白僵菌和绿僵菌在植物根际的定殖及对几种土传植物病原真菌的抑制作用研究
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摘要
虫生真菌是昆虫的重要自然调节因素，在农、林、卫生害虫生物防治方面发挥了重要作用。金龟子绿僵菌和球孢白僵菌是两类重要的昆虫病原真菌，可寄生多种昆虫，在害虫生物防治中得到广泛的应用。本文通过形态学鉴定、分子标记等方法研究了分离自涡阳、萧县、蒙城三个地区玉米根际土壤的白僵菌，以球孢白僵菌和金龟子绿僵菌为研究对象，探讨了虫生真菌对多菌灵的敏感性，虫生真菌在植物根际的定殖能力，虫生真菌对土传植物病原真菌的抑制作用及不同碳、氮营养对虫生真菌生物学特性和抑菌活性的影响。主要研究结果如下：
1.通过白僵菌选择性培养基从采自安徽省涡阳、萧县、蒙城三个地区的玉米根际土壤中共分离到39个白僵菌菌株，经培养特点、形态特征及rDNA ITS鉴定分离的菌株均为球孢白僵菌（Beauveria bassiana），且不同菌株间的菌落生长直径和分生孢子产生量存在显著差异。
2.通过ISSR-PCR分子标记技术对分离自玉米根际的球孢白僵菌的遗传多样性进行了研究。从40个引物中共筛选出11个多态性高、稳定性好的引物用于正式的扩增分析，在37个菌株中共扩增出83条谱带，其中多态性条带占69条，多态性百分率为83.13﹪。平均每引物扩增条带在7.5条。群体的多态位点百分率（PPL）是83.13﹪，Nei基因多样性指数（H）为0.3169，Shannon信息指数（I）为0.4657。结果表明，分离自安徽省涡阳、萧县、蒙城三个不同地区的球孢白僵菌具有较高的遗传多样性。
3.通过菌丝生长抑制率法测定了球孢白僵菌（B. bassiana）和金龟子绿僵菌（Metarhizium anisopliae）对多菌灵的敏感性。发现球孢白僵菌和金龟子绿僵菌不同菌株对多菌灵的敏感性存在一定的差异。在供试的球孢白僵菌菌株中，菌株GY~(-1)7的EC_(50)值最大，GY-6的EC_(50)值最小。在供试的金龟子绿僵菌菌株中，Ma55菌株的EC_(50)值最小，对多菌灵的敏感性最强，其次是Ma27菌株，Ma10菌株的EC_(50)值最高。
4.在含多菌灵平板上，通过贴接菌丝块法和涂分生孢子法定向筛选获得了球孢白僵菌和金龟子绿僵菌抗多菌灵菌株，并测定了不同抗性菌株对多菌灵的抗性水平。测定结果表明，在球孢白僵菌抗多菌灵菌株中，BC-4菌株的EC_(50)值最大，其EC_(50)值为258.7711，对多菌灵的抗性水平最高，达到242.11，BC-3菌株的EC_(50)值最小，其EC_(50)值为18.6311，抗性水平最低。在金龟子绿僵菌抗多菌灵菌株中，MC-2菌株的EC_(50)值最大，其EC_(50)值为397.0643，对多菌灵的抗性水平达到102.35；MC-4菌株的EC_(50)值最小，其EC_(50)值为149.5440。研究了球孢白僵菌和金龟子绿僵菌抗多菌灵菌株的菌丝生长速率和产孢能力的差异，发现球孢白僵菌和金龟子绿僵菌不同抗性菌株间的菌丝生长速率和产孢能力均存在一定的差异，抗性菌株的生长速率均比对照敏感菌株（亲本菌株）小，产孢能力均比对照敏感菌株要强，但不同菌株间存在一定的差异，在球孢白僵菌抗性菌株中，BC-4菌株的分生孢子产生量最大，在金龟子绿僵菌抗性菌株中，MC-2菌株的分生孢子产生量最大。
5.采用分生孢子悬浮液蘸根法研究了球孢白僵菌抗多菌灵菌株BC-8菌株和金龟子绿僵菌抗多菌灵菌株MC-2菌株在植物根际的定殖能力及对根际微生物的影响。结果显示，BC-8菌株和MC-2菌株均可以在玉米、棉花外根际和根表定殖，但在玉米、棉花根内未分离到供试菌株。BC-8菌株和MC-2菌株对植物根际微生物的数量都有一定程度的影响，尤其以前期影响较为明显，随着时间的推移，影响减弱。
6.在实验室条件下，研究了金龟子绿僵菌和球孢白僵菌对几种土传植物病原真菌的拮抗作用及其机制。对峙培养结果表明，金龟子绿僵菌和球孢白僵菌对供试的植物病原真菌均有抑制作用，其中绿僵菌以Ma55的制效果最好，白僵菌以Bb2092的效果最好。在培养基中加入Ma55和Bb2092不同浓度的分生孢子悬浮液，当浓度为106cfu·mL~(-1)时，对植物病原真菌菌丝生长具有明显的抑制作用。Ma55和Bb2092液体振荡培养获得的无菌发酵液对供试的植物病原真菌菌丝生长都有较好的的抑制作用，对植物病原真菌的分生孢子（菌核）产生及分生孢子（菌核）萌发也都有一定的抑制作用。显微镜观察未发现金龟子绿僵菌和球孢白僵菌与植物病原真菌菌丝间有重寄生现象。上述结果显示，虫生真菌对供试植物病原真菌的拮抗机制主要是营养竞争、空间竞争及抗生作用。
7.研究了不同碳源和氮源对球孢白僵菌和金龟子绿僵菌菌丝生长、分生孢子产生量、菌丝生物量及其次生代谢产物的抑菌活性。结果表明，虫生真菌对单糖、双糖、多糖等碳营养及有机氮和无机氮等氮营养均能够利用，但利用程度存在一定差异。代谢液的抑菌活性实验结果表明，不同处理获得的球孢白僵菌发酵液对供试的5种镰刀菌菌丝生长均有不同程度的抑制作用，在碳源发酵液中，甘油的抑菌效果最好，乳糖的抑菌效果最差。在氮源发酵液中，硫酸铵的抑菌效果最好，脲的抑菌效果最差；不同处理获得的金龟子绿僵菌代谢液对植物病原真菌菌丝生长均有较好的抑制作用，在碳源发酵液中，白砂糖的抑菌效果最好，乳糖的抑菌效果最差。在氮源发酵液中，蛋白胨的抑菌效果最好，脲的抑菌效果最差。
