Evaluation of Various Inoculation Methods on the Effect of Beauveria bassiana on the Plant Growth of Kiwi and on Halyomorpha halys Infestation: A Two-Year Field Study

Muhammad M., Basit A., Ali K., Ahmad H., Li W., Khan A., Mohamed H.I.

Phytopathogenic microorganisms have caused blight diseases that present significant challenges to global agriculture. These diseases result in substantial crop losses and have a significant economic impact. Due to the limitations of conventional chemical treatments in effectively and sustainably managing these diseases, there is an increasing interest in exploring alternative and environmentally friendly approaches for disease control. Using endophytic fungi as biocontrol agents has become a promising strategy in recent years. Endophytic fungi live inside plant tissues, forming mutually beneficial relationships, and have been discovered to produce a wide range of bioactive metabolites. These metabolites demonstrate significant potential for fighting blight diseases and provide a plentiful source of new biopesticides. In this review, we delve into the potential of endophytic fungi as a means of biocontrol against blight diseases. We specifically highlight their significance as a source of biologically active compounds. The review explores different mechanisms used by endophytic fungi to suppress phytopathogens. These mechanisms include competing for nutrients, producing antifungal compounds, and triggering plant defense responses. Furthermore, this review discusses the challenges of using endophytic fungi as biocontrol agents in commercial applications. It emphasizes the importance of conducting thorough research to enhance their effectiveness and stability in real-world environments. Therefore, bioactive metabolites from endophytic fungi have considerable potential for sustainable and eco-friendly blight disease control. Additional research on endophytes and their metabolites will promote biotechnology solutions.

Husain M., Sutanto K.D., Rasool K.G., Qureshi J.A., Aldawood A.S.

The date palm, Phoenix dactylifera L., is an ancient and valuable tree that provides food and other products. The date palm trees are attacked by several pests, including the red palm weevil, which is devastating to date palm plantations. Knowledge of the functionality of entomopathogenic fungi, including Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) species, in the tree trunk is critical for controlling date palm weevil and other pests. The goal of this study was to assess the movement of the entomopathogenic fungus, B. bassiana, within the date palm tree. Beauveria bassiana (BbSA-4) mixed with food colors was trunk-injected using a balloon injector into healthy date palm plants. Trunks were cut into one-meter logs 2, 20, and 86 days post-injection. Each log was further dissected into four quarters to examine the present of the fungus. The appearance of food colors and the detection of fungal spores at different heights from the point of injection revealed the translocation of B. bassiana within the trunk. The samples were taken from several locations where food color could be visible, and the distance traveled by the fungal spores was measured. The injected palm tissue samples were cultured on PDA media in the laboratory, and the present of fungal spores was confirmed. B. bassiana (BbSA-4) was found to be surviving in all treated date palm trees. The survival rate of isolate BbSA-4 averaged 70.5%, 34.9%, and 13.9% from dissected trunks examined at 2, 20, and 86 days, respectively, after injection. Isolate BbSA-4 was more apparent in the trunk after spiral injected than bottom injection. The findings revealed that using an entomopathogenic fungus as an endophytic to supplement IPM programs could be beneficial.

Abdrabo K.A., Phang G.J., Rahmadani S.Y., Huang Y.

AbstractLaurel wilt disease, caused by the fungus Harringtonia lauricola and transmitted by the ambrosia beetle Xyleborus glabratus, poses a significant ecological and economic threat to various species of the Lauraceae family, particularly avocado. The disease is characterized by the formation of tyloses blocking xylem vessels, hindering water conductance, and decreasing leaf gas exchange. The relationship between the fungus and the beetle is complex and not fully understood, which can be described, in general, as ambrosial symbiosis depending on the habitat. The secretome of the pathogen includes hydrolytic enzymes that aid in colonization and resistance of host defence. This paper reviews the current understanding of the causes, impacts, and management strategies for laurel wilt disease. Also, it provides an overview of the complex relationship between the fungal pathogen and its beetle vector and explores the various virulence factors and secretome of H. lauricola that contribute to the aggressive nature of the disease. Moreover, this review states the ecological and economic impacts of laurel wilt, particularly on ecologically and economically valuable plants such as avocado. Current management strategies for controlling the disease, including the use of insecticides, fungicides, and biological control methods, are reviewed. Finally, we highlight some critical key points in ambrosia symbiosis biology that are of importance for disease control.

Mantzoukas S., Koutsogeorgiou E.I., Lagogiannis I., Gogolashvili N., Fifis G.T., Navrozidis E.I., Thomidis T., Andreadis S.S.

