<i>Verticillium dahliae</i> strains that infect the same host plant display highly divergent effector catalogs

Gibriel, Hesham; Li, Jinling; Zhu, Longfu; Seidl, Michael; Thomma, B.P.H.J.

doi:10.1101/528729

Cited by 13 publications

(28 citation statements)

References 57 publications

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“…Resampling was completed using the bootstrap method with 1000 replicates. Pathogenicity on tomato confirmed in this study or in other studies using universally susceptible standard "Bonny Best" (Faino et al, 2015;Gibriel et al, 2019).…”

Section: Phylogenetic Analysissupporting

confidence: 83%

“…A study of the VdLs17 genome in 2011 showed only 127 effectors, however, the method by which they were classified as effectors was by sequence length (<400 bp) and being rich in cysteine (Klosterman et al, 2011). A more recent study of the VdLs17 (using SignalP v4.1 and EffectorP v1.0) reported 179 (Gibriel et al, 2019). In this study, additional secreted effectors were found.…”

Section: Secreted Effector Genesmentioning

confidence: 57%

“…Eight chromosome consensus sequences were concatenated from the 18 isolates from this study, as well as 8 outgroup genomes from Gibriel et al (2019) and the reference genome JR2 and were aligned using Mauve (Darling et al, 2004). Genetic distances were calculated using the Jukes-Cantor model (Jukes and Cantor, 1969).…”

Section: Phylogenetic Analysismentioning

confidence: 99%

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Comparative Genome Analyses of 18 Verticillium dahliae Tomato Isolates Reveals Phylogenetic and Race Specific Signatures

Ingram

Adhikari

et al. 2020

Front. Microbiol.

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Host resistance is one of the few strategies available to combat the soil borne pathogenic fungus Verticillium dahliae. Understanding pathogen diversity in populations is key to successfully deploying host resistance. In this study the genomes of 18 V. dahliae isolates of races 1 (n = 2), 2 (n = 4), and 3 (n = 12) from Japan, California, and North Carolina were sequenced and mapped to the reference genome of JR2 (from tomato). The genomes were analyzed for phylogenetic and pathogen specific signatures to classify specific strains or genes for future research. Four highly clonal lineages/groups were discovered, including a lineage unique to North Carolina isolates, which had the rare MAT1-1 mating type. No evidence for recombination between isolates of different mating types was observed, even in isolates of different mating types discovered in the same field. By mapping these 18 isolates genomes to the JR2 reference genome, 193 unique candidate effectors were found using SignalP and EffectorP. Within these effectors, 144 highly conserved effectors, 42 mutable effectors (truncated or present in some isolates but absent in others), and 7 effectors present in highly variable regions of the chromosomes were discovered. Of the 144 core effectors, 21 were highly conserved in V. alfalfae and V. longisporum, 7 of which have no known function. Within the non-core effectors 30 contained large numbers of non-synonymous mutations, while 15 of them contained indels, frameshift mutations, or were present on highly variable regions of the chromosome. Two of these highly variable region effectors (HVREs) were only present in race 2 isolates, but not in race 3 isolates. The race 1 effector Ave1 was also present in a highly variable region. These data may suggest that these highly variable regions are enriched in race determinant genes, consistent with the two-speed genome hypothesis.

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Section: Phylogenetic Analysissupporting

confidence: 83%

Section: Secreted Effector Genesmentioning

confidence: 57%

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Comparative Genome Analyses of 18 Verticillium dahliae Tomato Isolates Reveals Phylogenetic and Race Specific Signatures

Ingram

Adhikari

et al. 2020

Front. Microbiol.

