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

• Published in: Nature ecology & evolution Vol. 1; no. 12; pp. 1931 - 1941
• Main Authors: Sipos, György, Prasanna, Arun N., Walter, Mathias C., O’Connor, Eoin, Bálint, Balázs, Krizsán, Krisztina, Kiss, Brigitta, Hess, Jaqueline, Varga, Torda, Slot, Jason, Riley, Robert, Bóka, Bettina, Rigling, Daniel, Barry, Kerrie, Lee, Juna, Mihaltcheva, Sirma, LaButti, Kurt, Lipzen, Anna, Waldron, Rose, Moloney, Nicola M., Sperisen, Christoph, Kredics, László, Vágvölgyi, Csaba, Patrignani, Andrea, Fitzpatrick, David, Nagy, István, Doyle, Sean, Anderson, James B., Grigoriev, Igor V., Güldener, Ulrich, Münsterkötter, Martin, Nagy, László G.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-12-2017; Nature Publishing Group
• Subjects: 631/136; 631/181/2474; 631/208/212; BASIC BIOLOGICAL SCIENCES; Biological and Physical Anthropology; Biomedical and Life Sciences; Decay fungi; Developmental stages; Dispersal; Dispersion; Ecology; Evolutionary Biology; Fruit bodies; Fungi; Gene expression; Gene sequencing; Genes; Genomes; Life Sciences; Lignocellulose; Morphogenesis; Mycelia; Paleontology; Pathogenicity; Pathogens; Plant diseases; Proteomics; Rhizomorphs; Ribonucleic acid; RNA; Root rot; Species; Toolkits; Zoology
• ISSN: 2397-334X; 2397-334X
• DOI: 10.1038/s41559-017-0347-8

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.
Fungi of the genus
Armillaria
include devastating forest pathogens that cause root rot disease in many plants. Sequencing genomes and transcriptomes of several species, the authors reveal the genetic basis of dispersal, multicellular development and pathogenic mechanisms in
Armillaria
.