Microbiological Research, volume 286, pages 127819

Field isolates of Beauveria bassiana exhibit biological heterogeneity in multitrophic interactions of agricultural importance.

M. Ranesi 1
Stefania Vitale 1, 2
A. Staropoli 1, 2
Ilaria Di Lelio 1, 3
L. Izzo 1
Maria G. De Luca 1
Andrea Becchimanzi 1, 3
Francesco Pennacchio 1, 3
M. Lorito 1, 3
Sheridan L. Woo 3, 4
F. Vinale 2, 3, 5
David Turra 1, 3, 6, 7
Show full list: 12 authors
Publication typeJournal Article
Publication date2024-09-01
scimago Q1
wos Q1
SJR1.175
CiteScore10.9
Impact factor6.1
ISSN09445013, 16180623
Abstract
Beauveria bassiana (Bb) is a widespread entomopathogenic fungus widely used in agriculture for crop protection. Other than pest control, fungi belonging to the B. bassiana complex represent an important microbial resource in agroecosystems, considering their multiple interactions with other microorganisms as antagonists of phytopathogens, or with plants as endophytic colonizers and growth promoters. Here, we characterised field collected or commercial isolates of B. bassiana relative to the environmental factors that affect their growth. We further compared the metabolome, the entomopathogenic potential and biocontrol activity of the tested isolates respectively on the insect pest Spodoptera littoralis or against the fungal plant pathogen Fusarium oxysporum. Our analysis revealed that the B. bassiana complex is characterised by a high level of inter-isolate heterogeneity in terms of nutritional requirements, establishment of intra- or inter-kingdom interactions, and the nature of metabolites produced. Interestingly, certain B. bassiana isolates demonstrated a preference for low nutrient plant-derived media, which hints at their adaptation towards an endophytic lifestyle over a saprophytic one. In addition, there was a noticeable variation among different B. bassiana isolates in their capacity to kill S. littoralis larvae in a contact infection test, but not in an intrahaemocoelic injection experiment, suggesting a unique level of adaptability specific to the host. On the other hand, most B. bassiana isolates exhibited similar biocontrol efficacy against the soil-dwelling ascomycete F. oxysporum f. sp. lycopersici, a pathogen responsible for vascular wilt disease in tomato plants, effectively averting wilting. Overall, we show that the effectiveness of B. bassiana isolates can greatly vary, emphasising the importance of isolate selection and nutritional adaptability consideration for their use in sustainable agriculture.
Sui L., Lu Y., Zhou L., Li N., Li Q., Zhang Z.
Frontiers in Microbiology scimago Q1 wos Q2 Open Access
2023-08-16 citations by CoLab: 22 PDF Abstract  
IntroductionEntomopathogenic fungi (EPF) can colonize and establish symbiotic relationships with plants as endophytes. Recently, EPF have been reported to suppress plant pathogens and induce plant resistance to diseases. However, the potential mechanisms via which EPF as endophytes control major plant diseases in situ remain largely unknown.MethodsPot and field experiments were conducted to investigate the mechanisms via which an EPF, Beauveria bassiana, colonizes tomato, under Botrytis cinerea infection stress. B. bassiana blastospores were inoculated into tomato plants by root irrigation. Tomato resistance to tomato gray mold caused by B. cinerea was evaluated by artificial inoculation, and B. bassiana colonization in plants and rhizosphere soil under B. cinerea infection stress was evaluated by colony counting and quantitative PCR. Furthermore, the expression levels of three disease resistance-related genes (OXO, CHI, and atpA) in tomato leaves were determined to explore the effect of B. bassiana colonization on plant disease resistance performance in pot experiments.ResultsB. bassiana colonization could improve resistance of tomato plants to gray mold caused by B. cinerea. The incidence rate, lesion diameter, and disease index of gray mold decreased in both the pot and field experiments following B. bassiana colonization. B. bassiana was more likely to accumulate in the pathogen infected leaves, while decreasing in the rhizosphere soil, and induced the expression of plant resistance genes, which were up-regulated in leaves.DiscussionThe results indicated that plants could “recruit” B. bassiana from rhizosphere soil to diseased plants as directional effects, which then enhanced plant growth and resistance against pathogens, consequently inhibiting pathogen infection and multiplication in plants. Our findings provide novel insights that enhance our understanding of the roles of EPF during pathogen challenge.