Entomogenous fungi are an important regulator of insect populations and they spreadwidely in agro-ecosystems and play an important role for biological control of crop,orchard, forest and medical insects. Metarhizium anisopliae and Beauveria bassiana aretwo most important entomogenous fungi, which has a wide range of insect hosts and hasbeen widely used for fungal insecticides. In this paper, some isolates from maizerhizosphere soil collected from Guoyang, Xiaoxian and Mengcheng, north Anhui wereidentified as B. bassiana by both morphological method and rDNA ITS sequenceanalysis. They and some M. anisopliae isolates were tested for their sensitivity tocarbendazim, the colonization ability in plant rhizosphere, the inhibition on soil-borneplant pathogenic fungi, and the effects of different carbon and nitrogen sources on theirbiological characteristics and anti-fungal activity. The results were as follows:
1. With selective medium, thirty-nine strains of Beauveria were isolated from maizerhizosphere soil, collected from Counties of Guoyang, Xiaoxian, and Mengcheng in thenorth of Anhui province. The strains were classified and identified as B. bassiana by bothmorphological and molecular (rDNA ITS sequence analysis) means. The colony diameterand conidia number of different strains were tested in vitro and showed significantdifference.
2. The genetic diversity of thirty-seven B. bassiana strains isolated from maizerhizosphere was estimated using inter-simple sequence repeats (ISSR) markers. Elevenamong forty ISSR primers were chosen for their reproducibility and high polymorphism.Each primer resulted in7.5markers and totally83fragments were amplified, in which69(83.13%) were polymorphic. Genetic diversity analysis revealed a relatively high level ofintraspecific genetic diversity of B. bassiana. The percentage of polymorphic loci (PPL)was83.13﹪, Nei’s genetic diversity (H) was0.3169and Shannon’s information index (I)was0.4657. It suggested that the thirty-seven B. bassiana strains had highly geneticdiversity.
