Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun

INRA-Bioger, UR1290, Avenue Lucien Brétignières, BP 01, Thiverval-Grignon F-78850, France.
Nature Communications (Impact Factor: 11.47). 02/2011; 2(1):202. DOI: 10.1038/ncomms1189
Source: PubMed


Fungi are of primary ecological, biotechnological and economic importance. Many fundamental biological processes that are shared by animals and fungi are studied in fungi due to their experimental tractability. Many fungi are pathogens or mutualists and are model systems to analyse effector genes and their mechanisms of diversification. In this study, we report the genome sequence of the phytopathogenic ascomycete Leptosphaeria maculans and characterize its repertoire of protein effectors. The L. maculans genome has an unusual bipartite structure with alternating distinct guanine and cytosine-equilibrated and adenine and thymine (AT)-rich blocks of homogenous nucleotide composition. The AT-rich blocks comprise one-third of the genome and contain effector genes and families of transposable elements, both of which are affected by repeat-induced point mutation, a fungal-specific genome defence mechanism. This genomic environment for effectors promotes rapid sequence diversification and underpins the evolutionary potential of the fungus to adapt rapidly to novel host-derived constraints.

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    • "Plant pathogens show differing patterns of expansions and contractions in the gene families involved in pathogenicity, including effectors and PCWDEs (Raffaele & Kamoun, 2012). Although the direct impact of TEs on these genomes is only discussed in a few cases, their effects are striking and include accelerated evolutionary rates of effectors caused by repeat-induced point mutation of nearby TEs (Grandaubert et al., 2014; Rouxel et al., 2011) and a fusion of an effector family with a TE resulting in joint proliferation (Sacristán et al., 2009). Moreover, simulations suggest rearrangements mediated by TEs may contribute towards the compartmentalization of genomes into slower-and faster-evolving regions and so aid the generation of genomic plasticity underpinning adaptation to new environments (Crombach & Hogeweg, 2007). "
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    ABSTRACT: Genome architectures are likely shaped by species’ ecologies, but genomes are rarely discussed in ecological contexts. A major force in evolution is symbiosis, and a symbiotic niche may shape a genome’s size, gene order and gene content. The mycorrhizal symbiosis is ubiquitous and critical to the function of diverse ecosystems. Although there are tens of thousands of mycorrhizal fungi, there are no general principles defining the genetic architectures of these fungi. General principles may not exist, perhaps because of the multiple, independent origins of the symbiosis. But research with pathogenic fungi suggests general principles at work in the evolution of pathogen genomes, and to enable a more holistic understanding of the forces shaping genomes of mutualists we focus on the genus Amanita and the role of ecology in genome evolution. Amanita is an emerging model for the ecology and evolution of symbiosis, and to date our laboratory has sequenced the genomes of six species with diverse niches. We describe the natural histories of these species and current research on genomics. We offer novel analyses targeting two questions: did the evolution of the ectomycorrhizal symbiosis facilitate an adaptive radiation of symbiotic Amanita, and how are the genomes of asymbiotic fungi different from the derived genomes of ectomycorrhizal fungi? We also discuss the role transposable elements may have had in generating genomic variation, and a potential link between transposable element proliferation and patterns of speciation. Our descriptions of the genus identify as yet unexplored questions connecting genomics to the ecology of species’ ranges, and range expansions.
    Full-text · Chapter · Dec 2014
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    • "More recently, the genome of this dothideomycete fungus was sequenced and the annotations of fungal avirulence genes have been released publicly (Rouxel et al. 2011). "
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    ABSTRACT: A combination of staining, light microscopy and SYBR green- and dual-labelled fluorescent probe-based qPCR chemistries with species- and gene-specific primers was employed to evaluate fluctuations in the aerial biomass of Leptosphaeria maculans spores captured by volumetric spore trappings in Poznan, Poland (2006, 2008) and Harpenden, UK (2002, 2006). Arising from these surveys, DNA samples extracted from Burkard spore-trap tapes were screened for fluctuation patterns in the frequencies of AvrLm1 and AvrLm6, the most prominent of the 15 genes that code for avirulence effectors in this Dothideomycete cause of the destructive phoma stem canker disease of oilseed rape worldwide. In Poznan, very low frequencies of AvrLm1 allele were found in the autumn of both 2006 and 2008, reflecting significantly increased cultivation of rape seed with Rlm1-based resistance. In contrast, at least six folds-higher frequencies of AvrLm6, which were also confirmed by end-point PCR bioassays on phoma-infected leaves from the same region of Poland, were obtained during both years. In the UK, however, relatively higher AvrLm1 allele titres were found in L. maculans spores captured in air samples from the autumn of 2002 on the experimental fields of Rothamsted Research, Harpenden, that were historically sown to genetically heterogeneous B. napus cultivars. In the 2006 screen these levels had plummeted, to a 1:4 ratio, in favour of frequencies of the AvrLm6 allele. Patterns of fluctuations in erg11 (CYP51) fragments coding for sterol 14α-demethylase suggest October as the month with the most viable wind-dispersed L. maculans propagules of each season of the screens.
    Full-text · Article · Aug 2014 · Journal of applied genetics
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    • "Reference genomes were Lmb isolate v23.1.3 [2], Lbc isolate J154 (Grandaubert et al., submitted), and a Brassica exon array curated unigene set representing 135,201 gene models from B. napus, B. rapa and B. oleracea [27]. Aligned reads were quantified using Cufflinks v1.0.3 transcript assembly and quantification software and denoted as average expression levels (FPKM - fragments per kilobase of exon per million mapped reads) [28]. "
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    ABSTRACT: Leptosphaeria maculans ‘brassicae’ is a damaging fungal pathogen of canola (Brassica napus), causing lesions on cotyledons and leaves, and cankers on the lower stem. A related species, L. biglobosa ‘canadensis’, colonises cotyledons but causes few stem cankers. We describe the complement of genes encoding carbohydrate-active enzymes (CAZys) and peptidases of these fungi, as well as of four related plant pathogens. We also report dual-organism RNA-seq transcriptomes of these two Leptosphaeria species and B. napus during disease. During the first seven days of infection L. biglobosa ‘canadensis’, a necrotroph, expressed more cell wall degrading genes than L. maculans ‘brassicae’, a hemi-biotroph. L. maculans ‘brassicae’ expressed many genes in the Carbohydrate Binding Module class of CAZy, particularly CBM50 genes, with potential roles in the evasion of basal innate immunity in the host plant. At this time, three avirulence genes were amongst the top 20 most highly upregulated L. maculans ‘brassicae’ genes in planta. The two fungi had a similar number of peptidase genes, and trypsin was transcribed at high levels by both fungi early in infection. L. biglobosa ‘canadensis’ infection activated the jasmonic acid and salicylic acid defence pathways in B. napus, consistent with defence against necrotrophs. L. maculans ‘brassicae’ triggered a high level of expression of isochorismate synthase 1, a reporter for salicylic acid signalling. L. biglobosa ‘canadensis’ infection triggered coordinated shutdown of photosynthesis genes, and a concomitant increase in transcription of cell wall remodelling genes of the host plant. Expression of particular classes of CAZy genes and the triggering of host defence and particular metabolic pathways are consistent with the necrotrophic lifestyle of L. biglobosa ‘canadensis’, and the hemibiotrophic life style of L. maculans ‘brassicae’.
    Full-text · Article · Jul 2014 · PLoS ONE
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