The evolution of transposon repeat-induced point mutation in the genome of Colletotrichum cereale: Reconciling sex, recombination and homoplasy in an ‘‘asexual” pathogen

Crouch, Jo Anne; Glasheen, Bernadette M.; Giunta, Michael A.; Clarke, Bruce B.; Hillman, Bradley I.

doi:10.1016/j.fgb.2007.08.004

Cited by 42 publications

(33 citation statements)

References 93 publications

(86 reference statements)

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“…The functionality of these signals was experimentally verified by transient expression in planta (Figure S2), raising the possiblity that ChEC4 and ChEC9 are translocated into the host nucleus for transcriptional reprogramming. Interestingly, ChEC7 and ChEC10 had transcripts containing remnants of retrotransposons within their UTRs, which resembled CgT1, a non-LTR LINE-like element previously identified in C. gloeosporioides [20] and Ccret2 from C. cereale [21], respectively ([22]; Table S2). Taken together, secreted proteins, including ChECs, predominate among the most highly expressed genes in appressoria during early host invasion.…”

Section: Resultsmentioning

confidence: 76%

Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

et al. 2012

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Phytopathogens secrete effector proteins to manipulate their hosts for effective colonization. Hemibiotrophic fungi must maintain host viability during initial biotrophic growth and elicit host death for subsequent necrotrophic growth. To identify effectors mediating these opposing processes, we deeply sequenced the transcriptome of Colletotrichum higginsianum infecting Arabidopsis. Most effector genes are host-induced and expressed in consecutive waves associated with pathogenic transitions, indicating distinct effector suites are deployed at each stage. Using fluorescent protein tagging and transmission electron microscopy-immunogold labelling, we found effectors localised to stage-specific compartments at the host-pathogen interface. In particular, we show effectors are focally secreted from appressorial penetration pores before host invasion, revealing new levels of functional complexity for this fungal organ. Furthermore, we demonstrate that antagonistic effectors either induce or suppress plant cell death. Based on these results we conclude that hemibiotrophy in Colletotrichum is orchestrated through the coordinated expression of antagonistic effectors supporting either cell viability or cell death.

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Section: Resultsmentioning

confidence: 76%

Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

et al. 2012

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“…In V. dahliae , mating-type idiomorphs have been identified (see above) and evidence of repeat-induced point (RIP) mutations was found in a small subset of transposable elements in [48], [49]. RIP mutations prevent further transposition of repetitive elements in fungi but they only occur during meiosis [50], [51]. To our knowledge, no analyses have been published on meiosis-specific genes in V. dahliae .…”

Section: Introductionmentioning

confidence: 99%

Recombination between Clonal Lineages of the Asexual Fungus Verticillium dahliae Detected by Genotyping by Sequencing

et al. 2014

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Most asexual species of fungi have either lost sexuality recently, or they experience recombination by cryptic sexual reproduction. Verticillium dahliae is a plant-pathogenic, ascomycete fungus with no known sexual stage, even though related genera have well-described sexual reproduction. V. dahliae reproduces mitotically and its population structure is highly clonal. However, previously described discrepancies in phylogenetic relationships among clonal lineages may be explained more parsimoniously by recombination than mutation; therefore, we looked for evidence of recombination within and between clonal lineages. Genotyping by sequencing was performed on 141 V. dahliae isolates from diverse geographic and host origins, resulting in 26,748 single-nucleotide polymorphisms (SNPs). We found a strongly clonal population structure with the same lineages as described previously by vegetative compatibility groups (VCGs) and molecular markers. We detected 443 recombination events, evenly distributed throughout the genome. Most recombination events detected were between clonal lineages, with relatively few recombinant haplotypes detected within lineages. The only three isolates with mating type MAT1-1 had recombinant SNP haplotypes; all other isolates had mating type MAT1-2. We found homologs of eight meiosis-specific genes in the V. dahliae genome, all with conserved or partially conserved protein domains. The extent of recombination and molecular signs of sex in (mating-type and meiosis-specific genes) suggest that V. dahliae clonal lineages arose by recombination, even though the current population structure is markedly clonal. Moreover, the detection of new lineages may be evidence that sexual reproduction has occurred recently and may potentially occur under some circumstances. We speculate that the current clonal population structure, despite the sexual origin of lineages, has arisen, in part, as a consequence of agriculture and selection for adaptation to agricultural cropping systems.

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“…Most studies of RIP focus on Neurospora crassa, in which it was first discovered, although other fungi, including many model systems, employ RIP-like processes. These include Aspergillus nidulans (Clutterbuck 2004), Podospora anserina (Hamann et al 2000), Magnaporthe grisea (Ikeda et al 2002), Fusarium oxysporum (Daboussi et al 2002), and Colletotrichum cereale (Crouch et al 2008). Duplicated sequences appear to interact in a pairwise manner with the RIP machinery, which induces transition mutations of cytosine residues at particular di-or trinucleotide combinations.…”

Section: Introductionmentioning

confidence: 99%

The impact of genome defense on mobile elements in Microbotryum

et al. 2009

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Repeat induced point mutation (RIP), a mechanism causing hypermutation of repetitive DNA sequences in fungi, has been described as a 'genome defense' which functions to inactivate mobile elements and inhibit their deleterious effects on genome stability. Here we address the interactions between RIP and transposable elements in the Microbotryum violaceum species complex. Ten strains of M. violaceum, most of which belong to different species of the fungus, were all found to contain intragenomic populations of copia-like retrotransposons. Intragenomic DNA sequence variation among the copia-like elements was analyzed for evidence of RIP. Among species with RIP, there was no significant correlation between the frequency of RIP-induced mutations and inferred transposition rate based on diversity. Two strains of M. violaceum, from two different plant species but belonging to the same fungal lineage, contained copia-like elements with very low diversity, as would result from a high transposition rate, and these were also unique in showing no evidence of the hypermutation patterns indicative of the RIP genome defense. In this species, evidence of RIP was also absent from a Class II helitron-like transposable element. However, unexpectedly the absolute repetitive element load was lower than in other strains.

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The evolution of transposon repeat-induced point mutation in the genome of Colletotrichum cereale: Reconciling sex, recombination and homoplasy in an ‘‘asexual” pathogen

Cited by 42 publications

References 93 publications

Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum

Recombination between Clonal Lineages of the Asexual Fungus Verticillium dahliae Detected by Genotyping by Sequencing

The impact of genome defense on mobile elements in Microbotryum

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