Genetic structure of the poplar rust fungus Melampsora larici-populina: Evidence for isolation by distance in Europe and recent founder effects overseas

INRA, Université Bordeaux I, UMR1202 BioGeCo, F-33883 Villenave d’Ornon, France
Infection Genetics and Evolution (Impact Factor: 3.02). 04/2008; 8(5):577-587. DOI: 10.1016/j.meegid.2008.04.005
Source: PubMed

ABSTRACT Dispersal has a great impact on the genetic structure of populations, but remains difficult to estimate by direct measures. In particular, gradual and stochastic dispersal are often difficult to assess and to distinguish, although they have different evolutionary consequences. Plant pathogens, especially rust fungi, are suspected to display both dispersal modes, though on different spatial scales. In this study, we inferred dispersal capacities of the poplar rust fungus Melampsora larici-populina by examining the genetic diversity and structure of 13 populations from eight European and two overseas countries in the Northern hemisphere. M. larici-populina was sampled from both cultivated hybrid poplars and on the wild host, Populus nigra. The populations were analyzed with 11 microsatellite and 8 virulence markers. Although isolates displayed different virulence profiles according to the host plant, neutral markers revealed little population differentiation with respect to the type of host. This suggests an absence of reproductive isolation between populations sampled from cultivated and wild poplars. Conversely, studying the relationship between geographic and genetic structure allowed us to distinguish between isolation by distance (IBD) patterns and long distance dispersal (LDD) events. The European populations exhibited a significant IBD pattern, suggesting a regular and gradual dispersal of the pathogen over this spatial scale. Nonetheless, the genetic differentiation between these populations was low, suggesting an important gene flow on a continental scale. The two overseas populations from Iceland and Canada were shown to result from rare LDD events, and exhibited signatures of strong founder effects. Furthermore, the high genetic differentiation between both populations suggested that these two recent introductions were independent. This study illustrated how the proper use of population genetics methods can enable contrasted dispersal modes to be revealed.

