Biological disease control by beneficial (micro)organisms: Selected breakthroughs in the past 50 years

Biological control of plant disease by beneficial (micro)organisms is one of the main tools available to preserve plant health within the wider context of One Health and in line with the goals of the Agenda 2030 for Sustainable Development. The commercial development of biocontrol agents, together with a new perspective on the resident microbial community, all supported by innovative “omics” technologies, continues to gain in prominence in plant pathology, addressing the need to feed the increasing world population and to assure a safe and secure access to food. The present review considers selected advances within the last 50 years, highlighting those that can be considered as breakthroughs for the biological control research field. Selected examples of successful biocontrol agents and strategies are reported, including the history of the progress in researching Trichoderma isolates as commercial biocontrol agents, the exploitation of mycoviruses to confer hypovirulence to plant pathogenic fungi, the role of microbial communities in the suppressiveness of soils, and evolving approaches including the establishment of Synthetic Microbial Communities (SynCom)

Draft Whole-Genome Sequence of Trichoderma gamsii T6085, a Promising Biocontrol Agent of Fusarium Head Blight on Wheat

Trichoderma gamsii T6085 is a promising beneficial isolate whose effects consist of growth inhibition of the main agents causing Fusarium head blight, reduction of mycotoxin accumulation, competition for wheat debris, and reduction of the disease in both the lab and the field. Here, we present the first genome assembly of a T. gamsii isolate, providing a useful platform for the scientific community

Pathogenic potential of Beauveria pseudobassiana as bioinsecticide in protein baits for the control of the medfly Ceratitis capitata

The medfly, Ceratitis capitata (Wiedemann) (Diptera Tephritidae), is a major insect pest affecting fruit production worldwide whose control is mainly based on the use of protein baits laced with chemical insecticides. Entomopathogenic fungi are well- known to be effective against a wide spectrum of insect pests and are commonly utilized in integrated pest management and bio- logical control programs. Here, we assess the feasibility of using the recently described entomopathogenic species Beauveria pseudobassiana Rehner et Humber (Hypocreales Cordycipitaceae) as a biological insecticide in protein bait sprays for the control of the medfly. Firstly, we evaluated the pathogenicity of B. pseudobassiana against eggs, larvae, pupae and adults of the medfly. Secondly, we tested its efficacy as bioinsecticide in protein bait sprays. The results of the pathogenicity tests showed that B. pseu- dobassiana is able to infect, and lead to the death, all instar of the medfly. The efficacy of B. pseudobassiana was confirmed also when used as bioinsecticide in protein baits. In planta tests, the survival probability (Kaplan-Meier estimates) of flies in contact with the B. pseudobassiana-laced protein bait was significantly lower respect to control. Median survival time of flies treated with B. pseudobassiana-laced protein (6 ± 1.422 d) was at least three times shorter than in control (> 20 d). Based on our results, we confirmed the potential of B. pseudobassiana as bioinsecticide in entomopathogenic fungi-laced protein baits for the control of tephritid fruit flies

Insights on KP4 Killer Toxin-like Proteins of Fusarium Species in Interspecific Interactions

KP4 killer toxins are secreted proteins that inhibit cell growth and induce cell death in target organisms. In Fusarium graminearum, KP4-like (KP4L) proteins contribute to fungal virulence in wheat seedling rot and are expressed during Fusarium head blight development. However, fungal KP4L proteins are also hypothesized to support fungal antagonism by permeabilizing cell walls of competing fungi to enable penetration of toxic compounds. Here, we report the differential expression patterns of F. graminearum KP4L genes (Fgkp4l-1, -2, -3 and -4) in a competitive interaction, using Trichoderma gamsii as the antagonist. The results from dual cultures indicate that Fgkp4l-3 and Fgkp4l-4 could participate in the recognition at the distance of the antagonist, while all Fgkp4l genes were highly activated in the pathogen during the physical interaction of both fungi. Only Fgkp4l-4 was up-regulated during the interaction with T. gamsii in wheat spikes. This suggests the KP4L proteins could participate in supporting F. graminearum interspecific interactions, even in living plant tissues. The distribution of KP4L orthologous within the genus Fusarium revealed they are more represented in species with broad host-plant range than in host-specific species. Phylogeny inferred provides evidence that KP4L genes evolved through gene duplications, gene loss and sequence diversification in the genus Fusarium

A statistical protocol to describe differences among nutrient utilization patterns of Fusarium spp. and Trichoderma gamsii