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is becoming a major pest of Greece’s agricultural production, including tree fruit. Until now, the control of this pest has been based on conventional methods, with the application of chemical insecticides being the primary option. However, the wide distribution of H. halys, in combination with the large area of tree fruit production in Greece, raise the need for alternative control methods. In this study, we investigated the possibility of implementing microbial control agents for managing H. halys. Eggs and nymphs of H. halys were treated with 15 native entomopathogenic fungal isolates and their virulence was evaluated in the laboratory. After treatment, egg hatching time was recorded for 7 days and ranged from 4.5 to 7.0 days. Nymphal survival was recorded daily for 7 days following application and ranged from 2.1 to 6.6 days for second instar nymphs and 3.7 to 6.8 days for fourth instar ones. Beauveria varroae isolate displayed the highest toxicity to all H. halys stages that were tested and could be considered a promising biocontrol agent of this insect. Please check and confirm that the authors and their respective affiliations have been correctly identified and amend if necessary.οκ

Fite T., Kebede E., Tefera T., Bekeko Z.

Plant-associated endophytic fungi (EFs) are emerging as a promising solution to advancing modern agriculture and fostering environmental sustainability, especially in the face of climate change scenarios. These fungi, either naturally residing in plants or introduced through artificial inoculation techniques, improve agricultural production due to their various roles in protecting and supporting host plants. The majority of EFs serve as natural biocontrol agents for a variety of agricultural pests, such as insects, phytopathogens, nematodes, and weeds. Notably, EFs produce secondary metabolites, trigger immune responses, modify plant defense gene expression, confer host plant resistance and/or tolerance, and regulate pest growth, populations, and survival to combat agricultural pests. Beyond controlling pests, EFs promote optimal plant growth, development, and resilience by aiding in the synthesis of vital compounds such as phytohormones and bioactive metabolites, nutrient acquisition, and fortifying plants against environmental stresses and climatic changes. Moreover, the mostly nonpathogenic nature of EFs, coupled with their high yield potential, environmental safety, and cost effectiveness, positions them as eco-friendly and economically viable alternatives to synthetic agrochemicals amidst rapid climate change scenarios. As a result, the promising horizon of EFs in agricultural production necessitates interdisciplinary study and microbial modulation approaches to optimize symbiotic plant-EF relationships and their potential for improved productivity. This review provides current and comprehensive insights into the practical applications and multifaceted benefits of EFs in pest management, plant growth promotion, and climate change resilience for future agricultural production improvements. The analysis reveals the potential of developing EFs into innovative bioformulations such as biofertilizers, biostimulants, and biopesticides, thereby paving the way for their integration into a sustainable and more resilient future agricultural system.

Wippel K.

Beneficial microorganisms colonizing internal plant tissues, the endophytes, support their host through plant growth promotion, pathogen protection, and abiotic stress alleviation. Their efficient application in agriculture requires the understanding of the molecular mechanisms and environmental conditions that facilitate in planta accommodation. Accumulating evidence reveals that commensal microorganisms employ similar colonization strategies as their pathogenic counterparts. Fine-tuning of immune response, motility, and metabolic crosstalk accounts for their differentiation. For a holistic perspective, in planta experiments with microbial collections and comprehensive genome data exploration are crucial. This review describes the most recent findings on factors involved in endophytic colonization processes, focusing on bacteria and fungi, and discusses required methodological approaches to unravel their relevance within a community context.

Airin A.A., Arafat M.I., Begum R.A., Islam M.R., Seraj Z.I.

Abstract Background Plant growth-promoting endophytic fungi (PGPEF) that are associated with halophytes have the potential to boost crop salinity tolerance and productivity. This in turn has the potential of enabling and improving cultivation practices in coastal lands affected by salt stress. Methods Endophytic fungi from the wild halophytic rice Oryza coarctata were isolated, characterized, identified, and studied for their effects on all developing stages of rice plant growth and their yields both with and without salt stress. Key results In this study, three different fungal endophytes were isolated from the halophytic wild rice Oryza coarctata. Two isolates were identified as Talaromyces adpressus (OPCRE2) and Talaromyces argentinensis (OPCRh1) by ITS region sequencing. The remaining isolate NPCRE2 was confirmed as a novel strain named Aspergillus welwitschiae Ocstreb1 (AwOcstreb1) by whole genome sequencing. These endophytes showed various plant growth-promoting (PGP) abilities in vitro (e.g., IAA, ACC-deaminase and siderophore production, phosphate, and zinc solubilization as well as nitrogen fixation), where AwOcstreb1 was significantly more efficient compared to the other two isolates at high salinity (900 mm). Independent application of these fungi in commercial rice (Oryza sativa) showed significant elevation in plant growth, especially in the case of the AwOcstreb1 inoculants, which had enhanced metabolite and chlorophyll content at the seedling stage in both no-salt control and 100-mm salt-stressed plants. At the same time, AwOcstreb1-treated plants had a significantly lower level of H2O2, electrolyte leakage, and Na+/K+ ratio under saline conditions. Higher expression (1.6 folds) of the SOS1 (salt overly sensitive 1) gene was also observed in these plants under salinity stress. This strain also improved percent fertility, tillering, panicle number, and filled grain number in both no-salt control and 45-mm salt-stressed inoculated plants at the reproductive stage. Consequently, the differences in their yield was 125.16% and 203.96% (p < 0.05) in colonized plants in normal and saline conditions, respectively, compared to uninoculated controls. Conclusions We propose that AwOcstreb1 is a potential candidate for an eco-friendly biofertilizer formula to improve the cultivation and yield of rice or any other crop in the highly saline coastal regions of Bangladesh.

