研究，国内外研究者们发现大量植物内生菌与根围促生菌(Plant Growth-Promoting Rhizobacteria，PGPR)能诱导植物获得系统抗性。ISR在芽孢杆菌的生物防治中也是一种常见的防病机制，不仅安全可靠、对多种病原菌有效，而且具有持久的抗病效果[34]。芽孢杆菌一般通过诱导植物产生病程相关蛋白或诱导植物细胞壁结构变化等途径实现ISR[35]。Liu等2019年提出，一株解淀粉芽孢杆菌在大豆疫病的防治中可通过诱导活性氧暴发、NO生成(NO可提高植物抗逆性，在ISR中发挥重要作用)、胼胝质沉积和木质化来诱导大豆获得系统抗性[36]。有研究表明，芽孢杆菌还可诱导与几丁质酶、β-1, 3葡聚糖酶等有关的病程相关蛋白迅速表达[37]。

3 芽孢杆菌与杀菌剂复配防治植物病害

生防菌与杀菌剂的复配展现了生防剂与化学药剂间潜在的相容性。低剂量杀菌剂的使用在一定程度上抑制病原菌的同时可帮助生防菌稳定定殖，成为优势菌种[38]。芽孢杆菌对多种外界有害因子具有较强的耐受性和广谱的抑菌能力，分布空间广泛，而且大多数芽孢杆菌对人体无害。目前已有许多研究将芽孢杆菌与杀菌剂复配，包括枯草芽孢杆菌、多粘芽孢杆菌、解淀粉芽孢杆菌、蜡状芽孢杆菌(B. cereus)等多个菌种，这些研究经过验证能成功用于防治多种植物病害，其应用前景得到越来越广的拓展。

3.1 防治真菌性植物病害

在植物病害中，真菌病害所占比例最高，真菌杀菌剂是防治植物病害最为通用的类型。由于杀菌剂具有专一性，大部分真菌杀菌剂通常不会对细菌有效，这使得生防细菌与各种真菌杀菌剂复配具有较大的相容可能性。在国内外对芽孢杆菌与杀菌剂复配防治植物病害的研究中，用于防治真菌性病害的研究占了极大一部分比例。Ji等通过体外培养与盆栽试验研究了氟醚菌酰胺与甲基营养型芽孢杆菌TA-1菌株复配对番茄灰霉病的防效，体外培养试验结果表明，氟醚菌酰胺与甲基营养型芽孢杆菌TA-1菌株复配对灰霉菌菌丝生长的抑制效果明显强于二者单独使用的抑制效果；而盆栽试验同样展现出协同作用：联合施用108 cfu/mL的甲基营养型芽孢杆菌TA-1与50 g/hm2氟醚菌酰胺的防效可达到70.16%，较单独施用108 cfu/mL的甲基营养型芽孢杆菌TA-1菌株(防效为58.80%)和单独使用50 g/ha氟醚菌酰胺(防效为56.10%)有明显提高[39]。Kim等将解淀粉芽孢杆菌JCK-12菌株与杀菌剂联合使用对小麦赤霉病进行防治，实验结果表明JCK-12菌株的加入对化学杀菌剂起到增敏作用，温室防效达到96.40%，田间防效达到91.00%[40]。为防治番茄镰刀菌根腐病，Omar等将一株巨大芽孢杆菌制成106 cfu/mL菌悬液与多菌灵复配，当多菌灵浓度为10 μg/mL时防效可达84.00%[41]。陈志谊等将枯草芽孢杆菌Bs-916菌株与井冈霉素复配防治水稻纹枯病的研究影响甚广，研究表明，井冈霉素在复配剂中减少了一半的剂量，却能对水稻纹枯病实现更佳的防治效果；低剂量的井冈霉素不仅能与芽孢杆菌形成协同的防治效果，还能帮助芽孢杆菌更好地定殖[42]。毕秋艳等将一株生防枯草芽孢杆菌与嘧菌酯复配防治葡萄霜霉病，结果表明该组合的菌药间具有协同作用，防效达91.06%−98.92%，在防效相当的前提下减少了约1/3的嘧菌酯剂量，显然可实现农药减量化防治[43]。谢立等将枯草芽孢杆菌Czk-1菌株与根康复配用于防治橡胶根部病害的试验同样展现出明显的协同效果：当用6.46×107 cfu/mL的菌株发酵液与浓度为0.625 3 μg/mL的根康以7:3(体积比)复配时对橡胶红根病菌的抑制效果最佳(防效达76.66%)，当用2.33×108 cfu/mL的菌株发酵液与浓度为0.052 2 μg/mL的根康以7:3复配时对橡胶褐根病的抑制效果最佳(防效达89.32%)[44]。还存在一些芽孢杆菌能与不止一种杀菌剂复配成功的案例，例如Krishnamoorthy等将解淀粉芽孢杆菌B15菌株与肟菌酯∙戊唑醇和多菌灵2种杀菌剂都复配成功，用于防治甘蓝菌核病的田间防效分别达到78.55%和75.75%[45]。当生防菌种无法耐药且能产生具有明显拮抗作用的代谢产物时，可通过将发酵上清液与杀菌剂复配实现增效[46]。还有许多芽孢杆菌与杀菌剂复配防治真菌性植物病害的实例，具体信息如表 2所示。