3. The sensitivities of B. bassiana and M. anisopliae to carbendazim were studiedby mycelial growth inhibition rate method. The results showed that the sensitivities ofB. bassiana and M. anisopliae to carbendazim had some differences. Among the testedstrains of B. bassiana, the EC_(50)value of GY~(-1)7was the highest, but that of GY-6wasthe lowest. Among the tested strains of M. anisopliae, the EC_(50)value of Ma55was thelowest, followed by Ma27, while the EC_(50)value (4.05) of Ma10was the highest.
4. The resistant level of the carbendazim-resistant strains of B. bassiana and M.anisopliae were studied, by mycelium and conidium oriented screening. The resultsshowed that the resistant level of BC-4was the highest among thecarbendazim-resistant strains of B. bassiana, with EC_(50)and the resistant level at258.77and242.11, respectively. The resistance level of BC-3was the lowest amongthe carbendazim-resistant strains of B. bassiana, with EC_(50)at18.63. The resistantlevel of MC-2was the highest among the carbendazim-resistant strains of M.anisopliae, with EC_(50)and resistant level was397.06and102.35, respectively. TheEC_(50)of MC-4was the smallest (149.54). The mycelia growth rate and sporulationability of the carbendazim-resistant mutants were studied too. It showed that themycelium growth rate and sporulation capacity had some differences among differentcarbendazim-resistant mutants. The growth rate of resistant mutants was smaller thanthat of the control (parent strain), but sporulation ability was stronger than that of thecontrol (susceptible strain), and different strains had some differences. Among thecarbendazim-resistant strains, the sporulation of BC-4mutant and MC-2mutant wasthe highest.
5. The colonization ability and the influence on rhizosphere microorganisms of thecarbendazim-resistant mutants BC-8and MC-2in the plant rhizosphere were studied bymeans of dipping in conidial suspension. BC-8and MC-2were detected from outerrhizosphere and root surface of maize and cotton, but not from inside the roots. Itsuggested that BC-8strain and MC-2strain had a certain influence on the number of plantrhizosphere microorganisms, especially at the beginning, but the effects decreased withtime.
6. Under laboratory conditions, the inhibition of M. anisopliae and B. bassianaagainst Fusarium oxysporium f. sp. vasinfectum and other soil-borne plant pathogenicfungi, and its mechanism were studied in vitro by dual culture, cup-plate test andmicroscopic examination. The results of dual-culture test showed that among three M.anisopliae isolates and four B. bassiana isolates which all displayed obvious inhibition onthe tested soil-borne plant pathogenic fungi, Ma55and Bb2092resulted in the highestinhibition. On the PDA plates mixed with different concentrations of conidial suspensionof Ma55and Bb2092, the inhibition rate by the suspension of106conidia per milliliterswas the highest to all tested fungi. The inhibition on mycelia growth of the tested fungi bysterile fermented broth of M. anisopliae and B. bassiana shake culture was obvious, andthose to production and germination of their conidia (sclerotia) were also significant. No hyperparasitism of M. anisolpiae and B. bassiana on the hyphae of the tested fungi wasobserved microscopically. All these evidences suggested that the inhibitory mechanisms ofM. anisopliae and B. bassiana against the pathogen of soil-borne plant diseases weremainly competition to nutrition, space and antibiosis.
7. The biological characteristics of B. bassiana and M. anisopliae were compared indifferent carbon sources and nitrogen sources by measuring the mycelium growth, drymycelium biomass and conidia yield. The results showed that B. bassiana and M.anisopliae could use many carbohydrate and nitrogen sources for the mycelia growth. Bymeans of mycelium growth rate, the inhibitory rates of metabolic liquid cultured withdifferent carbon sources and nitrogen sources were tested. The anti-fungal assay of thesecondary metabolites of B. bassiana showed that the metabolic liquid cultured withdifferent carbon sources and nitrogen sources had significant difference on the5testedstrains of Fusarium. Among the metabolic liquid, the inhibitory rates of those withglycerol and ammonium sulfate as carbon and nitrogen source were the highest and thosewith lactose and urea as carbon and nitrogen source were the lowest. The anti-fungal assayof the secondary metabolites of M. anisopliae revealed that secondary metabolitesproduced in the culture with sucrose as the carbon source and/or the peptone as thenitrogen sources was the highest.
