Roles of plant volatiles in defence against microbial pathogens and microbial exploitation of volatiles

Plants emit a large variety of volatile organic compounds during infection by pathogenic microbes, including terpenes, aromatics, nitrogen‐containing compounds, and fatty acid derivatives, as well as the volatile plant hormones, methyl jasmonate, and methyl salicylate. Given the general antimicrobial activity of plant volatiles and the timing of emission following infection, these compounds have often been assumed to function in defence against pathogens without much solid evidence. In this review, we critically evaluate current knowledge on the toxicity of volatiles to fungi, bacteria, and viruses and their role in plant resistance as well as how they act to induce systemic resistance in uninfected parts of the plant and in neighbouring plants. We also discuss how microbes can detoxify plant volatiles and exploit them as nutrients, attractants for insect vectors, and inducers of volatile emissions, which stimulate immune responses that make plants more susceptible to infection. Although much more is known about plant volatile–herbivore interactions, knowledge of volatile–microbe interactions is growing and it may eventually be possible to harness plant volatiles to reduce disease in agriculture and forestry. Future research in this field can be facilitated by making use of the analytical and molecular tools generated by the prolific research on plant–herbivore interactions.A. H. and T. A. are funded by South African National Research Council Incentive Funds (2019) and the University of Pretoria, and J. G. is funded by the Max Planck Society.https://wileyonlinelibrary.com/journal/pce2020-10-01hj2020BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant PathologyZoology and Entomolog

Bark beetle population dynamics in the Anthropocene: Challenges and solutions

Tree-killing bark beetles are the most economically important insects in conifer forests worldwide. However, despite N200 years of research, the drivers of population eruptions and crashes are still not fully understood and the existing knowledge is thus insufficient to face the challenges posed by the Anthropocene. We critically analyze potential biotic and abiotic drivers of population dynamics of an exemplary species, the European spruce bark beetle (ESBB) (Ips typographus) and present a multivariate approach that integrates the many drivers governing this bark beetle system. We call for hypothesis-driven, large-scale collaborative research efforts to improve our understanding of the population dynamics of this and other bark beetle pests. Our approach can serve as a blueprint for tackling other eruptive forest insects

Phytophthora : an underestimated threat to agriculture, forestry, and natural ecosystems in sub-Saharan Africa

This article is part of the “Topical collection—since de Bary: Progress in Phytophthora researchAVAILABILITY OF DATA AND MATERIALS : The dataset associated with this study is available through the Mendeley Data (https://doi.org/10.17632/8khwwsn3xx.1) and as supporting data with this article.Phytophthora species are highly destructive plant pathogens and pose a significant threat to plants in various ecosystems, including agriculture, forest plantations, and natural environments. In sub-Saharan Africa, a total of 77 Phytophthora species have been identified and this review aims to provide an overview of the species diversity and progress of Phytophthora research in this region. Numerous important studies have been carried out in this region, contributing significantly to our understanding of Phytophthora in various research fields. However, compared to global data, the advancement of Phytophthora research in sub-Saharan Africa has been relatively slow. This is evident from the fact that some countries in the region have yet to report the presence of Phytophthora species. Thus, this review also highlights critical research gaps, particularly concerning the potential impacts of climate change, and suggests specific studies to address these gaps. The identified research studies are of utmost urgency as they not only aim to safeguard the iconic floral biodiversity of the region but also play a crucial role in enhancing the economy and ensuring food security.Open access funding provided by University of Pretoria. Forestry South Africa (FSA), the University of Pretoria and the Tree Protection Cooperative Programme (TPCP) and Forestry and Agricultural Biotechnology Institute (FABI).http://link.springer.com/journal/11557am2024BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant PathologyZoology and EntomologySDG-02:Zero HungerSDG-15:Life on lan

Tree defence and bark beetles in a drying world: carbon partitioning, functioning and modelling

Drought has promoted large‐scale, insect‐induced tree mortality in recent years, with severe consequences for ecosystem function, atmospheric processes, sustainable resources and global biogeochemical cycles. However, the physiological linkages among drought, tree defences, and insect outbreaks are still uncertain, hindering our ability to accurately predict tree mortality under on‐going climate change. Here we propose an interdisciplinary research agenda for addressing these crucial knowledge gaps. Our framework includes field manipulations, laboratory experiments, and modelling of insect and vegetation dynamics, and focuses on how drought affects interactions between conifer trees and bark beetles. We build upon existing theory and examine several key assumptions: 1) there is a trade‐off in tree carbon investment between primary and secondary metabolites (e.g. growth vs. defence); 2) secondary metabolites are one of the main component of tree defence against bark beetles and associated microbes; and 3) implementing conifer‐bark beetle interactions in current models improves predictions of forest disturbance in a changing climate. Our framework provides guidance for addressing a major shortcoming in current implementations of large‐scale vegetation models, the under‐representation of insect‐induced tree mortality

Comparative genomic and metabolomic analysis of Termitomyces species provides insights into the terpenome of the fungal cultivar and the characteristic odor of the fungus garden of Macrotermes natalensis termites