Proietti S., Falconieri G.S., Bertini L., Pascale A., Bizzarri E., Morales-Sanfrutos J., Sabido E., Ruocco M., Monti M.M., Russo A., Dziurka K., Ceci M., Loreto F., Caruso C.
Journal of Experimental Botany scimago Q1 wos Q1
2023-04-24 citations by CoLab: 14 Abstract  
Abstract Plant roots can exploit beneficial associations with soil inhabiting microbes, promoting growth and expanding the immune capacity of the host plant. In this work, we aimed to increase information on changes occurring in tomato interacting with the beneficial fungus Beauveria bassiana. Tomato leaf proteome revealed perturbed molecular pathways during the establishment of the plant-fungus relationship. In the early stages of colonization (5-7 days), proteins related to defense responses to fungus were down-regulated and proteins related to calcium transport were up-regulated. At later time points (12-19 days after colonization), up-regulation of molecular pathways linked to protein/amino acids turn-over and to biosynthesis of energy compounds suggests beneficial interaction enhancing plant growth and development. At the later stage, the profile of leaf hormones and related compounds was also investigated highlighting up-regulation of those related to plant growth and defense. Finally, B. bassiana colonization was found to improve plant resistance against Botrytis cinerea, impacting plant oxidative damage. Overall, our findings further expand current knowledge on the possible mechanisms underlying the beneficial role of B. bassiana on tomato plants.
Rehman A., Farooq M., Lee D., Siddique K.H.
2022-10-18 citations by CoLab: 63 Abstract  
The notion of food security is a global phenomenon that impinges on every human. Efforts to increase productivity and yields have historically degraded the environment and reduced biodiversity and ecosystem services, with the significant impact on the poor. Sustainable agriculture—farming in sustainable ways based on an understanding of ecosystem services—is a practical option for achieving global food security while minimizing further environmental degradation. Sustainable agricultural systems offer ecosystem services, such as pollination, biological pest control, regulation of soil and water quality, maintenance of soil structure and fertility, carbon sequestration and mitigation of greenhouse gas emissions, nutrient cycling, hydrological services, and biodiversity conservation. In this review, we discuss the potential of sustainable agriculture for achieving global food security alongside healthy ecosystems that provide other valuable services to humankind. Too often, agricultural production systems are considered separate from other natural ecosystems, and insufficient attention has been paid to how services can flow to and from agricultural production systems to surrounding ecosystems. This review also details the trade-offs and synergies between ecosystem services, highlights current knowledge gaps, and proposes areas for future research.
Wang Y., Fan Q., Wang D., Zou W., Tang D., Hongthong P., Yu H.
Frontiers in Microbiology scimago Q1 wos Q2 Open Access
2022-03-04 citations by CoLab: 20 PDF Abstract  
Beauveria is a very important fungal resource. Some Beauveria species have great economic and ecological value. Through surveying Beauveria in China and Thailand over the past 4 years, 15 Beauveria spp. were collected and identified. Three new species—namely, B. polyrhachicola, B. songmingensis, and B. subscarabaeidicola—were described and illustrated based on morphological characteristics and molecular data. The phylogenetic positions of the 15 species were evaluated according to phylogenetic inferences based on six loci (nrSSU, nrLSU, TEF, RPB1, RPB2, and Bloc). Nine species of Beauveria in our study were isolated from adult scarab beetles (Coleoptera: Scarabaeidae). The pathogenicity of the isolates from the B. bassiana complex and B. scarabaeidicola complex was determined with three bioassays using B. mori and T. molitor larvae, in addition to Protaetia brevitarsis adults. The results indicated that the B. bassiana complex isolates had great potential in the biocontrol of the three insects; by contrast, the B. scarabaeidicola complex isolates showed obvious host specificity and low virulence.
Ávila-Hernández J.G., Aguilar-Zárate P., Carrillo-Inungaray M.L., Michel M.R., Wong-Paz J.E., Muñiz-Márquez D.B., Rojas-Molina R., Ascacio-Valdés J.A., Martínez-Ávila G.C.
