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Delving into the Causes and Effects of Entomopathogenic Endophytic Metarhizium brunneum Foliar Application-Related Mortality in Spodoptera littoralis Larvae.

ABSTRACT: The aim of the current study was to delve into the causes of mortality of Spodoptera littoralis larvae feeding on Metarhizium-colonized plants in the absence of fungal outgrowth on the cadavers as previous studies reported and to elucidate the possible indirect effects of this fungus-colonized diet. The effect was evaluated in experiments conducted using leaf discs of colonized plants and in planta using fungus-colonized whole plants. The mortality rates of larvae fed on Metarhizium-colonized melon leaves were 45.0% and 87.5%, and the average survival times were 6.6 and 3.1 days in experiments performed with discs and in planta, respectively. Notably, these mortality levels were not associated with observed apoptosis mediated by caspases 1, 3-7 and 8; thus, further investigation into the possible immune system reaction of the insect after the ingestion of colonized plants is required. The leaf consumption of S. littoralis larvae fed on melon-colonized leaves was lower than that on control plants in the disc experiments but not in experiments conducted in planta. In this regard, in experiments performed in planta, plant damage increased larval mortality in both fungally challenged and control larvae. There was also a meaningful effect of exposure to Metarhizium-colonized melon leaf discs on S. littoralis fitness, with significant reductions in 39.0% and 22.0% in female fecundity and egg fertility, respectively, detected in females emerging from pupae developing from larvae surviving exposure to colonized plant discs; all larvae died in the in planta experiments. Hence, the present work presents new findings revealing the high potential of endophytic entomopathogenic fungi to improve the outcome of foliar applications against chewing insects in the short, mid- and long term, by the reduction of the reproductive potential of surviving adults and reveals new insights into the development of bioassays with whole plants for more detailed evaluation of the impact of these fungi as endophytes used for plant protection.

SUBMITTER: Garrido-Jurado I

PROVIDER: S-EPMC7412302 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Delving into the Causes and Effects of Entomopathogenic Endophytic Metarhizium brunneum Foliar Application-Related Mortality in Spodoptera littoralis Larvae.

Garrido-Jurado Inmaculada I Montes-Moreno David D Sanz-Barrionuevo Pilar P Quesada-Moraga Enrique E

Insects 20200709 7

The aim of the current study was to delve into the causes of mortality of Spodoptera littoralis larvae feeding on Metarhizium-colonized plants in the absence of fungal outgrowth on the cadavers as previous studies reported and to elucidate the possible indirect effects of this fungus-colonized diet. The effect was evaluated in experiments conducted using leaf discs of colonized plants and in planta using fungus-colonized whole plants. The mortality rates of larvae fed on Metarhi ...[more]

PMID: 32660021

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Project description:Entomopathogenic fungi (EPF) exhibit direct and indirect mechanisms to increase plant resistance against biotic and abiotic stresses. Plant responses to these stresses are interconnected by common regulators such as ethylene (ET), which is involved in both iron (Fe) deficiency and induced systemic resistance responses. In this work, the roots of cucurbit seedlings were primed with Metarhizium brunneum (EAMa 01/58-Su strain), and relative expression levels of 18 genes related to ethylene (ET), jasmonic acid (JA), and salicylic acid (SA) synthesis, as well as pathogen-related (PR) protein genes, were studied by reverse transcription-quantitative PCR (qRT-PCR). Effects of priming on Spodoptera littoralis were studied by feeding larvae for 15 days with primed and control plants. Genes showed upregulation in studied species; however, the highest relative expression was observed in roots and shoots of plants with Fe deficiency, demonstrating the complexity and the overlapping degree of the regulatory network. EIN2 and EIN3 should be highlighted; both are key genes of the ET transduction pathway that enhanced their expression levels up to eight and four times, respectively, in shoots of primed cucumber. Also, JA and SA synthesis and PR genes showed significant upregulation during the observation period (e.g., the JA gene LOX1 increased 506 times). Survival and fitness of S. littoralis were affected with significant effects on mortality of larvae fed on primed plants versus controls, length of the larval stage, pupal weight, and the percentage of abnormal pupae. These results highlight the role of the EAMa 01/58-Su strain in the induction of resistance, which could be translated into direct benefits for plant development. IMPORTANCE Entomopathogenic fungi are multipurpose microorganisms with direct and indirect effects on insect pests. Also, EPF provide multiple benefits to plants by solubilizing minerals and facilitating nutrient acquisition. A very interesting and novel effect of these fungi is the enhancement of plant defense systems by inducing systematic and acquired resistance. However, little is known about this function. This study sheds light on the molecular mechanisms involved in cucurbits plants' defense activation after being primed by the EPF M. brunneum. Furthermore, the subsequent effects on the fitness of the lepidopteran pest S. littoralis are shown. In this regard, a significant upregulation was recorded for the genes that regulate JA, SA, and ET pathways. This increased expression of defense genes caused lethal and sublethal effects on S. littoralis. This could be considered an added value for the implementation of EPF in integrated pest management programs.

Project description:Aedes aegypti is the vector of a wide range of diseases (e.g. yellow fever, dengue, Chikungunya and Zika) which impact on over half the world's population. Entomopathogenic fungi such as Metarhizium anisopliae and Beauveria bassiana have been found to be highly efficacious in killing mosquito larvae but only now are the underlying mechanisms for pathogenesis being elucidated. Recently it was shown that conidia of M. anisopliae caused stress induced mortality in Ae. aegypti larvae, a different mode of pathogenicity to that normally seen in terrestrial hosts. Blastospores constitute a different form of inoculum produced by this fungus when cultured in liquid media and although blastospores are generally considered to be more virulent than conidia no evidence has been presented to explain why. In our study, using a range of biochemical, molecular and microscopy methods, the infection process of Metarhizium brunneum (formerly M. anisopliae) ARSEF 4556 blastospores was investigated. It appears that the blastospores, unlike conidia, readily adhere to and penetrate mosquito larval cuticle. The blastospores are readily ingested by the larvae but unlike the conidia are able infect the insect through the gut and rapidly invade the haemocoel. The fact that pathogenicity related genes were upregulated in blastospores exposed to larvae prior to invasion, suggests the fungus was detecting host derived cues. Similarly, immune and defence genes were upregulated in the host prior to infection suggesting mosquitoes were also able to detect pathogen-derived cues. The hydrophilic blastospores produce copious mucilage, which probably facilitates adhesion to the host but do not appear to depend on production of Pr1, a cuticle degrading subtilisin protease, for penetration since protease inhibitors did not significantly alter blastospore virulence. The fact the blastospores have multiple routes of entry (cuticle and gut) may explain why this form of the inoculum killed Ae. aegypti larvae in a relatively short time (12-24hrs), significantly quicker than when larvae were exposed to conidia. This study shows that selecting the appropriate form of inoculum is important for efficacious control of disease vectors such as Ae. aegypti.

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Dataset Information

Delving into the Causes and Effects of Entomopathogenic Endophytic Metarhizium brunneum Foliar Application-Related Mortality in Spodoptera littoralis Larvae.

Publications

Delving into the Causes and Effects of Entomopathogenic Endophytic <i>Metarhizium brunneum</i> Foliar Application-Related Mortality in <i>Spodoptera littoralis</i> Larvae.

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