Means, motive and opportunity for biological invasions: Genetic introgression in a fungal pathogen

Abstract

Invasions by fungal plant pathogens pose a significant threat to the health of agriculture ecosystems. Despite limited standing genetic variation, many invasive fungal species can adapt and spread rapidly, resulting in significant losses in crop yields. Here, we report on the population genomics of Colletotrichum truncatum, a polyphagous pathogen that can infect more than 460 plant species, and an invasive pathogen on soybean in Brazil. We study the whole-genome sequences of 18 isolates representing 10 fields from two major regions of soybean production. We show that Brazilian C. truncatum is subdivided into three phylogenetically distinct lineages that exchange genetic variation through hybridization. Introgression affects 2 to 30% of the nucleotides of genomes and varies widely between the lineages. We find that introgressed regions comprise secreted protein-encoding genes, suggesting possible co-evolutionary targets for selection in those regions. We highlight the inherent vulnerability of genetically uniform crops in the agroecological environment, particularly when faced with pathogens that can take full advantage of the opportunities offered by an increasingly globalized world. Finally, we discuss "The Means, Motive, and Opportunity" of fungal pathogens and how they can become invasive species of crops. We call for more population genomic studies because such analyses can help identify geographic areas and pathogens that pose a risk, thereby helping to inform control strategies to better protect crops in the future.

Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose

“…These results corroborate a previous study that found evidence of recombination using the PHI test at the chromosome level [92]. Similar findings of low and fast LDecay are reported in other fungal plant pathogens which suggests the occurrence of genetic mechanisms responsible for creating such patterns in genomes [82,133,134]. In addition, the signature of repeat-induced point mutation (RIP), a genome defense mechanism that occurs during sexual reproduction, [135, 136] was detected in C. graminicola genomes [137, 138].…”

“…Genetic recombination is reported as an important factor in the ecology and evolution of many Colletotrichum species [82–87]. However, only a few population studies have characterized the genetic diversity of grass-infecting Colletotrichum species, such as C. sublineola and , C. cereale [85–89], and little is known about C. graminicola population diversity.…”

Population Genomics Provide Insights into the Global Genetic Structure of Colletotrichum graminicola , the Causal Agent of Maize Anthracnose

“…These results corroborate a previous study that found evidence of recombination using the PHI test at the chromosome level ( 97 ). Similar findings of low and fast LD decay have been reported in other fungal plant pathogens (i.e., half its maximum value over a distance of 10 kb or less), suggesting the occurrence of genetic mechanisms responsible for creating such patterns in genomes ( 78 , 98 , 99 ). In addition, the signature of repeat-induced point mutation (RIP), a genome defense mechanism which occurs during sexual reproduction ( 100 , 101 ), was detected in C. graminicola genomes ( 102 , 103 ).…”

“…S4 for details), although the teleomorph has not yet been found in field conditions. Although the absence of the sexual state in nature could lead to less recombination, population genetic studies have shown that several Colletotrichum species known to be exclusively asexual exhibit evidence of genetic recombination ( 78 , 79 , 110 ). Some studies have described alternative mechanisms, such as the parasexual cycle, as being responsible for creating genetic recombination in Colletotrichum species ( 75 , 80 , 111 – 113 ).…”

“…Genetic recombination is reported to be an important factor in the ecology and evolution of many Colletotrichum species ( 78 – 83 ). However, only a few population studies have characterized the genetic diversity of grass-infecting Colletotrichum species, such as C. sublineola and C. cereale ( 81 – 85 ), and little is known about C. graminicola population diversity.…”