Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria - Archive ouverte HAL Access content directly
Journal Articles Nature Microbiology Year : 2023

Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria

Neha Sahu
  • Function : Author
Boris Indic
  • Function : Author
Johanna Wong-Bajracharya
  • Function : Author
Zsolt Merényi
  • Function : Author
Huei-Mien Ke
Steven Ahrendt
Tori-Lee Monk
  • Function : Author
Sándor Kocsubé
  • Function : Author
Anna Lipzen
  • Function : Author
Balázs Bálint
Bernard Henrissat
Bill Andreopoulos
  • Function : Author
Francis Martin
Christoffer Bugge Harder
Daniel Rigling
Kathryn Ford
  • Function : Author
Gary Foster
  • Function : Author
Jasmyn Pangilinan
  • Function : Author
Alexie Papanicolaou
Kerrie Barry
Kurt Labutti
Máté Virágh
  • Function : Author
Maxim Koriabine
  • Function : Author
Mi Yan
  • Function : Author
Robert Riley
  • Function : Author
Simang Champramary
  • Function : Author
Krista Plett
  • Function : Author
Igor Grigoriev
Isheng Jason Tsai
Jason Slot
  • Function : Author
György Sipos
Jonathan Plett
László Nagy

Abstract

The fungal genus Armillaria contains necrotrophic pathogens and some of the largest terrestrial organisms that cause tremendous losses in diverse ecosystems, yet how they evolved pathogenicity in a clade of dominantly non-pathogenic wood degraders remains elusive. Here we show that Armillaria species, in addition to gene duplications and de novo gene origins, acquired at least 1,025 genes via 124 horizontal gene transfer events, primarily from Ascomycota. Horizontal gene transfer might have affected plant biomass degrading and virulence abilities of Armillaria, and provides an explanation for their unusual, soft rot-like wood decay strategy. Combined multi-species expression data revealed extensive regulation of horizontally acquired and wood-decay related genes, putative virulence factors and two novel conserved pathogenicity-induced small secreted proteins, which induced necrosis in planta. Overall, this study details how evolution knitted together horizontally and vertically inherited genes in complex adaptive traits of plant biomass degradation and pathogenicity in important fungal pathogens. The fungal genus Armillaria includes virulent necrotrophic pathogens, unusual wood decayers and the largest terrestrial organisms on Earth. Sahu et al. suggest that horizontal gene transfer contributed to the evolution of some of these unique traits.

Dates and versions

hal-04382375 , version 1 (09-01-2024)

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Neha Sahu, Boris Indic, Johanna Wong-Bajracharya, Zsolt Merényi, Huei-Mien Ke, et al.. Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria. Nature Microbiology, 2023, 8 (9), pp.1668-1681. ⟨10.1038/s41564-023-01448-1⟩. ⟨hal-04382375⟩
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