For plants, soil fungi of the genus Metarhizium are the perfect friends with benefits. While these fungi have long been known to be loyal friends to plants by infecting and killing insect pests, which would otherwise feed on them. Metarhizium can also exist as free-living saprophytes, rhizosphere colonizers or live endophytically in a symbiotic relationship with plants. As plant colonizers, these fungi boost plant growth, nutrition, and alleviate biotic and abiotic stresses. Their ability to change plant hormone levels, volatile emission profiles and secondary metabolite production results in changes in insect performance and preferences and impacts insect development, food consumption, oviposition, and larval survival and primes plants against pathogens. Only recently has the fungus’ ability to alternate between these lifestyles been truly appreciated and understood. The utilization of Metarhizium species as plant symbionts and simultaneous biopesticides has the potential to minimize crop losses and improve agricultural practices for more efficacy and yield.
1 - Metarhizium – the insect pathogen
Metarhizium is well-known for its ability to infect and kill a wide range of agriculturally important insects by contact, which makes them valuable to growers as bioinsecticides. Most typically, germinating fungal conidia penetrate the insect’s cuticle, differentiate into blastospores that then circulate inside the body, robbing the insect of nutrients and overpower the immune system. Insecticidal metabolites kill the host, and the fungus breaches the cuticle to colonize the body externally with conidia, which disperse to start new infections. Commercialized products containing Metarhizium are used worldwide; in what is considered the most successful biological control programme anywhere: the treatment of over 2-million hectares of sugarcane in Brazil every year, to control spittlebugs. Lallemand Plant Care currently contributes towards this successful biological control program with its Metarhizium-based biopesticide Opala in Brazil.
2 - Metarhizium – the symbiotic endophyte and plant colonizer
Endosymbiosis is a common strategy throughout the tree of life. Corals, for example, house algae in their skeleton in exchange for nutrients, and humans offer bacteria in our guts a safe and stable environment in exchange for their help in breaking down nutrients. More than 80% of vascular plants also co-occur with mycorrhiza fungi, which cannot survive without their plant partner. Fungi such as Metarhizium can be found living inside plant roots or growing in soil, nourishing themselves on dead organic matter. When found as root endophytes, Metarhizium collects a literal carbon tax of their plant host in exchange for several important services:
- promoting plant growth
- enhancing nutrient uptake
- enhancing tolerance to biotic (pests and pathogens) and to abiotic stresses (salinity and drought).
2.1 Enhanced plant growth promotion
Metarhizium produces indole-3-acetic acid (IAA), a best-known auxin that regulates plant growth, stimulates seed germination, increases root development, and controls vegetative growth processes. Studies reveal that Metarhizium can produce IAA in higher concentrations than Trichoderma harzianum, a species known for its plant growth stimulation. This function is in lots of ways like the function of mycorrhizal fungi, which themselves promote growth, root architecture and seed germination. Metarhizium also produces a diverse range of secondary metabolites including, volatile organic compounds (VOCs), which also contributes towards plant growth promotion. Two key VOCs, 1-octen-3-ol and 3-octanone, produced by the fungus, were able to significantly increase root and shoot growth of a wide range of commercially relevant crops. In doing so, the auxins and VOCs released by Metarhizium also boosts nutrient and water uptake by the plants leading to greater yields.
2.2 Enhanced nutrient uptake
There is growing awareness that insect pathogenicity and the ability of Metarhizium to associate endophytically with plants, are elegantly coupled to provide an active method of insect-derived nitrogen (N) transfer to plants via fungal hyphae. In fact, an experimental study showed that grasses and beans contained between 1-26% (estimated to be 0.5-7.4 kg/hectare/year) of insect-derived nitrogen when Metarhizium-infected insects were deposited in the soil. Such express delivery of nitrogen to plant roots is likely to stimulate growth and development in a wide variety of agricultural crops. So far Metarhizium was documented to endophytically colonize tomato (Solanum lycopersicum), potato (Solanum tuberosum), peanut (Arachis hypogaea), haricot bean (Phaseolus vulgaris), soybean (Glycine max), switchgrass (Panicum virgatum), wheat (Triticum aestivum) and cassava (Manihot esculenta). In agriculture, chemical fertiliser and pesticides have been in heavy usage ever since their inception. Chemical fertiliser and control agents have their pitfalls, however, and a clear shift away from chemicals towards the use of biological fertiliser and control agents is needed to maintain yields and increase sustainability.
