Genomic rearrangements generate hypervariable mini-chromosomes in host-specific isolates of the blast fungus

Langner, Thorsten; Harant, Adeline; Gómez-Luciano, Luis B.; Shrestha, Ram-Krishna; Malmgren, Angus; Latorre, Sergio M.; Burbano, Hernán A.; Win, Joe; Kamoun, Sophien

doi:10.1371/journal.pgen.1009386

Cited by 65 publications

(74 citation statements)

References 89 publications

(153 reference statements)

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“…Model M3 and M8 passed the chi-square test at a significance level of 1% ( S2 Table ). Ancestral state reconstruction was performed by a codon based maximum likelihood analysis with codeml (included in the PAML v4.9 package) according to [ 53 , 54 ].…”

Section: Methodsmentioning

confidence: 99%

A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum

et al. 2021

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Accelerated gene evolution is a hallmark of pathogen adaptation and specialization following host-jumps. However, the molecular processes associated with adaptive evolution between host-specific lineages of a multihost plant pathogen remain poorly understood. In the blast fungus Magnaporthe oryzae (Syn. Pyricularia oryzae), host specialization on different grass hosts is generally associated with dynamic patterns of gain and loss of virulence effector genes that tend to define the distinct genetic lineages of this pathogen. Here, we unravelled the biochemical and structural basis of adaptive evolution of APikL2, an exceptionally conserved paralog of the well-studied rice-lineage specific effector AVR-Pik. Whereas AVR-Pik and other members of the six-gene AVR-Pik family show specific patterns of presence/absence polymorphisms between grass-specific lineages of M. oryzae, APikL2 stands out by being ubiquitously present in all blast fungus lineages from 13 different host species. Using biochemical, biophysical and structural biology methods, we show that a single aspartate to asparagine polymorphism expands the binding spectrum of APikL2 to host proteins of the heavy-metal associated (HMA) domain family. This mutation maps to one of the APikL2-HMA binding interfaces and contributes to an altered hydrogen-bonding network. By combining phylogenetic ancestral reconstruction with an analysis of the structural consequences of allelic diversification, we revealed a common mechanism of effector specialization in the AVR-Pik/APikL2 family that involves two major HMA-binding interfaces. Together, our findings provide a detailed molecular evolution and structural biology framework for diversification and adaptation of a fungal pathogen effector family following host-jumps.

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Section: Methodsmentioning

confidence: 99%

A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum

et al. 2021

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“…These SVs may lead to the formation of accessory* regions, or even chromosomes. A study of SVs in four strains of the blast fungus Magnaporthe oryzae showed that accessory chromosomes probably emerged from interchromosomal translocations between core* and accessory* chromosomes and segmental duplications* of core* chromosomes (Langner et al ., 2021). These accessory* regions or chromosomes often are enriched in TEs, rapidly evolving genes, such as effector* genes, and various types of SVs relative to other regions of the genome.…”

Section: The Shaping Of Fungal Plant Pathogen Genomes By Structural V...mentioning

confidence: 99%

Using structural variants to understand the ecological and evolutionary dynamics of fungal plant pathogens

Hartmann

2021

New Phytologist

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Summary Deletions, duplications, insertions, inversions and translocations are commonly referred to as structural variants (SVs). Fungal plant pathogens have compact genomes, facilitating the generation of accurate maps of SVs for these species in recent studies. Structural variants have been found to constitute a significant proportion of the standing genetic variation in fungal plant pathogen populations, potentially leading to the generation of accessory genes, regions or chromosomes enriched in pathogenicity factors. Structural variants are involved in the rapid adaptation and ecological traits of pathogens, including host specialization and mating. Long‐read sequencing techniques coupled with theoretical and experimental approaches have considerable potential for elucidating the phenotypic effects of SVs and deciphering the evolutionary and genomic mechanisms underlying the formation of SVs in fungal plant pathogens.

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“…More complex events, known as chromoanagenesis, combine a cascade of chromosomal rearrangements 1 . Over the past few years, structural variants and complex genomic rearrangements have been implicated in various phenotypes: cancer 2 , 3 , rare disorders 4 – 9 and common diseases 10 in humans, reproduction traits in pigs 11 , virulence traits in plant pathogenic fungi 12 , local adaptation in maize 13 , and behavior in Caenorhabditis elegans ( C. elegans ) 14 . However, the technologies and methods used to identify SVs and complex rearrangements are still multifaceted and no approach has yet been recognized as standard.…”

Section: Introductionmentioning

confidence: 99%

Deciphering complex genome rearrangements in C. elegans using short-read whole genome sequencing

Maroilley

Oldach

et al. 2021

Sci Rep

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Genomic rearrangements cause congenital disorders, cancer, and complex diseases in human. Yet, they are still understudied in rare diseases because their detection is challenging, despite the advent of whole genome sequencing (WGS) technologies. Short-read (srWGS) and long-read WGS approaches are regularly compared, and the latter is commonly recommended in studies focusing on genomic rearrangements. However, srWGS is currently the most economical, accurate, and widely supported technology. In Caenorhabditis elegans (C. elegans), such variants, induced by various mutagenesis processes, have been used for decades to balance large genomic regions by preventing chromosomal crossover events and allowing the maintenance of lethal mutations. Interestingly, those chromosomal rearrangements have rarely been characterized on a molecular level. To evaluate the ability of srWGS to detect various types of complex genomic rearrangements, we sequenced three balancer strains using short-read Illumina technology. As we experimentally validated the breakpoints uncovered by srWGS, we showed that, by combining several types of analyses, srWGS enables the detection of a reciprocal translocation (eT1), a free duplication (sDp3), a large deletion (sC4), and chromoanagenesis events. Thus, applying srWGS to decipher real complex genomic rearrangements in model organisms may help designing efficient bioinformatics pipelines with systematic detection of complex rearrangements in human genomes.

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Genomic rearrangements generate hypervariable mini-chromosomes in host-specific isolates of the blast fungus

Cited by 65 publications

References 89 publications

A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum

A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum

Using structural variants to understand the ecological and evolutionary dynamics of fungal plant pathogens

Deciphering complex genome rearrangements in C. elegans using short-read whole genome sequencing

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