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Available from: Pascal Frey, Sep 27, 2015
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    • "F ST versus Q ST comparisons have suggested that this pattern is indeed an adaptation, rather than merely the consequence of genetic drift (Ali et al. 2010). There may initially be several proximal causes for a loss of sexual reproduction: (i) a lack of appropriate mates where asexual propagation is possible, as in the case of Phytophthora infestans, P. cinnamomi, P. ramorum and O. novo-ulmi, for which a single mating type was present for long periods in introduced ranges (Goodwin et al. 1994; Brasier 2001; Dobrowolski et al. 2003; Hardham 2005); (ii) a hybridization event, for example, in the human pathogen Cryptococcus neoformans (Lin et al. 2007); and (iii) a lack of the alternate host on which sex occurs in the case of complex life cycles, for example, in the rusts Puccinia striiformis f. sp.tritici and Melampsora larici-populina (Mboup et al. 2007, 2009; Barr es et al. 2008). There may also be diverse evolutionary causes for the selection against sexual reproduction (Bazin et al. 2014 "
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    ABSTRACT: Fungal invasions are increasingly recognized as a significant component of global changes, threatening ecosystem health and damaging food production. Invasive fungi also provide excellent models to evaluate the generality of results based on other eukaryotes. We first consider here the reasons why fungal invasions have long been overlooked: they tend to be inconspicuous and inappropriate methods have been used for species recognition. We then review the information available on the patterns and mechanisms of fungal invasions. We examine the biological features underlying invasion success of certain fungal species. We review population structure analyses, revealing native source populations and strengths of bottlenecks. We highlight the documented ecological and evolutionary changes in invaded regions, including adaptation to temperature, increased virulence, hybridization, shifts to clonality and association with novel hosts. We discuss how the huge census size of most fungi allows adaptation even in bottlenecked, clonal invaders. We also present new analyses of the invasion of the anther smut pathogen on white campion in North America, as a case study illustrating how an accurate knowledge of species limits and phylogeography of fungal populations can be used to decipher the origin of invasions. This case study shows that successful invasions can occur even when life-history traits are particularly unfavorable to long-distance dispersal and even with a strong bottleneck. We conclude that fungal invasions are valuable models to contribute to our view of biological invasions, in particular by providing insights into the traits as well as ecological and evolutionary processes allowing successful introductions. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Molecular Ecology 12/2014; 24(9). DOI:10.1111/mec.13028 · 6.49 Impact Factor
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    • "The second verification was performed on the urediniospores after multiplication on poplar leaves, in order to detect any contamination from a nonrelated rust isolate. DNA was extracted from infected poplar leaf discs and from urediniospores using the BioSprint 96 DNA plant kit used in combination with the BioSprint automated workstation (Qiagen), as previously described (Barrès et al., 2008). Microsatellite loci amplification and fragment analysis were performed as previously described (Xhaard et al., 2011). "
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    ABSTRACT: The poplar rust fungus Melampsora larici-populina causes significant yield reduction and severe economic losses in commercial poplar plantations. After several decades of breeding for qualitative resistance and subsequent breakdown of the released resistance genes, breeders now focus on quantitative resistance, perceived to be more durable. But quantitative resistance also can be challenged by an increase of aggressiveness in the pathogen. Thus it is of primary importance to better understand the genetic architecture of aggressiveness traits. To this aim, our goal is to build a genetic linkage map for M. larici-populina in order to map quantitative trait loci related to aggressiveness. First, a large progeny of M. larici-populina was generated through selfing of the reference strain 98AG31 (which genome sequence is available) on larch plants, the alternate host of the poplar rust fungus. The progeny’s meiotic origin was validated through a segregation analysis of 115 offspring with 14 polymorphic microsatellite markers, of which 12 segregated in the expected 1:2:1 Mendelian ratio. A microsatellite-based linkage disequilibrium analysis allowed us to identify one potential linkage group comprising two scaffolds. The whole genome of a subset of 47 offspring was resequenced using the Illumina HiSeq 2000 technology at a mean sequencing depth of 6X. The reads were mapped onto the reference genome of the parental strain and 144,566 SNPs were identified across the genome. Analysis of distribution and polymorphism of the SNPs along the genome led to the identification of 2580 recombination blocks. A second linkage disequilibrium analysis, using the recombination blocks as markers, allowed us to group 81 scaffolds into 23 potential linkage groups. These preliminary results showed that a high-density linkage map could be constructed by using high-quality SNPs based on low-coverage resequencing of a larger number of M. larici-populina offspring.
    Frontiers in Plant Science 09/2014; 5:454. DOI:10.3389/fpls.2014.00454 · 3.95 Impact Factor
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    • "In view of results presented here and those of Barrès et al. (2008) "
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    ABSTRACT: The basidiomycete Melampsora larici-populina causes foliar rust on Populus species from the sections Aigeiros and Tacamahaca, causing reduction in biomass production and economic losses. In the present study, samples of Icelandic M. larici-populina were collected for analysis of genetic diversity and population structure. A total of 439 isolates, collected at 15 locations, and analysed using 22 microsatellite markers were compared to data from French M. larici-populina populations. Twenty-one of the loci analysed were polymorphic, with an average of 3.4 alleles per locus. The mean observed and expected heterozygosities for all populations were 0.35 and 0.38. Evidence was found for a substructure within the Icelandic population with three subpopulations being the most likely scenario with low levels of gene flow. The population structure seen here is most likely shaped by both isolation and genetic drift as well as repeated events of colonization. In the future it can therefore be expected that regional poplar rust genotypes in Iceland change by two different modes; on one hand by transport of spores within the country and on the other hand by repeated colonization events. The results reported here underline the importance of closely monitoring the development of fungal diseases in Iceland, and to carefully select for resistance in Icelandic plant breeding programs.
    European Journal of Plant Pathology 07/2014; 139(3):597–608. DOI:10.1007/s10658-014-0416-7 · 1.49 Impact Factor
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