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Malmgren, A.

Publications and source records attributed to Malmgren, A..

5 recordsLinked to original sources

Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages

Crop disease pandemics are often driven by clonal lineages of plant pathogens that reproduce asexually. How these clonal pathogens continuously adapt to their hosts despite harboring limited genetic variation, and in absence of sexual recombination remains elusive. Here, we reveal multiple instances of horizontal chromosome transfer within pandemic clonal lineages of the blast fungus Magnaporthe (Syn. Pyricularia) oryzae. We identified a horizontally transferred 1.2Mb supernumerary mini-chromosome which is remarkably conserved between M. oryzae isolates from both the rice blast fungus lineage and the lineage infecting Indian goosegrass (Eleusine indica), a wild grass that often grows in the proximity of cultivated cereal crops. Furthermore, we show that this mini-chromosome was horizontally acquired by clonal rice blast isolates through at least nine distinct transfer events over the past three centuries. These findings establish horizontal mini-chromosome transfer as a mechanism facilitating genetic exchange among different host-associated blast fungus lineages. We propose that blast fungus populations infecting wild grasses act as genetic reservoirs that drive genome evolution of pandemic clonal lineages that afflict cereal crops.

evolutionary biology↗

Wild grass isolates of Magnaporthe (Syn. Pyricularia) spp. from Germany can cause blast disease on cereal crops

Pathogens that cause destructive crop diseases often infect wild host plants. However, surveys of major plant pathogens tend to be skewed towards cultivated crops and often neglect the wild hosts. Here, we report an emerging disease threat generated by the blast fungus Magnaporthe (Syn. Pyricularia) spp. in central Europe. We found that this notoriously devastating plant pathogen infects the wild grasses foxtail millet (Setaria spp.) and crabgrass (Digitaria spp.) in south-western Germany, a region previously deemed unfavorable for blast disease. Using phenotypic characterization and genomic analyses, we determined that the observed disease symptoms are associated with the Setaria spp.-infecting lineage of M. oryzae and its sister species Magnaporthe grisea. We showed that M. oryzae isolates can infect barley and wheat, thus highlighting the risk of pathogen spread to crops. In addition, M. oryzae isolates which co-occur in natural populations display compatible mating types and variable candidate effector gene content, which may enhance the pathogens adaptive potential. Our findings stress the risk of blast fungus infections expanding into European cereal crops through migration and host jumps. This underlines the importance for pathogen surveillance not only on cultivated crops, but also on wild host plants. Author SummaryWild plant species are often overlooked during pathogen virulence surveys. However, many of the diseases we observe in crops are a consequence of host jumps from wild to cultivated plant species. This is reminiscent of zoonotic diseases, where host jumps from wild animals to humans result in new disease outbreaks. Here, we report that the notoriously devastating blast fungus Magnaporthe (Syn. Pyricularia) spp. occurs on wild grasses in south-western Germany. This region, which is at the center of the European cereal belt, has so far been viewed as having unfavorable climatic conditions for the blast disease. The newly identified blast fungus isolates have the capacity to infect wheat and barley cultivars, highlighting the risk of the disease spreading to staple cereal crops. In addition, there is potential for sexual recombination in local populations, which may increase the evolutionary potential of the fungus and might facilitate host jumps to cereal crops. Our findings emphasize the urgent need for surveillance of plant diseases on both wild hosts and crops.

plant biology↗

A pandemic clonal lineage of the wheat blast fungus

Wheat, the most important food crop, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America, and to guide pre-emptive wheat breeding for blast resistance.

evolutionary biology↗

SNP calling parameters have minimal impact on population structure and divergence time estimates for the rice blast fungus

ObjectivesAccurate single-nucleotide polymorphisms (SNP) calls are crucial for robust evolutionary and population genetic inferences in genomic analyses. Such inferences can reveal the time-scales and processes associated with the emergence and spread of pandemic plant pathogens, such as the rice blast fungus Magnaporthe oryzae (Syn. Pyricularia oryzae). However, the specificity and sensitivity of SNP calls depend on the filtering parameters applied to the data. Here, we used a benchmarking approach to evaluate the impact of SNP calling on different population genetic analyses of the rice blast fungus, namely genetic clustering, topology of phylogenetic reconstructions and estimation of evolutionary rates. ResultsTo benchmark SNP calling parameters, we generated a gold standard set of validated SNPs by sequencing nine M. oryzae genomes with both Illumina short-reads and Oxford Nanopore Technologies (ONT). We used the gold standard set of SNPs to identify the SNP calling parameter configuration that maximizes sensitivity and specificity. We found that the choice of parameter configurations can substantially change the number of ascertained SNPs, preferentially affecting SNPs segregating at low population frequency. However, SNP calling parameter configurations did not significantly affect the clustering of isolates in clonal lineages, the monophyly of each clonal lineage, and the estimation of evolutionary rates. We leverage the evolutionary rates obtained from each SNP calling parameter configuration to generate divergence time estimates that take into account the uncertainty associated with both the estimation of evolutionary rates and SNP calling. Our analysis indicates that M. oryzae clonal lineage expansions took place ~300 years ago.

genomics↗

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

BackgroundUnderstanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae --the causal agent of blast disease of cereals-- is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined multiple genomics datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries. ResultsThe global population of the rice blast fungus consists of a diverse set of individuals and three well-defined genetic groups. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in South East Asia followed by three independent clonal expansions that took place over the last [~]200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence/absence of candidate effector genes. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of effector presence/absence define each of the pandemic clonal lineages. ConclusionsOur analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence/absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

evolutionary biology↗