Abstract Some entomopathogenic fungi, such as Metarhizium spp. and Beauveria spp., closely interact with plants by colonizing the rhizosphere or growing endophytically inside root tissues. These characteristics increase the potential for endophytic entomopathogenic fungi to persist in the root system when used as biological control agents. The mechanism by which endophytic entomopathogenic fungi are capable to colonize the internal plant tissues is also influenced by plants and can be regarded as an adaptive protection acquired by plants against herbivorous insects. The mutual benefits obtained by plants and fungi through this peculiar endophytic association supports the bodyguard hypothesis. The objectives of this study were to evaluate the ability of different isolates of Metarhizium spp. and a single isolate of Beauveria bassiana, coated onto seeds, to colonize the rhizosphere and root tissues of maize (Zea mays) and to assess whether the presence of an insect pest and fungal root pathogen influenced this interaction. All the entomopathogenic fungal isolates tested were able to colonize the rhizosphere to some extent, but one isolate of M. anisopliae and the one of M. robertsii performed best. Overall, the presence of Costelytra giveni (Scarabaeidae) larvae significantly decreased rhizosphere colonization by the entomopathogens, while the phytopathogenic fungus Fusarium graminearum (Nectriaceae: Hypocreales) did not. Similarly, the presence of C. giveni decreased endophytic growth in root tissues by around 75% when considering all entomopathogens together. In contrast, a 112% increase in overall root endophytic colonization occurred in the presence of F. graminearum. Salicylic acid (SA) and jasmonic acid (JA) content in maize plants changed depending on the isolate of M. anisopliae incorporated through seed coating and root herbivory by larval presence. In the absence of C. giveni, plants treated with M. anisopliae A1080 had higher SA and JA root content than control plants. Conversely, when larvae were present, maize plants treated with M. anisopliae F672 had increased levels of both phytohormones, indicating a potentially primed state. The observed decrease in root colonization by some entomopathogenic fungal isolates in the presence of larvae of C. giveni and the increase in endophytic colonization in the presence of F. graminearum are in accordance with the bodyguard hypothesis. Additionally, the changes observed in the SA and JA content in Metarhizium treated plants corresponded to plant responses related to systemic acquired resistance and to induced systemic resistance. Our results demonstrate that biotic soil factors can shape the outcome of endophytic entomopathogenic fungi-plant interaction, as well as affecting the plant physiology.

中文翻译：

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玉米根系害虫和真菌病原体对昆虫病原真菌根际定植、内生菌和植物激素诱导的影响

摘要 一些昆虫病原真菌，如绿僵菌属。和 Beauveria spp.，通过在根际定植或在根组织内内生生长而与植物密切相互作用。当用作生物防治剂时，这些特征增加了内生昆虫病原真菌在根系中持续存在的可能性。内生昆虫病原真菌能够在植物内部组织定殖的机制也受植物的影响，可以看作是植物对食草昆虫的适应性保护。植物和真菌通过这种特殊的内生关联获得的互利支持了保镖假说。本研究的目的是评估绿僵菌不同分离株的能力。和一个白僵菌分离株，涂在种子上，在玉米 (Zea mays) 的根际和根组织定植，并评估害虫和真菌根病原体的存在是否影响了这种相互作用。测试的所有昆虫病原真菌分离物都能够在一定程度上定植于根际，但 M. anisopliae 的一种分离物和 M. robertsii 的一种表现最好。总体而言，Costelytra giveni（金龟子科）幼虫的存在显着减少了昆虫病原体在根际的定植，而植物病原真菌禾谷镰刀菌（Nectriaceae：Hypocreales）则没有。类似地，当将所有昆虫病原体一起考虑时，给定念珠菌的存在使根组织中的内生生长减少了约 75%。相比之下，在禾谷镰刀菌存在的情况下，整体根内生定植增加了 112%。玉米植株中的水杨酸 (SA) 和茉莉酸 (JA) 含量根据幼虫存在而通过种子包衣和根食草吸收的 M. anisopliae 的分离物而变化。在不存在给定念珠菌的情况下，用绿僵菌 A1080 处理的植物比对照植物具有更高的 SA 和 JA 根含量。相反，当幼虫存在时，用 M. anisopliae F672 处理的玉米植物的两种植物激素水平都增加，表明可能处于致敏状态。观察到一些昆虫病原真菌分离株在给定念珠菌幼虫存在时根部定植减少，而在禾谷镰刀菌存在下内生定植增加，这与保镖假说一致。此外，在绿僵菌处理的植物中观察到的 SA 和 JA 含量变化对应于与系统获得性抗性和诱导系统抗性相关的植物反应。我们的研究结果表明，生物土壤因素可以影响内生昆虫病原真菌-植物相互作用的结果，并影响植物生理学。