表 2　芽孢杆菌与杀菌剂复配防止植物病害的具体配方及防效Table 2　Specific formula and control effect of the combination of Bacillus and fungicides to prevent plant diseases

Strains Fungicides Concentration/Dose of biocontrol bacterias and fungicides Diseases to control Control effects Bacillus methylotrophicus TA-1 Fluopimomide 108 cfu/mL & 50 g/hm2 Tomato gray mold Field control effect 70.16%[39] Bacillus amyloliquefaciens JCK-12 Almuri 500-fold dilution of fermentation broth of JCK-12 & 4 000-fold dilution of Almuri Fusarium head blight Field control effect 91.00%[40] Bacillus megaterium c96 Carbendazim 106 cfu/mL & 10 μg/mL Fusarium crown and root rot of tomato Greenhouse control effect 84.00%[41] Bacillus subtilis Bs-916 Jinggangmycin 1010 cfu/mL & 2.5% Jinggangmycin 4.5 kg/hm2 Rice sheath blight Field control effect 82.10%−82.30%[42] Bacillus subtilis HMB-20428 Azoxystrobin 108 cfu/mL & 0.080 μg/mL Grape downy mildew Greenhouse control effect 98.92%[43] Bacillus subtilis Czk-1 “Gen Kang” 6.46×107 cfu/mL & 0.625 3 μg/mL (7:3) Rubber red root Vitro culture control effect 76.66% 2.33×108 cfu/mL & 0.052 2 μg/mL (7:3) Rubber brown root Vitro culture control effect 89.32%[44] Bacillus amyloliquefaciens B15 Nativo 10 mL/L & 1.5 g/L Head rot of cabbage Field control effect 78.55% Carbendazim 10 mL/L & 2 g/L Field control effect 75.75%[45] Bacillus subtilis H158 Azoxystrobin 108 cfu/mL & 56.25 g.a.i/hm2 Rice sheath blight Field control effect 83.60% Pyraclostrobin Field control effect 81.50% Trifloxystrobin Field control effect 79.10%[47] Bacillus subtilis NJ-18 Kresoxim-methyl 5.0×107 cfu/mL & 225 g.a.i/hm2 Rice sheath blight Field control effect 92.7%−100.00%[48] Bacillus subtilis C10-1 Prochloraz 107 cfu/mL & 0.1 mg/L Fusarium oxysporum wilt of banana Vitro culture control effect 94.96%[49] Bacillus subtilis RB14-C Flutolanil 30 mL fermentation broth of RB14-C & 94 μg flutolanil (per basin) Damping-off of tomato Greenhouse control effect 70.00%[50]

3.2 防治细菌性植物病害

目前，芽孢杆菌与杀菌剂复配防治细菌性植物病害的研究实例较少。这可能与芽孢杆菌和杀细菌剂相容难度较大有关，但依然可以通过驯化筛选、紫外诱导、离子束诱变、原生质融合等方式获得耐药生防菌株[51]。Peng等将枯草芽孢杆菌B-001菌株与噻森铜复配用于防治番茄青枯病：在盆栽试验中，灌根处理的2个复配组(50 mg/L噻森铜 & 108 cfu/mL与100 mg/L噻森铜 & 108 cfu/mL)均表现出协同作用，防效明显高于单独施用杀菌剂或生防菌；田间试验结果显示，200 mg/kg噻森铜与B-001菌株复配防效相当于单独使用400 mg/kg噻森铜的药效，而显著高于单独使用200 mg/kg噻森铜的药效[52]。黄小琴等以解淀粉芽孢杆菌Bs2-4菌株筛选出与其相容性较好的杀菌剂硫酸链霉素，复配施用对烟草青枯病的防效明显高于单独使用生防菌或杀菌剂的处理，在减少农药剂量的同时表现出良好的防治效果[53]。于宏安等通过培养皿对峙试验、离体果控病试验、田间试验验证了地衣芽孢杆菌(Bacillus licheniformis)复配苯噻酮对脐橙溃疡病的防效，田间防效可达74.2%[54]。