2022-01-21 citations by CoLab: 6 Abstract  
Fungal secondary metabolites with antimicrobial properties are used for biological pest control. Their production is influenced by several factors as environment, host, and culture conditions. In the present work, the secondary metabolites from fermented extracts of Beauveria bassiana PQ2 were tested as antifungal agents against Gibberella moniliformis LIA. The L18 (21 × 37) orthogonal array from Taguchi methodology was used to assess 8 parameters (pH, agitation, sucrose, yeast extract, KH2PO4, MgSO4, NH4NO3, and CaCl2) in B. bassiana PQ2 submerged fermentation. The ability of the fermented extracts to slow down the growth rate of G. moniliformis LIA was evaluated. The results from 18 trials were analyzed by Statistica 7 software by evaluating the signal-to-noise ratio (S/N) to find the lower-the-better condition. Optimal culture conditions were pH, 5; agitation, 250 rpm; sucrose, 37.5 g/L−1; yeast extract, 10 g/L−1; KH2PO4, 0.8 g/L−1; MgSO4, 1.2 g/L−1; NH4NO3, 0.1 g/L−1; and CaCl2, 0.4 g/L−1, being the agitation at the highest level the most significant factor. The optimal conditions were validated in a sparged bottle bioreactor resulting in a higher S/N value (12.48) compared to the estimate. The extract obtained has the capacity to inhibit the germination of G. moniliformis spores at 24 h. HPLC-ESI-MS2 allowed to identify the water-soluble red pigment as oosporein (m/z 304.9). The secondary metabolites from B. bassiana PQ2 are a suitable alternative to control the growth and sporulation of G. moniliformis.
Barrow N.J., Lambers H.
Plant and Soil scimago Q1 wos Q2
2022-01-11 citations by CoLab: 20 Abstract  
Organisms intended to solubilise soil phosphate are chosen on their ability to produce a clear halo on a plate containing a sparingly soluble phosphate. This involves production of acidity. However, if these organisms establish on plant roots any benefit from increased acidity is likely to be as a result of increased rate of uptake of phosphate by plant roots rather than from increased desorption of phosphate from soil.
Sinno M., Ranesi M., Di Lelio I., Iacomino G., Becchimanzi A., Barra E., Molisso D., Pennacchio F., Digilio M.C., Vitale S., Turrà D., Harizanova V., Lorito M., Woo S.L.
Pathogens scimago Q2 wos Q2 Open Access
2021-09-26 citations by CoLab: 44 PDF Abstract  
Endophytic fungi (EF) can enhance both plant growth and defense barriers against pests and pathogens, contributing to the reduction of chemical pesticides and fertilizers use in agriculture. Beauveria bassiana is an entomopathogenic fungus showing endophytism in several crops, often associated with a good capacity to limit the development of pests and disease agents. However, the diversity of the protective efficacy and plant response to different strains can be remarkable and needs to be carefully assessed for the successful and predictable use of these beneficial microorganisms. This study aims to select B. bassiana strains able to colonize tomato plants as endophytes as well as to control two important disease agents, Botrytis cinerea and Alternaria alternata, and the pest aphid, Macrosiphum euphorbiae. Nine wild-type isolates and one commercial strain were screened for endophytism, then further characterized for plant-growth promotion plus inhibition of disease development and pest infestation. Four isolates proved to have a good control activity against the biotic stressors tested, but only Bb716 was also able to promote plant growth. This work provides a simple workflow for the selection of beneficial EF, paving the way towards more effective use of B. bassiana in Integrate Pest Management (IPM) of tomato.
Wang H., Peng H., Li W., Cheng P., Gong M.
Frontiers in Microbiology scimago Q1 wos Q2 Open Access
2021-08-26 citations by CoLab: 87 PDF Abstract  
The long-term and excessive usage of pesticides is an enormous burden on the environment, which also increases pest resistance. To overcome this problem, research and application of entomopathogenic fungi, which are both environmentally friendly and cause lower resistance, have gained great momentum. Entomopathogenic fungi have a wide range of prospects. Apart from Bacillus thuringiensis, Beauveria bassiana is the most studied biopesticide. After invading insect hosts, B. bassiana produces a variety of toxins, which are secondary metabolites such as beauvericin, bassianin, bassianolide, beauverolides, tenellin, oosporein, and oxalic acid. These toxins help B. bassiana to parasitize and kill the hosts. This review unequivocally considers beauveria toxins highly promising and summarizes their attack mechanism(s) on the host insect immune system. Genetic engineering strategies to improve toxin principles, genes, or virulent molecules of B. bassiana have also been discussed. Lastly, we discuss the future perspective of Beauveria toxin research, including newly discovered toxins.