The Biolog® Phenotype MicroArrays™ (PM) system offers a simple and cheap tool to rapidly providing a high throughput of information about the phenotypes of fungal isolates in a short lapse of time. In order to improve the use of the PM system in fungal ecology studies, in the present work we propose a new statistical protocol based on two approaches, i.e. a functional PCA to describe similarity patterns of growth curves and a Bayesian GAMs to allow inferences on specific growth features, in order to analyse nutrient fungal utilization in a model system including four causal agents of FHB, the natural competitor Fusarium oxysporum and the beneficial isolate Trichoderma gamsii T6085. Analysis of data collected by the Biolog® Phenotype MicroArrays™ (PM) in our biological system showed a different nutritional competitive potential of the four pathogens, as well as an intermediate behaviour of the natural competitor and of our biocontrol agent. This protocol, applicable to different fungal phenotypical studies both at isolate and community level, allows a full exploitation of data obtained by PM system and provides important information about the nutritional pattern of a single isolate compared to those of other fungi, a key information to be exploited in biocontrol strategies

DON on wheat crop residues: effects on mycobiota as a source of potential antagonists of Fusarium culmorum

Fusarium culmorum, a pathogenic fungal species associated with Fusarium Head Blight (FHB) of wheat, can produce the mycotoxin deoxynivalenol (DON) that is frequently found as contaminant in cereals. Wheat haulms, as decomposing plant material, are an important inoculum source of F. culmorum for subsequent crops. In the present work we exploited the mycobiota of haulms buried in natural soil as a source of potential antagonists of F. culmorum and evaluated the role played by DON in determining the composition of such mycobiota. DON was added to wheat haulm pieces that were incubated in three natural soils, namely sandy, clayey and mixed, all with a previous history of wheat cultivation. Composition of mycobiota associated with DON-treated cultural debris was evaluated and compared with mycobiota from control haulms, in order to evaluate the effect of soil type and of the presence of the mycotoxin. Our results showed that DON affected neither the number nor species profile of fungal isolates. Among fungi associated with cultural debris, thirty-nine Pythium spp. isolates were collected and five of them, both from treated and not treated haulms, were tested for their antagonistic ability against F. culmorum. The two strains showing the highest antagonistic activity were further tested against F. oxysporum, a species considered a major competitor of F. culmorum for wheat residues, and frequently recovered from haulms in our experiments. The two Pythium spp. isolates showed a positive antagonistic and mycoparasitic activity against F. culmorum, without affecting the growth of F. oxysporum. Mycobiota of haulms buried in soil represents an interesting source of potential antagonists and competitors for future exploitation in a multitrophic approach for biocontrol of FHB

Corrigendum: UV-B Pre-treatment Alters Phenolics Response to Monilinia fructicola Infection in a Structure-Dependent Way in Peach Skin

[This corrects the article DOI: 10.3389/fpls.2018.01598.]

Draft Whole-Genome Sequence of the Biocontrol Agent Trichoderma harzianum T6776

Trichoderma harzianum T6776 is a promising beneficial isolate whose effects consist of growth promotion, positive response of photosynthetic activity, hormonal signaling, and carbon partitioning in tomato, coupled with biocontrol of plant pathogens. Here, we present the first genome assembly of T6776, providing a useful platform for the scientific community

Understanding the mechanisms underlying biological control of Fusarium diseases in cereals

Many Fusarium species cause serious diseases for cereal cultivation. These include Fusarium head blight and crown rot on wheat and bakanae disease on rice. These represent a major concern both in terms of food security and food safety. The latter is connected with the risk of mycotoxin contamination of grains. Biological control has proven its potential for controlling head blight and crown rot diseases of cereals caused by Fusarium species in a number of studies, and indeed several commercial products are under development. We review current knowledge of the mechanisms underlying biological control with a focus on fungal biocontrol agents, and also include challenges related to co-occurrence of Fusarium species. Several of the established biological control mechanisms (antibiosis, competition, hyperparasitism and induced resistance) can act simultaneously, thus resulting in disease control and, consequently, reduction of mycotoxin contamination. We also review the biological roles of some of the many mycotoxins produced by Fusarium species, and the mechanisms by which they are detoxified by cereal enzymes or by other fungi and how biological control agents (BCAs) can stimulate their degradation. Finally, the effect of biocontrol agents on the resident microbiota, as well as the effect of the resident microbiota on the performances of BCAs, are discussed. New perspectives on the use of biocontrol agents for the management of Fusarium diseases on cereals