Solubilization of phosphorus (P) from mineral and organic sources has also been verified for Metarhizium several times. These data highlight the potential of Metarhizium to improve the P content in plants and to enhance plant growth. The same is true for iron (Fe), one of the most abundant elements on earth and an essential micronutrient for several living organisms. Siderophores play an important role in iron uptake by plants and siderophore-secreting microorganisms, like Metarhizium, inside plant tissues act in the transport of Fe3+ for the synthesis of ATP, chlorophyll, and DNA, contributing to plant growth and yield. Some studies indicated that the siderophore production by Metarhizium could be involved in plant growth promotion while other studies have shown that Metarhizium-produced siderophores play an important role during insect infection and fungal virulence.
2.3 Enhanced plant tolerance to biotic and abiotic stress
Metarhizium aids their plant host in modulating their hormonal responses to insects and pathogens, and changes volatile emission profiles and secondary metabolite production, all of which induce plant defence. These changes impact insect performance and preferences and primes plants against pathogens. This is important to growers because inoculation with Metarhizium could significantly reduce the amount of damage caused by insects and mites, by retarding insect development, providing a feeding deterrent and restricting insect survival and oviposition. It also reduces the occurrence of plant pathogens, which together contribute towards decreased crop yields.
Jasmonic acid (JA), for instance, is a hormone employed by plants to signal and coordinate defences against chewing insects. Some studies in maize show that inoculated Metarhizium altered gene expression in the JA biosynthesis pathways, which proactively increased maize defence against herbivours. There is a high cost to the plant in mobilizing defence pathways that can change the quality of the plant as a food resource and affect the feeding rate of insects. Foliar feeding pests like mites, can also be significantly reduced after Metarhizium colonization, as was observed in several commercial strawberry fields in Brazil, where inoculated plants had increased yields and lower mite populations compared to controls. The systemic effects of Metarhizium applied to faba bean (Vicia faba) seeds reduced the growth rates, offspring performance and fecundity of two aphid species and seedling survival was increased by 20-100% compared to the non-treated control. In addition, the role of some Metarhizium-produced VOCs was found to have insect repellent activity and deterred the banana weevil, Cosmopolites sordidus (Coleoptera: Curculionidae).
Metarhizium is also able to protect bean roots from fungal pathogens, like Fusarium solani f. sp. phaseoli. This protection may be through the secretions of secondary metabolites from Metarhizium or through the enhancement of plant phytoalexins (isoflavonoids) and terpenoids which are produced during the symbiotic associations of the beneficial fungus with plants which reduce the effects of plant pathogens. Metarhizium root colonization can also prime the immune system of plants, leading to reduced pathogen infections. Plants can recognise their beneficial fungal friends from pathogens because they can short-circuit plant defence responses by reducing abscisic acid (ABA), increasing stomatal size, and decreasing relative expression of immune response genes compared to pathogens which have the opposite effect.
As for abiotic stress tolerance, this well-known rhizocompetent fungus has been shown to alleviate salinity stress with enhanced plant growth promotion. Tomato plants inoculated with Metarhizium and exposed to salt stress showed significantly enhanced growth attributes such as seedling height, vigour index, and fresh and dry weight of seedlings during the seedling stage and had thicker root epidermis and improved xylem tissue compared to control plants. Metarhizium inoculated tomato plants also enhanced the production of the biochemical elements (phenolics, and flavonoids content of the osmolyte proline, which is critical in maintaining osmotic balance) required for plants to endure There are many hypotheses, based on the ability of other endophytic fungi that suggest plant tolerance to drought may be possible with Metarhizum but no definitive study was found.
3 - Metarhizium – allies with many benefits
Metarhizium’s overall strategy is to be exploitative of short-lived insect hosts but beneficial friends to plants that provide them a stable environment. They have an ability to kill a wide range of insects, which maximises protection to plants and provides them nitrogen from a frequently encountered source that the fungus trades from carbon. As key player amongst members of the rhizosphere, Metarhizium can assist plant development and persistence in the face of insect pests, pathogens, nutrient scarcity, and abiotic stress. A better understanding of Metarhizium’s symbiotic relationship and its value-added benefits to plants opens new opportunities for the application of these fungi in agroecosystems. The application of Metarhizium in the production of diverse crops, like grains and vegetables, will allow us to enter in an era of novel, biocontrol strategies that will bring value to crop protection for growers.
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