Subtelomeric regions and a repeat-rich chromosome harbor multicopy effector gene clusters with variable conservation in multiple plant pathogenic<i>Colletotrichum</i>species

P, Gan; Hiroyama, Ryoko; Tsushima, Ayako; Masuda, Sachiko; Shibata, Arisa; Ueno, Akihiko; Kumakura, Naoyoshi; Narusaka, Mari; Tx, Hoat; Narusaka, Yoshihiro; Takano, Yoshitaka; Shirasu, Ken

doi:10.1101/2020.04.28.061093

Cited by 7 publications

(8 citation statements)

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“…In many filamentous pathogens, effector genes are enriched in TE-rich and gene-sparse compartments, while they are typically underrepresented in TE-poor and gene-dense genomic regions that typically harbor housekeeping genes (Seidl and Thomma 2014;Dong, et al 2015;Frantzeskakis, et al 2020). TE-rich compartments are often characterized by increased substitution rates and increased occurrence of SVs and presence/absence polymorphisms (Raffaele, et al 2010;Croll and McDonald 2012;de Jonge, et al 2012;de Jonge, et al 2013;Dutheil, et al 2016;Fokkens, et al 2018;Gan, et al 2020;Wyka, et al 2020). Notably, a similar association of TEs with genes involved in immune responses has also been observed in plant hosts (Leister 2004;Kawakatsu, et al 2016;Mascher, et al 2017;Seidl and Thomma 2017).…”

Section: Introductionmentioning

confidence: 99%

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Torres

Thomma

Seidl

2021

Preprint

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Transposable elements (TEs) are a major source of genetic and regulatory variation in their host genome and are consequently thought to play important roles in evolution. Many fungal and oomycete plant pathogens have evolved dynamic and TE-rich genomic regions containing genes that are implicated in host colonization. TEs embedded in these regions have typically been thought to accelerate the evolution of these genomic compartments, but little is known about their dynamics in strains that harbor them. Here, we used whole-genome sequencing data of 42 strains of the fungal plant pathogen Verticillium dahliae to systematically identify polymorphic TEs that may be implicated in genomic as well as in gene expression variation. We identified 2,523 TE polymorphisms and characterize a subset of 8% of the TEs as dynamic elements that are evolutionary younger, less methylated, and more highly expressed when compared with the remaining 92% of the TE complement. As expected, the dynamic TEs are enriched in the dynamic genomic regions. Besides, we observed an association of dynamic TEs with pathogenicity-related genes that localize nearby and that display high expression levels. Collectively, our analyses demonstrate that TE dynamics in V. dahliae contributes to genomic variation, correlates with expression of pathogenicity-related genes, and potentially impacts the evolution of dynamic genomic regions.Significance statementTransposable elements (TEs) are ubiquitous components of genomes and are major sources of genetic and regulatory variation. Many plant pathogens have evolved TE-rich genomic regions containing genes with roles in host colonization, and TEs are thought to contribute to accelerated evolution of these dynamic regions. We analyzed the fungal plant pathogen Verticillium dahliae to identify TE variation between strains and to demonstrate that polymorphic TEs have specific characteristic that separates them from the majority of TEs. Polymorphic TEs are enriched in dynamic genomic regions and are associated with structural variants and highly expressed pathogenicity-related genes. Collectively, our results provide evidence for the hypothesis that dynamic TEs contribute to increased genomic diversity, functional variation, and the evolution of dynamic genomic regions.

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Section: Introductionmentioning

confidence: 99%

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Torres

Thomma

Seidl

2021

Preprint

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“…Total RNA was extracted from C. higginsianum MAFF 305635, C. orbiculare MAFF 240422, and C. graminicola MAFF 244463 cultured in potato dextrose (PD) broth (BD Biosciences) at 24°C in the dark for two days. Total RNA was extracted from strawberry (Sachinoka) leaves three days after inoculation with C. fructicola Nara gc5 (JCM 39093) as previously described (Gan et al, 2020). RNA was extracted using RNeasy Plant Mini Kit (Qiagen) with DNase I treatment according to the manufacturer’s introductions, and reverse transcribed using ReverTraAce qPCR RT Kit (Toyobo, Co., Ltd.) or SuperScript III Reverse Transcriptase (Thermo Fisher Scientific).…”

