A collection of 76 plant-pathogenic and 41 saprophytic Fusarium oxysporum strains was screened for sensitivity to 2,4-diacetylphloroglucinol (2,4-DAPG), a broad-spectrum antibiotic produced by multiple strains of antagonistic Pseudomonas fluorescens. Approximately 17% of the F. oxysporum strains were relatively tolerant to high 2,4-DAPG concentrations. Tolerance to 2,4-DAPG did not correlate with the geographic origin of the strains, formae speciales, intergenic spacer (IGS) group, or fusaric acid production levels. Biochemical analysis showed that 18 of 20 tolerant F. oxysporum strains were capable of metabolizing 2,4-DAPG. For two tolerant strains, analysis by mass spectrometry indicated that deacetylation of 2,4-DAPG to the less fungitoxic derivatives monoacetylphloroglucinol and phloroglucinol is among the initial mechanisms of 2,4-DAPG degradation. Production of fusaric acid, a known inhibitor of 2,4-DAPG biosynthesis in P. fluorescens, differed considerably among both 2,4-DAPG-sensitive and -tolerant F. oxysporum strains, indicating that fusaric acid production may be as important for 2,4-DAPG-sensitive as for -tolerant F. oxysporum strains. Whether 2,4-DAPG triggers fusaric acid production was studied for six F. oxysporum strains; 2,4-DAPG had no significant effect on fusaric acid production in four strains. In two strains, however, sublethal concentrations of 2,4-DAPG either enhanced or significantly decreased fusaric acid production. The implications of 2,4-DAPG degradation, the distribution of this trait within F. oxysporum and other plant-pathogenic fungi, and the consequences for the efficacy of biological control are discussed.
SUMMARYThe fungal genus Verticillium contains ten species, some of which are notorious plant pathogens causing vascular wilt diseases in host plants, while others are known as saprophytes and opportunistic plant pathogens. Whereas the genome of V. dahliae, the most notorious plan pathogen of the genus, has been well characterized, evolution and speciation of other members of the genus received little attention thus far. Here, we sequenced the genomes of the nine haploid Verticillium spp. to study evolutionary trajectories of their divergence from a last common ancestor. Frequent occurrence of chromosomal rearrangement and gene family loss was identified. In addition to ~11,000 core genes that are shared among all species, only 200-600 species-specific genes occur. Intriguingly, these species-specific genes show different features than core genes.
The genetic and biochemical basis of defence mechanisms in plant pathogenic fungi against antifungal compounds produced by antagonistic microorganisms is largely unknown. The results of this study show that both degradative and non-degradative defence mechanisms enable the plant pathogenic fungus Botrytis cinerea to resist the broad-spectrum, phenolic antibiotic 2,4-diacetylphloroglucinol (2,4-DAPG). The efflux pump BcAtrB provides the first line of defence for B. cinerea, preventing accumulation of 2,4-DAPG in the cell to toxic concentrations, whereas the extracellular laccase BcLCC2 mediates, via conversion of tannic acid, subsequent degradation of 2,4-DAPG. Expression of BcatrB is induced by 2,4-DAPG and efflux gives B. cinerea sufficient time to more effectively initiate the process of BcLCC2-mediated antibiotic degradation. This is supported by the observations that the BcatrB mutant is significantly more sensitive to 2,4-DAPG than its parental strain, and is substantially less effective in 2,4-DAPG degradation. The results of this study further showed that BcLCC2 itself is not able to degrade 2,4-DAPG, but requires tannic acid as a mediator for 2,4-DAPG degradation. To our knowledge, this is the first time that the laccase-mediator system is shown to play a role in the detoxification of a broad-spectrum antibiotic compound from bacterial origin. We postulate that yet unknown constituents present in tannic acid act as substrate(s) of BcLCC2, thereby generating radicals that mediate 2,4-DAPG degradation.