Mantzoukas S., Lagogiannis I., Mpousia D., Ntoukas A., Karmakolia K., Eliopoulos P.A., Poulas K.
Journal of Fungi scimago Q1 wos Q1 Open Access
2021-02-16 citations by CoLab: 30 PDF Abstract  
The common grape vine, Vitis vinifera, is a widely known plant with commercial and pharmacological value. The plant hosts a variety of microorganisms known as endophytes that can live within the tissues of the plant for a considerable time period, or even their whole life cycle. The fungus Beauveria bassiana is a well-studied endophyte which can colonize a variety of plants in many ways and in different parts of the plant. In this study, we examined the effect of the endophytic fungus B. bassiana on the growth of V. vinifera. The results demonstrated not only a successful colonization of the endophyte, but also a noteworthy impact on the growth of the V. vinifera root without harming the plant in any way. The fungus was also re-isolated from the parts of the plant using inst bait method. Overall, the study demonstrates the capability of B. bassiana to colonize V. vinifera plants, adding to the already existing knowledge of its endophytic activity, and highlighting its beneficial impact on the root growth.
Palmieri D., Vitale S., Lima G., Di Pietro A., Turrà D.
Nature Communications scimago Q1 wos Q1 Open Access
2020-10-16 citations by CoLab: 55 PDF Abstract  
Soil-inhabiting fungal pathogens use chemical signals released by roots to direct hyphal growth towards the host plant. Whether other soil microorganisms exploit this capacity for their own benefit is currently unknown. Here we show that the endophytic rhizobacterium Rahnella aquatilis locates hyphae of the root-infecting fungal pathogen Fusarium oxysporum through pH-mediated chemotaxis and uses them as highways to efficiently access and colonize plant roots. Secretion of gluconic acid (GlcA) by R. aquatilis in the rhizosphere leads to acidification and counteracts F. oxysporum-induced alkalinisation, a known virulence mechanism, thereby preventing fungal infection. Genetic abrogation or biochemical inhibition of GlcA-mediated acidification abolished biocontrol activity of R. aquatilis and restored fungal infection. These findings reveal a new way by which bacterial endophytes hijack hyphae of a fungal pathogen in the soil to gain preferential access to plant roots, thereby protecting the host from infection. Soil-borne fungal pathogens use chemotropism and extracellular pH alkalinisation to reach and penetrate plant roots. Here, Palmieri et al. show that soil endophytic bacteria swim along fungal hyphae to colonize plant roots and protect host plants by modulating the pH of the rhizosphere.
Rawat P., Das S., Shankhdhar D., Shankhdhar S.C.
2020-09-30 citations by CoLab: 330 Abstract  
Phosphorus is the second most critical macronutrient after nitrogen required for metabolism, growth, and development of plants. Despite the abundance of phosphorus in both organic and inorganic forms in the soil, it is mostly unavailable for plant uptake due to its complexation with metal ions in the soil. The use of agrochemicals to satisfy the demand for phosphorus to improve crop yield has led to the deterioration of the ecosystem and soil health, as well as an imbalance in the soil microbiota. Consequently, there is a demand for an alternate cost-effective and eco-friendly strategy for the biofortification of phosphorus. One such strategy is the application of phosphate-solubilizing microorganisms which can solubilize insoluble phosphates in soil by different mechanisms like secretion of organic acids, enzyme production, and excretion of siderophores that can chelate the metal ions and form complexes, making phosphates available for plant uptake. These microbes not only solubilize phosphates but also promote plant growth and crop yield by producing plant-growth-promoting hormones like auxins, gibberellins, and cytokinins, antibiosis against pathogens, 1-aminocyclopropane-1-carboxylic acid deaminase which enhances plant growth under stress conditions, improving plant resistance to heavy metal toxicity, and so on. Pyrroloquinoline quinine (pqq) and glucose dehydrogenase (gcd) are the representative genes for phosphorus solubilization in microorganisms. The content presented in this review paper focuses on different mechanisms and modes of action of phosphate-solubilizing microorganisms, their contribution to phosphorus solubilization, growth-promoting attributes in plants, and the molecular aspects of phosphorus solubilization.