Section: Methodsmentioning

confidence: 99%

“…To date, more than 100 genomes of Colletotrichum spp. have been sequenced due to their agricultural importance and scientific interest (O’Connell et al, 2012; Baroncelli et al, 2014, 2016a; Gan et al, 2016, 2019, 2020; Hacquard et al, 2016). Using these abundant genome resources, it is now feasible to conduct comparative genomic analysis and reverse genetics of Colletotrichum spp.…”

Section: Introductionmentioning

confidence: 99%

The ConservedColletotrichumspp. Effector CEC3 Induces Nuclear Expansion and Cell Death in Plants

Tsushima

Narusaka²,

Gan

et al. 2021

Preprint

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Plant pathogens secrete small proteins, known as effectors, that promote infection by manipulating host cells. Members of the phytopathogenic fungal genus Colletotrichum collectively have a broad host range and generally adopt a hemibiotrophic lifestyle that includes an initial biotrophic phase and a later necrotrophic phase. We hypothesized that Colletotrichum fungi use a set of conserved effectors during infection to support the two phases of their hemibiotrophic lifestyle. This study aimed to examine this hypothesis by identifying and characterizing conserved effectors among Colletotrichum fungi. Comparative genomic analyses using genomes of ascomycete fungi with different lifestyles identified seven effector candidates that are conserved across the genus Colletotrichum. Transient expression assays showed that one of these conserved effectors, CEC3, induces nuclear expansion and cell death in Nicotiana benthamiana, suggesting that CEC3 is involved in promoting host cell death during infection. Nuclear expansion and cell death induction were commonly observed in CEC3 homologs from four different Colletotrichum species that vary in host specificity. Thus, CEC3 proteins could represent a novel class of core effectors with functional conservation in the genus Colletotrichum.

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“…Repeat element prediction was performed using the genome sequences of eight F. oxysporum strains in the NCBI database that had contig N50 values greater than 1 Mb (last accessed on November 24, 2019) as described in Gan et al 57 . Code used for this analysis are available at: https://github.com/pamgan/colletotrichum_genome.…”

Section: Analysis Of Repeat Elementsmentioning

confidence: 99%

A pair of effectors encoded on a conditionally dispensable chromosome ofFusarium oxysporumsuppress host-specific immunity

Ayukawa

Asai

Gan

et al. 2020

Preprint

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Many plant pathogenic fungi contain conditionally dispensable (CD) chromosomes that are associated with virulence, but not growth in vitro. Virulence-associated CD chromosomes carry genes encoding effectors and/or host-specific toxin biosynthesis enzymes that may contribute significantly to determining host specificity. Fusarium oxysporum causes devastating diseases of more than 100 plant species. Among a large number of host-specific forms, F. oxysporum f. sp. conglutinans (Focn) can infect Brassicaceae plants including Arabidopsis and cabbage. Here we show that Focn has multiple CD chromosomes involved in virulence but also in vegetative growth, which is an atypical feature of CD chromosomes. We identified specific CD chromosomes that are required for virulence on Arabidopsis, cabbage, or both, and describe a pair of effectors encoded on one of the CD chromosomes that is required for suppression of Arabidopsis-specific phytoalexin-based immunity. The effector pair is highly conserved in F. oxysporum isolates capable of infecting Arabidopsis, but not of other plants. This study provides insight into how host specificity of F. oxysporum may be determined by a pair of effector genes on a transmissible CD chromosome.

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Subtelomeric regions and a repeat-rich chromosome harbor multicopy effector gene clusters with variable conservation in multiple plant pathogenicColletotrichumspecies

Abstract: 15

Cited by 7 publications

References 58 publications

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

The ConservedColletotrichumspp. Effector CEC3 Induces Nuclear Expansion and Cell Death in Plants

A pair of effectors encoded on a conditionally dispensable chromosome ofFusarium oxysporumsuppress host-specific immunity

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