4 芽孢杆菌与杀菌剂复配的研究方法

在进行生防菌与杀菌剂复配试验时，首先要进行相容性测定[55]以获得相容性最佳的菌药组合与菌药配比，或通过诱变、驯化等方法获得耐药生防菌株。驯化选育一般先将生防菌置于含有较低浓度杀菌剂的平板中培养，然后挑取长势较好的菌落接种至杀菌剂浓度按梯度提高的平板，经过层层梯度不断选育，最后获得耐药菌株[56]。诱变选育则通过物理、化学等因素诱导生防菌株具备耐药性。何文艳通过自然驯化、亚硝基胍(Nitrosoguanidin，NTG)诱变、循环选育获得耐井岗霉素的生防蜡状芽孢杆菌，用于防治水稻纹枯病[57]。于春生等通过紫外-氯化锂复合诱变使生防菌获得了对多菌灵的较强耐受性，有望进行后续的菌药混配[58]。除了使生防菌产生耐药性，提高生防菌对病原菌的拮抗活性也可通过诱变实现。Chen等以常压等离子射流(Atmospheric Pressure Plasma Jet，APPJ)作为诱变原，筛选出一株能产生高量抗生素且对禾谷镰刀菌(Fusarium graminearum)具有强生防性能的枯草芽孢杆菌突变菌株，可成为一株很有前途的生防菌用于农业生产[59]。

在获得耐药生防菌株后，往往还需要通过体外培养试验(常用抑菌圈法或对峙法)、盆栽试验、田间试验来评价菌株与杀菌剂复配的实际防效以及菌药间的互作[60]。可先通过体外培养试验确定防效较好的菌药浓度配比范围作为盆栽试验与田间试验的基础[39]。各组处理通常分为仅施生防菌、仅施杀菌剂、菌药联用，以不施生防菌与杀菌剂作为空白对照；杀菌剂浓度根据田间推荐剂量逐级减少配制，试验时还可分喷雾组与灌根组来测试不同施药方式对防效的影响[52]，有时还需对生防菌的定殖能力进行测试[61]。处理2−3周后对各组植物发病等级进行统计，计算病情指数与防效[62]，再判断菌药间互作效应，用SPSS软件分析显著性差异[63]。由于不确定生防菌与杀菌剂复配的稳定性，还需通过重复试验来验证复配剂是否具备持续稳定的防效。

5 展望

在植物病害防治中，随着人们对高效环保防治方式的不断探索，许多新型药剂正不断被开发。虽然化学防治依然是植物病害防治的主要方式，但农药减量化已成为可持续发展的必然趋势。将生防菌与杀菌剂复配，一方面可大大降低农药成本，减少农药残留、农药对植物的负面影响以及农药对人体的安全风险[64]，同时避免病原菌抗药性的产生；另一方面可提升生防菌防治效果的稳定性，发挥生防菌与杀菌剂的协同作用。芽孢杆菌作为一类抗逆性极强的常用生防菌，可抑制多种植物病原物，目前已逐渐被用于与各种杀菌剂复配的研究，适应于新型药剂的开发趋势，具有十足的应用潜力与广阔的发展前景。芽孢杆菌与农药复配产品正不断被开发[65]，但能实际推广应用于农业生产的还为数不多，可能是由于杀菌剂类型、芽孢杆菌特性和病害的多样性以及田间较为复杂的环境因素致使防效无法在各地区田间都实现稳定。如何保持长久稳定的田间防效是一个关键性问题。充分考虑气候与施药时间、剂型选择、生防菌与杀菌剂的匹配程度等因素，并通过大范围的田间调查与长时间的反复验证也许能解决这一问题。除此之外，有关生防菌与杀菌剂之间协同作用机制的研究还较为稀少，进一步研究此方面问题或许能更大程度地发挥菌药间协同作用的优势。

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