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“…Examples comprise the wheat pathogens Zymoseptoria tritici[67] and Blumeria graminis f. sp. tritici[68], and the broad host range pathogen Verticillium dahlia[69]. Moreover, different strains can encode different alleles of the same effector gene; this was, for example, reported for the low complexity regions containing Ustilago maydis effector Rsp3[58].Several reports suggest that effector proteins containing low complexity regions can play important roles in virulence[37,70], and results presented in the present work suggest that different fungal lifestyles contribute to the evolution of low complexity regions in effector proteins.ConclusionsA comparative genomics study with 121 plant colonizing fungi representing six different lifestyles showed that protein type (cytoplasmic or secreted), protein age (ancestral proteins conserved in most species or recent species-specific proteins), and lifestyle of different fungal species contribute to the evolution of low complexity regions in effector proteins.…”

supporting

confidence: 76%

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

Schweizer¹

2020

Preprint

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Background: Interactions between plants and fungi range from mutual symbiosis to parasitism. Fungi secrete proteins (termed effectors) to establish different forms of interactions with host plants. Such proteins are thought to coevolve with their molecular plant targets, and this can favor the emergence of novel alleles of fungal effector proteins. Low complexity regions in protein sequences are abundant in eukaryotes and were shown to contribute to the formation of novel protein sequences. This suggests that low complexity regions may play a role in the evolution of effector proteins. Several effector proteins with low complexity regions were functionally characterized in plant colonizing fungi that showed diverse lifestyles and belonged to different taxonomic groups. To investigate if low complexity regions in fungal effector proteins could contribute to the evolution of different plant-fungus interaction types, I employed publicly available genomic data from 121 species of plant colonizing fungi representing six different lifestyles and three phyla. I classified proteins in each species as cytoplasmic, secreted-non effector or effector protein and predicted low complexity regions in all protein sequences.Results: I found that the fraction of proteins that contain a low complexity region differs between cytoplasmic and secreted proteins. Moreover, the fraction of a protein sequence that spans a low complexity region differed on average between cytoplasmic and secreted proteins. Inferring homologous relationships between effector proteins revealed that this fraction is higher in recent compared to ancestral proteins, suggesting that low complexity regions contribute to the formation of novel effector alleles. Furthermore, a principal component analysis and the results of a generalized linear model showed that the lifestyle of different fungi contributes to the evolution of low complexity regions. Likewise, the relative position of low complexity regions differed between cytoplasmic and secreted proteins, between ancestral and recent effector proteins, and between effectors of different lifestyles.Conclusions: Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi, but molecular and evolutionary mechanisms explaining the differences between different protein types and proteins of different lifestyles remain to be elucidated.

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“…However, based on previously performed RNA sequencing experiments, no expression of any of these candidates could be monitored during colonization of Arabidopsis thaliana, Nicotiana benthamiana or cotton plants (Extended data Fig. 6) 17,20,27,28 . Additionally, in vitro cultivation of V. dahliae in the presence of E. coli , B. subtilis or T. viride , or of peptidoglycan to mimic bacterial encounter, did not lead to induction of any of the effector candidate genes (Extended data Fig.…”

Section: Introductionmentioning

confidence: 99%

A plant pathogen utilizes effector proteins for microbiome manipulation

Snelders

Rövenich

Petti

et al. 2020

Preprint

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During colonization of their hosts, pathogens secrete effector proteins to promote disease development through various mechanisms. Increasing evidence shows that the host microbiome plays a crucial role in health, and that hosts actively shape their microbiomes to suppress disease. We hypothesized that pathogens evolved to manipulate host microbiomes to their advantage in turn. Here, we show that the fungal plant pathogen Verticillium dahliae utilizes effector proteins for niche colonization through selective manipulation of host microbiomes by suppressing microbes with antagonistic activities. Moreover, we show that effector proteins are similarly exploited for microbiome manipulation in the soil environment, where the fungus resides in absence of a host. In conclusion, we demonstrate that pathogens utilize effector proteins to modulate microbiome compositions and propose that their effector catalogs represent an untapped resource for novel antibiotics.

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Verticillium dahliae strains that infect the same host plant display highly divergent effector catalogs

Cited by 13 publications

References 57 publications

Comparative Genome Analyses of 18 Verticillium dahliae Tomato Isolates Reveals Phylogenetic and Race Specific Signatures

Comparative Genome Analyses of 18 Verticillium dahliae Tomato Isolates Reveals Phylogenetic and Race Specific Signatures

Protein type and lifestyle contribute to the evolution of low complexity regions in proteins of plant colonizing fungi

A plant pathogen utilizes effector proteins for microbiome manipulation

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