24Chitin is a major structural component of fungal cell walls and acts as a microbe-25 associated molecular pattern (MAMP) that, upon recognition by a plant host, triggers the 26 activation of immune responses. In order to avoid the activation of these responses, the 27 Septoria tritici blotch (STB) pathogen of wheat, Zymoseptoria tritici, secretes LysM 28 effector proteins. Previously, the LysM effectors Mg1LysM and Mg3LysM were shown to 29 protect fungal hyphae against host chitinases. Furthermore, Mg3LysM, but not Mg1LysM, 30 was shown to suppress chitin-induced reactive oxygen species (ROS) production. 31Whereas initially a third LysM effector gene was disregarded as a presumed pseudogene, 32 we now provide functional data to show that also this gene encodes a LysM effector, 33 named Mgx1LysM, that is functional during wheat colonization. While Mg3LysM confers 34 a major contribution to Z. tritici virulence, Mgx1LysM and Mg1LysM contribute to Z. tritici 35 virulence with smaller effects. All three LysM effectors display partial functional 36 redundancy. We furthermore demonstrate that Mgx1LysM binds chitin, suppresses the 37 chitin-induced ROS burst and is able to protect fungal hyphae against chitinase hydrolysis. 38Finally, we demonstrate that Mgx1LysM is able to undergo chitin-induced polymerisation. 39Collectively, our data show that Zymoseptoria tritici utilizes three LysM effectors to 40 disarm chitin-triggered wheat immunity. et al., 2014; Takahara et al., 2016). For example, some fungi can convert the 68 surface-exposed chitin in fungal cell walls to chitosan, which is a poor substrate for 69 chitinases, thus avoiding the activation of chitin-triggered immune responses during host 70 invasion (El Gueddari et al., 2002; Ride and Barber, 1990). Furthermore, from the soil-71 borne fungus Verticillium dahliae a secreted polysaccharide deacetylase was 72 characterized to facilitate fungal virulence through direct deacetylation of chitin 73 oligomers, converting them to chitosan that is a relatively poor inducer of immune 74 responses (Gao et al., 2019). The use of effector molecules to successfully target chitin-75 triggered plant immunity has been well-studied for the tomato leaf mould fungus 76 Cladosporium fulvum. This fungus secretes the invertebrate chitin-binding domain 77 (CBM14)-containing effector protein Avr4 to bind fungal cell wall chitin, resulting in the 78 protection of its hyphae against hydrolysis by tomato chitinases (van den Burg et al., 2006; 79 van Esse et al., 2007). Additionally, C. fulvum secretes the effector protein Ecp6 80 (extracellular protein 6) that carries three LysMs, binds chitin and suppresses chitin-81 induced plant immunity. A crystal structure of Ecp6 revealed that two of its three LysM 82 domains undergo ligand-induced intramolecular dimerization, thus establishing a groove 83 with ultrahigh (pM) chitin binding-affinity that enables Ecp6 to outcompete plant 84 receptors for chitin binding (Sánchez-Vallet et al., 2013). Whereas Avr4 cannot suppress 85 chitin-t...
Selection pressure impacts genomes unevenly, as different genes adapt with differential speed to establish an organism’s optimal fitness. Plant pathogens co-evolve with their hosts, which implies continuously adaption to evade host immunity. Effectors are secreted proteins that mediate immunity evasion, but may also typically become recognized by host immune receptors. To facilitate effector repertoire alterations, in many pathogens, effector genes reside in dynamic genomic regions that are thought to display accelerated evolution, a phenomenon that is captured by the two-speed genome hypothesis. The genome of the vascular wilt pathogen Verticillium dahliae has been proposed to obey to a similar two-speed regime with dynamic, lineage-specific regions that are characterized by genomic rearrangements, increased transposable element activity and enrichment in in planta-induced effector genes. However, little is known of the origin of, and sequence diversification within, these lineage-specific regions. Based on comparative genomics among Verticillium spp. we now show differential sequence divergence between core and lineage-specific genomic regions of V. dahliae. Surprisingly, we observed that lineage-specific regions display markedly increased sequence conservation. Since single nucleotide diversity is reduced in these regions, host adaptation seems to be merely achieved through presence/absence polymorphisms. Increased sequence conservation of genomic regions important for pathogenicity is an unprecedented finding for filamentous plant pathogens and signifies the diversity of genomic dynamics in host-pathogen co-evolution.
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