Akter, Mimma A.A., Haque M.A., Hossain M.M., Ghosh T.K., Zinan N., Chowdhury M.Z., Islam S.M.

One of the most important abiotic factors that hinder plant development, growth, and production is salt stress. In recent years, there has been a lot of interest in the biological treatment of salt stress in plants using beneficial microbes. The fungal endophyte Beauveria bassiana provides a wide variety of ecosystem services, like suppressing insect pests and pathogens and enhancing plant growth. However, the role of B. bassiana in reducing salt stress in plants has not yet been clarified. This study was undertaken to evaluate the performance of B. bassiana isolate BeauA1 primed rice under salt stress by estimating rice growth, stress parameters, and mitigator characteristics. Primarily, rice seeds were primed with BeauA1 and placed in an agar medium with 120 mM NaCl (≈12 dS m−1 salt solution) to observe the role of BeauA1 in the early establishment of rice seedlings in salt conditions. Seed priming with BeauA1 resulted in an enhancement of rice growth attributes under both control and NaCl stress conditions. In the pot experiment, the BeauA1 primed rice seedlings were planted in soil with different concentrations of salt, viz. 8, 10, and 12 dS m−1. The BeauA1 primed rice plants showed improvement in leaf succulence, leaf area, photosynthetic pigments, and shoot relative water content (RWC), leading to enhanced growth under both salt stress and control conditions. The biochemical study found that BeauA1 considerably increased proline content, total soluble sugars, total carbohydrates, and K+/Na+ in leaves. The antioxidant enzymes catalase (CAT), ascorbate peroxidase (APX), peroxidase (POD), glutathione S-transferase (GST), and nonenzymatic antioxidants phenol and flavonoid were upregulated in BeauA1-primed plants under both control and stressed conditions. Further significant reductions of the lipid peroxidation products malondialdehyde (MDA) and hydrogen peroxide (H2O2) by BeauA1 under salt stress were consistent with higher antioxidant activities in salt stress conditions. Principal component analysis (PCA) further validated BeauA1-primed plants' modulation of growth, antioxidant defense, and reduction of MDA and H2O2 in rice under salt-stress conditions. Our findings indicated that utilizing BeauA1 to reduce salt stress would be a useful strategy to increase rice yield in salt-affected regions.

Tamburini G., Laterza I., Nardi D., Mele A., Mori N., Pasini M., Scaccini D., Pozzebon A., Marini L.

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), native to eastern Asia, has become one of the most serious pests of fruit orchards worldwide. This invasive species is highly polyphagous and capable of moving across the agricultural matrix at long distances. However, comprehensive studies exploring how landscape characteristics influence H. halys colonization of orchards are still lacking. Here, we investigated the impact of landscape composition on the trap captures of H. halys in 113 orchards of different fruit tree crops (i.e., apple, pear, peach, walnut and kiwi) in northern Italy. We found that landscapes rich in semi-natural habitats and vineyards and poor in annual crops supported a higher abundance of H. halys juveniles in traps. This pattern became more evident towards the end of the growing season as the abundance of juveniles increased. Adults were instead not affected by the landscape. The invasive stink bug best responded to landscape processes at large spatial scales (3000 m) confirming its high dispersal ability. Moreover, H. halys did not display a strong preference among fruit orchards, although fewer individuals were caught in walnut orchards. Our findings suggest that the habitat composition of agricultural landscapes is a key factor driving the dynamics of this pest in agroecosystems and that semi-natural habitats might be important in supporting H. halys populations and crop colonization. These effects are however limited to juveniles while adult density was similar even in landscapes with very contrasting structures.

Muola A., Birge T., Helander M., Mathew S., Harazinova V., Saikkonen K., Fuchs B.

