Like all other plants, trees are vulnerable to attack by a multitude of pests and pathogens. Current control measures for many of these diseases are limited and relatively ineffective. Several methods, including the use of conventional synthetic agro-chemicals, are employed to reduce the impact of pests and diseases. However, because of mounting concerns about adverse effects on the environment and a variety of economic reasons, this limited management of tree diseases by chemical methods is losing ground. The use of biological control, as a more environmentally friendly alternative, is becoming increasingly popular in plant protection. This can include the deployment of soil inoculants and foliar sprays, but the increased knowledge of microbial ecology in the phytosphere, in particular phylloplane microbes and endophytes, has stimulated new thinking for biocontrol approaches. Endophytes are microbes that live within plant tissues. As such, they hold potential as biocontrol agents against plant diseases because they are able to colonize the same ecological niche favoured by many invading pathogens. However, the development and exploitation of endophytes as biocontrol agents will have to overcome numerous challenges. The optimization and improvement of strategies employed in endophyte research can contribute towards discovering effective and competent biocontrol agents. The impact of environment and plant genotype on selecting potentially beneficial and exploitable endophytes for biocontrol is poorly understood. How endophytes synergise or antagonise one another is also an important factor. This review focusses on recent research addressing the biocontrol of plant diseases and pests using endophytic fungi and bacteria, alongside the challenges and limitations encountered and how these can be overcome. We frame this review in the context of tree pests and diseases, since trees are arguably the most difficult plant species to study, work on and manage, yet they represent one of the most important organisms on Earth.
Bacterial canker is a major disease of Prunus species, such as cherry (Prunus avium). It is caused by Pseudomonas syringae pathovars, including P. syringae pv. syringae (Pss) and P. syringae pv. morsprunorum race 1 (Psm1) and race 2 (Psm2). Concerns over the environmental impact of, and the development of bacterial resistance to, traditional copper controls calls for new approaches to disease management. Bacteriophagebased biocontrol could provide a sustainable and natural alternative approach to combat bacterial pathogens. Therefore, seventy phages were isolated from soil, leaf and bark of cherry trees in six locations in the south east of England. Subsequently, their host range was assessed against strains of Pss, Psm1 and Psm2. While these phages lysed different Pss, Psm and some other P. syringae pathovar isolates, they did not infect beneficial bacteria such as Pseudomonas fluorescens. A subset of thirteen phages were further characterized by genome sequencing, revealing five distinct clades in which the phages could be clustered. No known toxins or lysogeny-associated genes could be identified. Using bioassays, selected phages could effectively reduce disease progression in vivo, both individually and in cocktails, reinforcing their potential as biocontrol agents in agriculture.
The global sustainability agenda is increasing the demand for reduction in inputs into agricultural production while maintaining profitable yield of quality products. Plant diseases are a major constraint for both yield and product quality, but often tools for their control are ineffective or lacking. Biological control using antagonistic microorganisms has long been a subject of research resulting in a wide range of products that are now available and marketed in specific territories around the world. These preparations are often niche products with narrow uses. The research effort is intense both to develop new biological control agents (BCAs) and to obtain knowledge of the mechanisms underlying biological disease control. The prospects for biological control are promising. As a minimum, BCAs supplement other sustainable disease management practices such as disease resistance, and present opportunities for controlling diseases for which other approaches are ineffective or unavailable. We can realistically expect increasing use of BCAs to control crop diseases in ways that will benefit the environment. This review paper arose from a webinar held by the British Society for Plant Pathology as part of the International Year of Plant Heath (IYPH2020), at which many of the 300 participants posed or discussed interesting questions. This review is based on that input and the panel members at the webinar are all included as co-authors in this review.
The root endophytic fungus Piriformospora indica (Sebacinacea) forms mutualistic symbioses with a broad range of host plants, increasing their biomass production and resistance to fungal pathogens. This study evaluated the effect of P. indica on fusarium crown rot disease of wheat, under in vitro and glasshouse conditions. Interaction of P. indica and Fusarium isolates under axenic culture conditions indicated no direct antagonistic activity of P. indica against Fusarium isolates. Seedlings of wheat were inoculated with P. indica and pathogenic Fusarium culmorum or F. graminearum and grown in sterilized soil‐free medium or in a non‐sterilized mix of soil and sand. Fusarium alone reduced emergence and led to visible browning and reduced root growth. Roots of seedlings in pots inoculated with both Fusarium isolates and P. indica were free of visible symptoms; seed emergence and root biomass were equivalent to the uninoculated. DNA was quantified by real‐time polymerase chain reaction (qPCR). The ratio of FusariumDNA to wheat DNA rose rapidly in the plants inoculated with Fusarium alone; isolates and species were not significantly different. Piriformospora indica inoculation reduced the ratio of Fusarium to host DNA in the root systems. The reduction increased with time. The ratio of P. indica to wheat DNA initially rose but then declined in root systems without Fusarium. With Fusarium, the ratio rose throughout the experiment. The absolute amount of FusariumDNA in root systems increased in the absence of P. indica but was static in plants co‐inoculated with P. indica.
