Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens.

Jonathan Grandaubert,Corinne Cruaud,Marie-Hélène Balesdent,Valérie Barbe,Jessica L Soyer,Thierry Rouxel,Nicolas Lapalu,Bénédicte Ollivier,Angela P Van De Wouw,Juliette Linglin,Sophie Mangenot,Rohan Gt Lowe,Isabelle Fudal,Barbara J Howlett,Barbara Robbertse,Hossein Borhan,Conrad L Schoch,Matthew G Links

doi:10.1186/1471-2164-15-891

Abstract

BackgroundMany plant-pathogenic fungi have a tendency towards genome size expansion, mostly driven by increasing content of transposable elements (TEs). Through comparative and evolutionary genomics, five members of the Leptosphaeria maculans-Leptosphaeria biglobosa species complex (class Dothideomycetes, order Pleosporales), having different host ranges and pathogenic abilities towards cruciferous plants, were studied to infer the role of TEs on genome shaping, speciation, and on the rise of better adapted pathogens.ResultsL. maculans ‘brassicae’, the most damaging species on oilseed rape, is the only member of the species complex to have a TE-invaded genome (32.5%) compared to the other members genomes (<4%). These TEs had an impact at the structural level by creating large TE-rich regions and are suspected to have been instrumental in chromosomal rearrangements possibly leading to speciation. TEs, associated with species-specific genes involved in disease process, also possibly had an incidence on evolution of pathogenicity by promoting translocations of effector genes to highly dynamic regions and thus tuning the regulation of effector gene expression in planta.ConclusionsInvasion of L. maculans ‘brassicae’ genome by TEs followed by bursts of TE activity allowed this species to evolve and to better adapt to its host, making this genome species a peculiarity within its own species complex as well as in the Pleosporales lineage.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-891) contains supplementary material, which is available to authorized users.

Highlights

Many plant-pathogenic fungi have a tendency towards genome size expansion, mostly driven by increasing content of transposable elements (TEs)
In this paper we investigate when and how genome expansion took place in the L. maculans-L. biglobosa species complex, and the consequences it had on genome structure, adaptability and pathogenicity
Phylogeny and estimates of divergence times L. maculans and L. biglobosa belong to order Pleosporales from the class Dothideomycetes

Summary

Introduction

Many plant-pathogenic fungi have a tendency towards genome size expansion, mostly driven by increasing content of transposable elements (TEs). Some are plant and animal pathogens of major economic importance and as stressed by Kupferschmidt [1], “Fungi have become a greater global threat to crops, forests, and wild animals than ever before They have killed countless amphibians, pushing their free-living relatives [8], the first genome data from filamentous fungi did not indicate differences between genome size of fungal pathogens and that of saprophytes. The 45-Mb genome of Leptosphaeria maculans, the ascomycete that causes stem canker of crucifers contains 33% TEs, the 120-Mb genome of cereal downy mildew, Blumeria graminis, contains 64% TEs (while other closely related downy mildew pathogens have even larger genomes), and that of the 240-Mb oomycete Phytophthora infestans contains 74% TEs [8] These data, suggesting convergent evolution towards bigger genomes in widely divergent fungal and oomycete species, are intriguing and the counterbalance between selective advantage conferred to the pathogen and the cost of maintaining this amount of “parasitic” DNA is unknown

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