Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

György Sipos,László G Nagy,László Kredics,István Nagy,James B Anderson,Martin Münsterkötter,Csaba Vágvölgyi,Bettina Bóka,Ulrich Güldener,Balázs Bálint,Krisztina Krizsán,Jaqueline Hess,R M Waldron ,Anna Lipzen,Robert Riley,Christoph Sperisen,Mathias C Walter,Andrea Patrignani,Seán Doyle ,Juna Lee,Eabhann O’connor ,Sirma Mihaltcheva,Igor V Grigoriev,Torda Varga,Jason C Slot ,Brigitta Kiss,Kurt Labutti,Kerrie Barry,Arun N Prasanna,Daniel Rigling,David A Fitzpatrick ,Nicola M Moloney

doi:10.1038/s41559-017-0347-8

Abstract

Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth. They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Here, we sequenced and analysed the genomes of four Armillaria species and performed RNA sequencing and quantitative proteomic analysis on the invasive and reproductive developmental stages of A. ostoyae. Comparison with 22 related fungi revealed a significant genome expansion in Armillaria, affecting several pathogenicity-related genes, lignocellulose-degrading enzymes and lineage-specific genes expressed during rhizomorph development. Rhizomorphs express an evolutionarily young transcriptome that shares features with the transcriptomes of both fruiting bodies and vegetative mycelia. Several genes show concomitant upregulation in rhizomorphs and fruiting bodies and share cis-regulatory signatures in their promoters, providing genetic and regulatory insights into complex multicellularity in fungi. Our results suggest that the evolution of the unique dispersal and pathogenicity mechanisms of Armillaria might have drawn upon ancestral genetic toolkits for wood-decay, morphogenesis and complex multicellularity.

Highlights

Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth
The only -omics data published so far have highlighted a substantial repertoire of plant cell wall degrading enzymes (PCWDE) and secreted proteins, among others, in A. mellea and A. solidipes[11,12], while analyses of the genomes of other pathogenic basidiomycetes identified genes coding for PCWDEs, secreted and effector proteins or secondary metabolism (SM) as putative pathogenicity factors
We report the genomes of A. ostoyae, A. cepistipes, A. gallica and A. solidipes sequenced using a combination of PacBio and Illumina technologies (Table 1)

Summary

Introduction

Armillaria species are both devastating forest pathogens and some of the largest terrestrial organisms on Earth They forage for hosts and achieve immense colony sizes via rhizomorphs, root-like multicellular structures of clonal dispersal. Individuals of Armillaria can reach immense sizes and include the ‘humongous fungus’, one of the largest terrestrial organisms on Earth[3], measuring up to 965 hectares and 600 tons[4], and can display a mutation rate ≅3 orders of magnitude lower than most filamentous fungi[5] Individuals reach this immense size via growing rhizomorphs, dark mycelial strings 1–4 mm wide that allow the fungus to bridge gaps between food sources or host plants[1,6] ( the name shoestring root rot). Transcript and proteome profiling of invasive and reproductive developmental stages shed light on the role of rhizomorphs, several putative pathogenicity factors, and the morphogenetic mechanisms of rhizomorph and fruiting body development

Methods

Results

Conclusion