1.通过白僵菌选择性培养基从采自安徽省涡阳、萧县、蒙城三个地区的玉米根际土壤中共分离到39个白僵菌菌株，经培养特点、形态特征及rDNA ITS鉴定分离的菌株均为球孢白僵菌（Beauveria bassiana），且不同菌株间的菌落生长直径和分生孢子产生量存在显著差异。
2.通过ISSR-PCR分子标记技术对分离自玉米根际的球孢白僵菌的遗传多样性进行了研究。从40个引物中共筛选出11个多态性高、稳定性好的引物用于正式的扩增分析，在37个菌株中共扩增出83条谱带，其中多态性条带占69条，多态性百分率为83.13﹪。平均每引物扩增条带在7.5条。群体的多态位点百分率（PPL）是83.13﹪，Nei基因多样性指数（H）为0.3169，Shannon信息指数（I）为0.4657。结果表明，分离自安徽省涡阳、萧县、蒙城三个不同地区的球孢白僵菌具有较高的遗传多样性。
3.通过菌丝生长抑制率法测定了球孢白僵菌（B. bassiana）和金龟子绿僵菌（Metarhizium anisopliae）对多菌灵的敏感性。发现球孢白僵菌和金龟子绿僵菌不同菌株对多菌灵的敏感性存在一定的差异。在供试的球孢白僵菌菌株中，菌株GY~(-1)7的EC_(50)值最大，GY-6的EC_(50)值最小。在供试的金龟子绿僵菌菌株中，Ma55菌株的EC_(50)值最小，对多菌灵的敏感性最强，其次是Ma27菌株，Ma10菌株的EC_(50)值最高。
4.在含多菌灵平板上，通过贴接菌丝块法和涂分生孢子法定向筛选获得了球孢白僵菌和金龟子绿僵菌抗多菌灵菌株，并测定了不同抗性菌株对多菌灵的抗性水平。测定结果表明，在球孢白僵菌抗多菌灵菌株中，BC-4菌株的EC_(50)值最大，其EC_(50)值为258.7711，对多菌灵的抗性水平最高，达到242.11，BC-3菌株的EC_(50)值最小，其EC_(50)值为18.6311，抗性水平最低。在金龟子绿僵菌抗多菌灵菌株中，MC-2菌株的EC_(50)值最大，其EC_(50)值为397.0643，对多菌灵的抗性水平达到102.35；MC-4菌株的EC_(50)值最小，其EC_(50)值为149.5440。研究了球孢白僵菌和金龟子绿僵菌抗多菌灵菌株的菌丝生长速率和产孢能力的差异，发现球孢白僵菌和金龟子绿僵菌不同抗性菌株间的菌丝生长速率和产孢能力均存在一定的差异，抗性菌株的生长速率均比对照敏感菌株（亲本菌株）小，产孢能力均比对照敏感菌株要强，但不同菌株间存在一定的差异，在球孢白僵菌抗性菌株中，BC-4菌株的分生孢子产生量最大，在金龟子绿僵菌抗性菌株中，MC-2菌株的分生孢子产生量最大。
5.采用分生孢子悬浮液蘸根法研究了球孢白僵菌抗多菌灵菌株BC-8菌株和金龟子绿僵菌抗多菌灵菌株MC-2菌株在植物根际的定殖能力及对根际微生物的影响。结果显示，BC-8菌株和MC-2菌株均可以在玉米、棉花外根际和根表定殖，但在玉米、棉花根内未分离到供试菌株。BC-8菌株和MC-2菌株对植物根际微生物的数量都有一定程度的影响，尤其以前期影响较为明显，随着时间的推移，影响减弱。
6.在实验室条件下，研究了金龟子绿僵菌和球孢白僵菌对几种土传植物病原真菌的拮抗作用及其机制。对峙培养结果表明，金龟子绿僵菌和球孢白僵菌对供试的植物病原真菌均有抑制作用，其中绿僵菌以Ma55的制效果最好，白僵菌以Bb2092的效果最好。在培养基中加入Ma55和Bb2092不同浓度的分生孢子悬浮液，当浓度为106cfu·mL~(-1)时，对植物病原真菌菌丝生长具有明显的抑制作用。Ma55和Bb2092液体振荡培养获得的无菌发酵液对供试的植物病原真菌菌丝生长都有较好的的抑制作用，对植物病原真菌的分生孢子（菌核）产生及分生孢子（菌核）萌发也都有一定的抑制作用。显微镜观察未发现金龟子绿僵菌和球孢白僵菌与植物病原真菌菌丝间有重寄生现象。上述结果显示，虫生真菌对供试植物病原真菌的拮抗机制主要是营养竞争、空间竞争及抗生作用。
7.研究了不同碳源和氮源对球孢白僵菌和金龟子绿僵菌菌丝生长、分生孢子产生量、菌丝生物量及其次生代谢产物的抑菌活性。结果表明，虫生真菌对单糖、双糖、多糖等碳营养及有机氮和无机氮等氮营养均能够利用，但利用程度存在一定差异。代谢液的抑菌活性实验结果表明，不同处理获得的球孢白僵菌发酵液对供试的5种镰刀菌菌丝生长均有不同程度的抑制作用，在碳源发酵液中，甘油的抑菌效果最好，乳糖的抑菌效果最差。在氮源发酵液中，硫酸铵的抑菌效果最好，脲的抑菌效果最差；不同处理获得的金龟子绿僵菌代谢液对植物病原真菌菌丝生长均有较好的抑制作用，在碳源发酵液中，白砂糖的抑菌效果最好，乳糖的抑菌效果最差。在氮源发酵液中，蛋白胨的抑菌效果最好，脲的抑菌效果最差。