Barra-Bucarei L., González M.G., Iglesias A.F., Aguayo G.S., Peñalosa M.G., Vera P.V.
Insects scimago Q1 wos Q1 Open Access
2020-09-02 citations by CoLab: 38 PDF Abstract  
The tomato, Solanum lycopersicum L. is one of the most consumed vegetables in the world; nevertheless, it is affected by biotic and abiotic factors that reduce its productivity. The whitefly is globally considered as the main pest under protected crop conditions, where biologic control using endophytic fungi emerges as a sustainable alternative. We evaluated the indirect effects of five native endophytic strains of Beauveria bassiana on the reproduction of greenhouse whiteflies and the growth of tomatoes. The plant growth substrate was inoculated with five strains of this endophyte and the resulting plants were then exposed to whiteflies afterwards. The effect that endophytic strains had on phosphate solubilization, iron siderophore production, plant height, and plant biomass were evaluated. The evaluated endophytes reduced the number of eggs per cm2 on leaflets compared to the control and behaved similarly to the commercial synthetic insecticide. Leaflets inoculated with strains RGM-557, RGM-644 and RGM-731 showed fewer nymphs than the control and those treated with insecticide. RGM-557 and RGM-731 produced the greatest plant heights; RGM-731 obtained the greatest plant biomass. Our study provides evidence that native endophytic strains of B. bassiana have a biocontrol effect on whiteflies and could be used to promote tomato growth.
Amobonye A., Bhagwat P., Pandey A., Singh S., Pillai S.
2020-08-10 citations by CoLab: 50 Abstract  
Beauveria bassiana though widely perceived as an entomopathogenic fungus has also been found in nature to be endophytic. As entomopathogens, the life cycle of different B. bassiana strains are organized and adapted as pathogens to their invertebrate hosts while as endophytes they maintain a symbiotic relationship with their plant hosts. To fulfill these aforementioned ecological roles, this fungus secretes an array of enzymes as well as secondary metabolites, which all have significant biological roles. Basically, chitinases, lipases and proteases are considered to be the most important of all the enzymes produced by B. bassiana. However, studies have also shown their ability to produce other vital enzymes which include amylase, asparaginase, cellulase, galactosidase etc. Previous reports on this filamentous fungus have laid more emphasis on its entomopathogenicity, its endophytism and its highly acclaimed application in the biological control of pests. This review, however, is the first to fully assess the enzyme-secreting potential of this entomopathogenic fungus and its use as a novel source of several industrial biocatalysts and other important biochemicals. This article highlights the inherent properties of the fungus to degrade various biopolymers as well as its relative safety for human use. Some of the important factors have raised the possibilities of exploitation for industrial production and as safe hosts for gene expression.
Zhang Z., Lu Y., Xu W., Sui L., Du Q., Wang Y., Zhao Y., Li Q.
BMC Genomics scimago Q1 wos Q2 Open Access
2020-06-30 citations by CoLab: 21 PDF Abstract  
Beauveria bassiana (B. bassiana) is a famous entomopathogenic fungus that could parasitize on hundreds of insect species, which are being used as an environmentally friendly mycoinsecticide. Nevertheless, the possible effect of genetic diversity of these B. bassiana isolates from different hosts on virulence has not been explored before. In order to explore that issue, we compared the genome sequences among seventeen B. bassiana isolates from 17 different insects using whole genome re-sequencing, with B. bassiana strain ARSEF 2860 as the reference genome. There were a total of 10,098 missense mutated genes, 720 positively selected genes were identified in 17 strains of B. bassiana. Among these, two genes with high frequency mutations encode the toxin-producing non-ribosomal peptide synthase (NRPS) protein. Seven genes undergoing positive selection were enriched in the two-component signaling pathway that is known to regulate the fungal toxicity. In addition, the domain changes of three positively selected genes are also directly related to the virulence plasticity. Besides, the functional categorization of mutated genes showed that most of them involved in the biological functions of toxic proteins involved in. Based on our data, our results indicate that several mutated genes and positively selected genes may underpin virulence of B. bassiana towards hosts during infection process, which provide an insight into the potential effects of natural variation on the virulence of B. bassiana, which will be useful in screening out potential virulence factors in B. bassiana.
