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: 10.74). 02/2011; 2:202. DOI: 10.1038/ncomms1189
Source: PubMed

ABSTRACT 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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Available from: Brett Tyler, Aug 23, 2015
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    • "For example in the Leptosphaeria complex, one species associated with oilseed rape has experienced a recent and massive burst of movement by a few TE families. The alterations caused by these TEs took place in discrete regions of the genome leading to shuffling of the genomic landscape and the appearance of genes specific to the species, such as effectors useful for the interactions with a particular plant (Rouxel et al., 2011). Other presentations showed the importance of TEs in affecting genome organization. "
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    • "In many fungal pathogens, infection-related genes cluster into " pathogenicity islands " that can sweep rapidly through populations (Kä mper et al. 2006; Fedorova et al. 2008; Stergiopoulus and de Wit, 2009; Rouxel et al. 2011). We hypothesized that Z. tritici genes regulated during infection could likewise be distributed nonrandomly in the genome. "
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    ABSTRACT: Host specialization by pathogens requires a repertoire of virulence factors as well as fine-tuned regulation of gene expression. The fungal wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola) is a powerful model system for the discovery of genetic elements that underlie virulence and host specialization. We transcriptionally profiled the early stages of Z. tritici infection of a compatible host (wheat) and a noncompatible host (Brachypodium distachyon). The results revealed infection regulatory programs common to both hosts and genes with striking wheat-specific expression, with many of the latter showing sequence signatures of positive selection along the Z. tritici lineage. Genes specifically regulated during infection of wheat populated two large clusters of coregulated genes that may represent candidate pathogenicity islands. On evolutionarily labile, repeat-rich accessory chromosomes (ACs), we identified hundreds of highly expressed genes with signatures of evolutionary constraint and putative biological function. Phylogenetic analyses suggested that gene duplication events on these ACs were rare and largely preceded the diversification of Zymoseptoria species. Together, our data highlight the likely relevance for fungal growth and virulence of hundreds of Z. tritici genes, deepening the annotation and functional inference of the genes of this model pathogen.
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    • "In L. maculans, for example, the characteristics of the effector genes strongly suggest that they were subjected to RIP as a result of their genome location (Rouxel et al., 2011). The consequent rapid sequence diversification contributes either to a loss of function due to deleterious effect of RIP or to an accelerated pace of mutation, eventually resulting in neofunctionalization and generation of novel effectors with novel specificities (Rouxel et al., 2011). Although frequently postulated, only in a few cases were TEs demonstrated to have favoured LGT. "
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    ABSTRACT: In complex eukaryotes, transposable elements (TEs), previously considered as junk DNA, are more and more acknowledged as genome shapers and as a source of gene innovation, genome plasticity and genome divergence. Fungi are simple and easy-to-manipulate eukaryotic organisms, for which ever-increasing genome information indicates that many plant-associated fungi have a tendency to have expanded genomes. This increase in genome size is mostly driven by TE expansion that eventually shapes adaptive regions of the genome. Such genome regions harbour genes involved in niche adaptation and favour accelerated evolution of these genes. The recent rise of comparative genomics in fungi now allows the use of phylogeny to date TE invasion and proliferation in genomes. This in turn provides inferences about the impact of TEs on speciation and on the rise of better-adapted species. Here, focusing on plant-associated fungi, we review our current level of knowledge on how TEs may have contributed to speciation, the rise of two-speed genomes and the shaping of specific genome environments. Moreover, we consider the role of TEs in gene duplication and diversification that contribute to both adaptation to new hosts and adaptation to host resistance genes in gene-for-gene systems.
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