Entomogenous fungi are an important regulator of insect populations and they spreadwidely in agro-ecosystems and play an important role for biological control of crop,orchard, forest and medical insects. Metarhizium anisopliae and Beauveria bassiana aretwo most important entomogenous fungi, which has a wide range of insect hosts and hasbeen widely used for fungal insecticides. In this paper, some isolates from maizerhizosphere soil collected from Guoyang, Xiaoxian and Mengcheng, north Anhui wereidentified as B. bassiana by both morphological method and rDNA ITS sequenceanalysis. They and some M. anisopliae isolates were tested for their sensitivity tocarbendazim, the colonization ability in plant rhizosphere, the inhibition on soil-borneplant pathogenic fungi, and the effects of different carbon and nitrogen sources on theirbiological characteristics and anti-fungal activity. The results were as follows:
1. With selective medium, thirty-nine strains of Beauveria were isolated from maizerhizosphere soil, collected from Counties of Guoyang, Xiaoxian, and Mengcheng in thenorth of Anhui province. The strains were classified and identified as B. bassiana by bothmorphological and molecular (rDNA ITS sequence analysis) means. The colony diameterand conidia number of different strains were tested in vitro and showed significantdifference.
2. The genetic diversity of thirty-seven B. bassiana strains isolated from maizerhizosphere was estimated using inter-simple sequence repeats (ISSR) markers. Elevenamong forty ISSR primers were chosen for their reproducibility and high polymorphism.Each primer resulted in7.5markers and totally83fragments were amplified, in which69(83.13%) were polymorphic. Genetic diversity analysis revealed a relatively high level ofintraspecific genetic diversity of B. bassiana. The percentage of polymorphic loci (PPL)was83.13﹪, Nei’s genetic diversity (H) was0.3169and Shannon’s information index (I)was0.4657. It suggested that the thirty-seven B. bassiana strains had highly geneticdiversity.