Barra-Bucarei L., France Iglesias A., Gerding González M., Silva Aguayo G., Carrasco-Fernández J., Castro J.F., Ortiz Campos J.
Microorganisms scimago Q2 wos Q2 Open Access
2019-12-31 citations by CoLab: 70 PDF Abstract  
Botrytis cinerea causes substantial losses in tomato and chili pepper crops worldwide. Endophytes have shown the potential for the biological control of diseases. The colonization ability of native endophyte strains of Beauveria bassiana and their antifungal effect against B. cinerea were evaluated in Solanaceae crops. Root drenching with B. bassiana was applied, and endophytic colonization capacity in roots, stems, and leaves was determined. The antagonistic activity was evaluated using in vitro dual culture and also plants by drenching the endophyte on the root and by pathogen inoculation in the leaves. Ten native strains were endophytes of tomato, and eight were endophytes of chili pepper. All strains showed significant in vitro antagonism against B. cinerea (30–36%). A high antifungal effect was observed, and strains RGM547 and RGM644 showed the lowest percentage of the surface affected by the pathogen. Native strains of B. bassiana colonized tomato and chili pepper tissues and provided important levels of antagonism against B. cinerea.
Vitale S., Salzano F., Staropoli A., Marra R., Turrà D., Lorito M., Vinale F.
2025-02-04 citations by CoLab: 0 PDF Abstract  
The efficacy of biocontrol agents depends critically on their environmental adaptability, with nutrient availability being a key determinant of their success. In Trichoderma species, the mechanisms linking nutrient sensing to physiological responses remain poorly understood, despite their importance for biocontrol applications. This study reveals how different nitrogen sources fundamentally regulate the physiology and metabolism of Trichoderma harzianum through pH modulation. Under nutrient-rich conditions, T. harzianum exhibited a biphasic pH response characterized by initial acidification followed by alkalinization, which correlated with enhanced sporulation. Examining specific nitrogen sources, we found that sodium nitrate induced environmental alkalinization, while ammonium nitrate caused sustained acidification. These pH changes were linked to distinct physiological responses: alkaline conditions promoted sporulation, while acidic conditions enhanced mycelial growth and triggered specific metabolic responses. Notably, acidic conditions specifically induced the production of harzianic acid and related bioactive compounds, suggesting pH-dependent regulation of secondary metabolism. This nitrogen-dependent pH modulation pattern was conserved across Trichoderma species, as demonstrated by parallel responses in T. asperellum. Our findings establish nitrogen source availability as a master regulator of Trichoderma physiology through pH-dependent mechanisms, controlling both development and secondary metabolism. This understanding provides new strategies for optimizing biocontrol formulations by manipulating nitrogen sources and pH conditions to enhance both fungal fitness and beneficial metabolite production.
Schiesaro G., Undabarrena A., Sørensen M.B., Wäneskog M., Jönsson M., Tenente R., Rago D., Deichmann M., Hoch-Schneider E., Kandasamy V., Özdemir E., Cruz-Morales P., Frimurer T.M., Clemmensen L.K., Jensen M.K., et. al.
2024-10-30 citations by CoLab: 0 Abstract  
AbstractFungi are essential members of natural ecosystems and industrial biotechnology, yet they also pose significant risks to crops and human health. To thrive in microbial consortia a fungal organism must integrate the perception of both inter- and intra-species signals from the environment. Here we present a Yeast Mating Platform (YeMaP) to decipher cell-cell communication between fungal G protein-coupled receptors and short pheromone peptides. We use YeMaP to investigate the influence of abiotic factors on cell-cell communication in multiplex and for high-throughput screening of natural and synthetic pheromones to identify peptides with either improved potency or antagonism action. Additionally, we demonstrate that the plant pathogenFusarium oxysporumpossesses a robust cell-cell communication mechanism, which can, however, be disrupted by supplementing pheromones to promote the communication of non-pathogenic organisms. Taken together, we envision that YeMaP could be applied to uncover the complexity of fungal communication and lead the application of future crop pest- and disease-management programs.

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