AbstractBackgroundCultivation of oilseed rape Brassica napus is pesticide‐intensive, and alternative plant protection strategies are needed because both pesticide resistance and legislation narrow the range of effective chemical pesticides. The entomopathogenic fungus Beauveria bassiana is used as a biocontrol agent against various insect pests, but little is known about its endophytic potential and role in plant protection for oilseed rape. First, we studied whether B. bassiana can establish as an endophyte in oilseed rape, following seed inoculation. To evaluate the plant protection potential of endophytic B. bassiana on oilseed rape, we next examined its ability to induce plant metabolite biosynthesis. In another experiment, we tested the effect of seed inoculation on seedling survival in a semi‐field experiment.ResultsBeauveria bassiana endophytically colonized oilseed rape following seed inoculation, and, in addition, natural colonization was also recorded. Maximum colonization rate was 40%, and generally increased with inoculation time. Seed inoculation did not affect the germination probability or growth of oilseed rape, but B. bassiana inoculated seeds germinated more slowly compared to controls. Endophytic colonization of B. bassiana induced biosynthesis of several flavonoids in oilseed rape leaves under controlled conditions. In the experiment conducted in semi‐field conditions, inoculated seedlings had slightly higher mortality compared to control seedlings.ConclusionBeauveria bassiana showed endophytic potential on oilseed rape via both natural colonization and seed inoculation, and it induced the biosynthesis of flavonoids. However, its use as an endophyte for plant protection against pests or pathogens for oilseed rape remains unclear. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Rocha J.P., Nunes T.V., Rodrigues J.N., Lima N.M., Rocha P.A., Pinto I.D., Sarmento M.I., Araújo W.L., de Moraes C.B., Sarmento R.A.

The galling insect Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) is a major limiting factor in the cultivation of drought-tolerant eucalyptus. The insect L. invasa is a major pest of eucalyptus plantations, and Beauveria bassiana (Bals.) Vuill (Ascomycota: Hypocreales) is being investigated as a potential biocontrol agent against this pest. The fungus B. bassiana can produce metabolites that affect insect biology and survival. Here, we investigated the ability of the entomopathogenic B. bassiana to endophytically develop and induce resistance to L. invasa in a drought-tolerant eucalyptus hybrid. In a greenhouse under semi-controlled conditions, a group of seedlings were sprayed with a solution containing the fungal spores of B. bassiana. The uninoculated seedlings and seedlings inoculated were infested with L. invasa, and their morphometric responses, gas exchange, and chlorophyll indexes were assessed. The number of leaves and height of the inoculated plants was higher than those of the uninoculated plants. The mean CO2 assimilation rate (A) and transpiration rate (E) were higher for inoculated plants. The inoculated plants showed higher chl a and chl b contents. Compared to the uninoculated plants, the inoculated plants developed much fewer galls, while some showed only scar formations where L. invasa deposited its eggs. These results indicated that inoculating Eucalyptus with B. bassiana promoted resistance to L. invasa. To the best of our knowledge, this is the first study showing that an entomopathogenic fungus can develop endophytically to promote resistance against a galling insect pest.

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.

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.

McKinnon A.C., Ridgway H.J., Mendoza Mendoza A., Glare T.R.

Bhattacharyya P.N., Sarmah S.R., Roy S., Sarma B., Nath B.C., Bhattacharyya L.H.

Injudicious and indiscriminate use of toxic chemicals in tea deteriorates the plant, soil, and environment and escalates maximum residue limits (MRLs) in the end products. This requires for the adoption of safe, eco-friendly and non-chemical sustainable alternatives in tea. Beauveria bassiana is an entomopathogenic fungus that displayed high potential for controlling a wide range of tea pests, including the old looper Biston (= Buzura) suppressaria and the emerging looper Hyposidra talaca, as well as the red spider mite (Oligonychus coffeae) and the tea mosquito bug (Helopeltis theivora). The purpose of this review is to broaden our understanding of B. bassiana-mediated pest control in tea and its action mechanisms in crop protection. This fungal species is known to produce a wide variety of mycotoxins and enzymes in its spores that kill or inhibit the metabolic activity of pests. Numerous environmental and physiological factors, such as moisture, pH, humidity, temperature, atmospheric CO2 concentrations, and fungal spore load (colony forming unit/ml), spore viability, enzyme types in action, host plant chemistry and interactions, insect host species, and insect life stages, can speed up or slow down the microbial-mediated pest interaction in plants. The development of the fungus, sporulation, and multiplication within the host are all influenced by prevailing weather conditions and climate change. Studies on entomopathogen compatibility with tea agrochemicals are critical for optimal field application and adoption of suitable integrated pest management (IPM) schedules. Understanding the physiological, genetic, and molecular perspectives of entomopathogenesis and recent developments to improve mycoinfection could provide novel insights to enhance B. bassiana-mediated pest management in tea. Key steps for quality product formulations and their significance for future sustainability in tea include registering and patenting of biopesticides, mass production, and commercialisation of quality strains.