The most economically important biotic stresses in crop production are caused by fungi, oomycetes, insects, viruses, and bacteria. Often chemical control is still the most commonly used method to manage them. However, the development of resistance in the different pathogens/pests, the putative damage on the natural ecosystem, and the toxic residues in the field and thus contamination of the environment have stimulated the search for safer alternatives such as the use of biological control agents (BCAs). Among BCAs, viruses, a major driver for controlling host populations and evolution, are somewhat underused, mostly because of regulatory hurdles that make the cost of registration of such host-specific BCAs not affordable in comparison with the limited potential market. Here, we provide a comprehensive overview of the state of the art of virus-based BCAs against fungi, bacteria, viruses, and insects, with a specific focus on new approaches that rely on not only the direct biocidal virus component but also the complex ecological interactions between viruses and their hosts that do not necessarily result in direct damage to the host. Expected final online publication date for the Annual Review of Phytopathology, Volume 60 is August 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Piriformospora indica (Sebacinaceae) is a cultivable root endophytic fungus. It colonizes the roots of a wide range of host plants. In many settings colonization promotes host growth, increases yield and protects the host from fungal diseases. Evaluation was made of the effect of P. indica on fusarium head blight (FHB) disease of winter (cv. Battalion) and spring (cv. Paragon, Mulika, Zircon, Granary, KWS Willow and KWS Kilburn) wheat and consequent contamination by the mycotoxin deoxynivalenol (DON) under UK weather conditions. Interactions of P. indica with an arbuscular mycorrhizal fungus (Funneliformis mosseae), fungicide application (Aviator Xpro) and low and high fertilizer levels were considered. Piriformospora indica application reduced FHB disease severity and incidence by 70%. It decreased mycotoxin DON concentration of winter and spring wheat samples by 70 and 80%, respectively. Piriformospora indica also increased aboveground biomass, 1000-grain weight and total grain weight. Piriformospora indica reduced disease severity and increased yield in both high and low fertilizer levels. The effect of P. indica was compatible with F. mosseae and foliar fungicide application. Piriformospora indica did not have any effects on plant tissue nutrients. These results suggest that P. indica might be useful in biological control of Fusarium diseases of wheat.
The annual plant Impatiens glandulifera (Himalayan balsam) is the most widespread invasive non‐native weed in the British Isles. Manual control is widely used, but is costly and laborious. Recently, biological control using the rust fungus Puccinia komarovii var. glanduliferae has been trialled. We designed an experiment to assess the impact of these control methods on invertebrate communities in relation to unmanaged and uninvaded habitats, and to determine whether mycorrhizal inoculation aided post‐control recovery of these communities. Sixty invaded and twenty uninvaded field soil blocks were transplanted to the experiment site, where a mycorrhizal inoculum was added to half of all blocks. Biological and mechanical control treatments were applied to twenty invaded blocks independently; the twenty remaining invaded blocks were left intact. Above‐ and belowground invertebrate samples were collected from the blocks at the end of the growing season. Overall, aboveground invertebrate abundance increased with the removal of I. glandulifera, and several groups showed signs of recovery within one growing season. The effect of mechanical control was more variable in belowground invertebrates. Biological control did not affect aboveground invertebrate abundance but resulted in large increases in populations of belowground Collembola. Our experiment demonstrates that mechanical removal of I. glandulifera can cause rapid increases in invertebrate abundance and that its biological control with P. komarovii var. glanduliferae also has the potential to benefit native invertebrate communities.
Piriformospora indica (Sebacinaceae), a root endophytic fungus, was originally isolated from an arid subtropical soil. P. indica forms mutualistic symbioses with a broad range of host plants, increases biomass production, resistance and tolerance to fungal pathogens and abiotic stresses. These characteristics make it a very attractive component of more sustainable agriculture. So, it is desirable to understand its wider ecosystem effects. We determined how long P. indica could survive in the soil and how it interacts with other soil microorganisms and some important arable weeds. Survival of P. indica in the soil, under winter and summer conditions in the UK was tested by isolating DNA and RNA of P. indica from pots of soil which had been left open to winter-summer weather conditions without host plants, followed by PCR and reverse transcription-PCR (RT-PCR) with P. indica-specific primers. P. indica effects on other soil and root microorganisms were tested by PCR-denaturing gradient gel electrophoresis analysis of DNA extracted from soil and roots from pots in which P. indica-infected wheat had been grown. The effect of P. indica on growth of black-grass (Alopecuris myosuroides), wild-oat (Avena fatua) and cleavers (Galium aparine) was tested alone and in competition with wheat. In soil P. indica-mRNA and DNA could still be detected after eight months, but not after 15 months. Soils from P. indica-inoculated pots had distinct fungal and bacterial species communities which were more diverse than non-inoculated controls. P. indica infected A. myosuroides and A. fatua but was not detected in G. aparine. The average above-ground competitiveness of the weeds with wheat was decreased.
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