3. The sensitivities of B. bassiana and M. anisopliae to carbendazim were studiedby mycelial growth inhibition rate method. The results showed that the sensitivities ofB. bassiana and M. anisopliae to carbendazim had some differences. Among the testedstrains of B. bassiana, the EC_(50)value of GY~(-1)7was the highest, but that of GY-6wasthe lowest. Among the tested strains of M. anisopliae, the EC_(50)value of Ma55was thelowest, followed by Ma27, while the EC_(50)value (4.05) of Ma10was the highest.
4. The resistant level of the carbendazim-resistant strains of B. bassiana and M.anisopliae were studied, by mycelium and conidium oriented screening. The resultsshowed that the resistant level of BC-4was the highest among thecarbendazim-resistant strains of B. bassiana, with EC_(50)and the resistant level at258.77and242.11, respectively. The resistance level of BC-3was the lowest amongthe carbendazim-resistant strains of B. bassiana, with EC_(50)at18.63. The resistantlevel of MC-2was the highest among the carbendazim-resistant strains of M.anisopliae, with EC_(50)and resistant level was397.06and102.35, respectively. TheEC_(50)of MC-4was the smallest (149.54). The mycelia growth rate and sporulationability of the carbendazim-resistant mutants were studied too. It showed that themycelium growth rate and sporulation capacity had some differences among differentcarbendazim-resistant mutants. The growth rate of resistant mutants was smaller thanthat of the control (parent strain), but sporulation ability was stronger than that of thecontrol (susceptible strain), and different strains had some differences. Among thecarbendazim-resistant strains, the sporulation of BC-4mutant and MC-2mutant wasthe highest.
5. The colonization ability and the influence on rhizosphere microorganisms of thecarbendazim-resistant mutants BC-8and MC-2in the plant rhizosphere were studied bymeans of dipping in conidial suspension. BC-8and MC-2were detected from outerrhizosphere and root surface of maize and cotton, but not from inside the roots. Itsuggested that BC-8strain and MC-2strain had a certain influence on the number of plantrhizosphere microorganisms, especially at the beginning, but the effects decreased withtime.
6. Under laboratory conditions, the inhibition of M. anisopliae and B. bassianaagainst Fusarium oxysporium f. sp. vasinfectum and other soil-borne plant pathogenicfungi, and its mechanism were studied in vitro by dual culture, cup-plate test andmicroscopic examination. The results of dual-culture test showed that among three M.anisopliae isolates and four B. bassiana isolates which all displayed obvious inhibition onthe tested soil-borne plant pathogenic fungi, Ma55and Bb2092resulted in the highestinhibition. On the PDA plates mixed with different concentrations of conidial suspensionof Ma55and Bb2092, the inhibition rate by the suspension of106conidia per milliliterswas the highest to all tested fungi. The inhibition on mycelia growth of the tested fungi bysterile fermented broth of M. anisopliae and B. bassiana shake culture was obvious, andthose to production and germination of their conidia (sclerotia) were also significant. No hyperparasitism of M. anisolpiae and B. bassiana on the hyphae of the tested fungi wasobserved microscopically. All these evidences suggested that the inhibitory mechanisms ofM. anisopliae and B. bassiana against the pathogen of soil-borne plant diseases weremainly competition to nutrition, space and antibiosis.
7. The biological characteristics of B. bassiana and M. anisopliae were compared indifferent carbon sources and nitrogen sources by measuring the mycelium growth, drymycelium biomass and conidia yield. The results showed that B. bassiana and M.anisopliae could use many carbohydrate and nitrogen sources for the mycelia growth. Bymeans of mycelium growth rate, the inhibitory rates of metabolic liquid cultured withdifferent carbon sources and nitrogen sources were tested. The anti-fungal assay of thesecondary metabolites of B. bassiana showed that the metabolic liquid cultured withdifferent carbon sources and nitrogen sources had significant difference on the5testedstrains of Fusarium. Among the metabolic liquid, the inhibitory rates of those withglycerol and ammonium sulfate as carbon and nitrogen source were the highest and thosewith lactose and urea as carbon and nitrogen source were the lowest. The anti-fungal assayof the secondary metabolites of M. anisopliae revealed that secondary metabolitesproduced in the culture with sucrose as the carbon source and/or the peptone as thenitrogen sources was the highest.
引文
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