Macrotermitinae termites have domesticated fungi of the genus Termitomyces as food for their colony, analogously to human farmers growing crops. Termites propagate the fungus by continuously blending foraged and predigested plant material with fungal mycelium and spores (fungus comb) within designated subterranean chambers. To test the hypothesis that the obligate fungal symbiont emits specific volatiles (odor) to orchestrate its life cycle and symbiotic relations, we determined the typical volatile emission of fungus comb biomass and Termitomyces nodules, revealing α-pinene, camphene, and d-limonene as the most abundant terpenes. Genome mining of Termitomyces followed by gene expression studies and phylogenetic analysis of putative enzymes related to secondary metabolite production encoded by the genomes uncovered a conserved and specific biosynthetic repertoire across strains. Finally, we proved by heterologous expression and in vitro enzymatic assays that a highly expressed gene sequence encodes a rare bifunctional mono-/sesquiterpene cyclase able to produce the abundant comb volatiles camphene and d-limonene. IMPORTANCE The symbiosis between macrotermitinae termites and Termitomyces is obligate for both partners and is one of the most important contributors to biomass conversion in the Old World tropic’s ecosystems. To date, research efforts have dominantly focused on acquiring a better understanding of the degradative capabilities of Termitomyces to sustain the obligate nutritional symbiosis, but our knowledge of the small-molecule repertoire of the fungal cultivar mediating interspecies and interkingdom interactions has remained fragmented. Our omics-driven chemical, genomic, and phylogenetic study provides new insights into the volatilome and biosynthetic capabilities of the evolutionarily conserved fungal genus Termitomyces, which allows matching metabolites to genes and enzymes and, thus, opens a new source of unique and rare enzymatic transformations

Phenolic compound degradation by Pseudomonas syringae phylogroup 2 strains

It has recently been shown that Pseudomonas syringae strains pathogenic to woody hosts belonging to phylogroup (PG) 2 lack phenolic compound degradation pathways such as the beta-ketoadipate and protocatechuate pathways. The aim of this study was to analyse a selection of P. syringae PG 2 genomes, including those used previously to determine if they had other phenolic compound degradation pathways and to determine whether or not they were functional. Twenty-one publicly available genomes of PG 2 strains were analyzed. These strains had previously been isolated from both woody and herbaceous hosts. Phenolic degradation enzymes were present in 5 (23%) of the strains analysed, originating from both woody and herbaceous hosts. Hypothetical pathways were proposed to determine if catechol, anthranilate and benzoic acid were degraded by these strains. Both spectrophotometric and HPLC were used to determine phenolic compound degradation. The five strains with phenolic degradation enzymes were able to metabolize catechol, and HRI-W 7924 and MAFF 301072 could also metabolize anthranilate and benzoate, respectively. The study showed that even though some PG 2 strains lack the beta-ketoadipate and protocatechuate pathways, they still have phenolic compound degrading enzymes that may play a role in virulence.The Horticultural Knowledge Group (HORTGRO) and National Research Foundation (NRF).https://link.springer.com/journal/421612019-07-01am2019BiochemistryForestry and Agricultural Biotechnology Institute (FABI)Microbiology and Plant PathologyZoology and Entomolog

Bark beetle attack history does not influence the induction of terpene and phenolic defenses in mature Norway spruce (Picea abies) trees by the bark beetle-associated fungus Endoconidiophora polonica

Terpenes and phenolics are important constitutive and inducible conifer defenses against bark beetles and their associated fungi. In this study, the inducible defenses of mature Norway spruce (Picea abies) trees with different histories of attack by the spruce bark beetle, Ips typographus were tested by inoculation with the I. typographusassociated fungus Endoconidiophora polonica. We compared trees that had been under previous attack with those under current attack and those that had no record of attack. After fungal inoculation, the concentrations of mono-, sesqui-, and diterpenes in bark increased 3- to 9-fold. For the phenolics, the flavan-3-ols, catechin, and gallocatechin, increased significantly by 2- and 5-fold, respectively, while other flavonoids and stilbenes did not. The magnitudes of these inductions were not influenced by prior bark beetle attack history for all the major compounds and compound classes measured. Before fungal inoculation, the total amounts of monoterpenes, diterpenes, and phenolics (constitutive defenses) were greater in trees that had been previously attacked compared to those under current attack, possibly a result of previous induction. The transcript levels of many genes involved in terpene formation (isoprenyl diphosphate synthases and terpene synthases) and phenolic formation (chalcone synthases) were significantly enhanced by fungal inoculation suggesting de novo biosynthesis. Similar inductions were found for the enzymatic activity of isoprenyl diphosphate synthases and the concentration of their prenyl diphosphate products after fungal inoculation. Quantification of defense hormones revealed a significant induction of the jasmonate pathway, but not the salicylic acid pathway after fungal inoculation. Our data highlight the coordinated induction of terpenes and phenolics in spruce upon infection by E. polonica, a fungal associate of the bark beetle I. typographus, but provide no evidence for the priming of these defense responses by prior beetle attack.Zwillenberg-Tietz Foundation and the Max Planck Society.https://www.frontiersin.org/journals/plant-sciencedm2022Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog