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

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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.

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New genomic assemblies and annotation generated in this study are deposited under the 1000 Fungal Genome Project at JGI Mycocosm (https://mycocosm.jgi.doe.gov/Armillaria/Armillaria.info.html) and at DDBJ/EMBL/GenBank under the accession numbers PRJNA463936, PRJNA500536, PRJNA500837, PRJNA519860, PRJNA519861, PRJNA571622, PRJNA677793 and PRJNA677794. New RNA-seq datasets used in this study are deposited in the National Center for Biotechnology Information’s Gene Expression Omnibus Archive at https://www.ncbi.nlm.nih.gov/geo/. Accession number for the in planta assay between A. luteobubalina and E. grandis is PRJNA975488, or GSE233220. For the stem invasion assay, the accession numbers are PRJNA972908 for A. ostoyae and PRJNA972989 for A. borealis. Phylogenetically validated gene trees and gene expression heatmaps for various gene families for the six RNA-seq datasets used in this study can be found in the Figshare repository at https://figshare.com/articles/dataset/Gene_trees/22730534 and https://figshare.com/articles/figure/Gene_expression_heatmaps/22778477?file=40472333 respectively. Source data are provided with this paper.

Codes associated with the data analyses and visualization are available at https://github.com/nehasahu486/Armillaria-phylogenomics/tree/main.

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We acknowledge support by the ‘Momentum’ programme of the Hungarian Academy of Sciences (contract no. LP2019-13/2019 to L.G.N.) the European Research Council (grant no. 758161 to L.G.N.) as well as the Eotvos Lorand Research Network (SA-109/2021). G.S. acknowledges support by the Hungarian National Research, Development, and Innovation Office (GINOP-2.3.2-15-2016-00052). The work (proposals: https://doi.org/10.46936/10.25585/60001060 and https://doi.org/10.46936/10.25585/60001019) conducted by the US Department of Energy (DOE) Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the US DOE operated under contract no. DE-AC02-05CH11231. The research was performed in collaboration with the Genomics and Bioinformatics Core Facility at the Szentágothai Research Centre of the University of Pécs. Ian Hood and Pam Taylor (Scion Research, New Zealand Forest Research Institute Ltd.) kindly provided the A. nova-zealandiae 2840 strain. D. Lindner (Forest Products Laboratory, USA) kindly shared strains of A. borealis and A. ectypa for sequencing. We appreciate the permission of G. Bonito for using the genome of Flagelloscypha sp.

Huei-Mien Ke

Present address: Department of Microbiology, Soochow University, Taipei, Taiwan

Biological Research Center, Synthetic and Systems Biology Unit, Szeged, Hungary

Neha Sahu, Zsolt Merényi, Balázs Bálint, Máté Virágh & László G. Nagy

Doctoral School of Biology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary

Neha Sahu & Simang Champramary

Functional Genomics and Bioinformatics Group, Faculty of Forestry, Institute of Forest and Natural Resource Management, University of Sopron, Sopron, Hungary

Boris Indic, Simang Champramary & György Sipos

Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales, Australia

Johanna Wong-Bajracharya, Tori-Lee Monk, Alexie Papanicolaou & Jonathan Plett

Elizabeth Macarthur Agricultural Institute, NSW Department of Primary Industries, Menangle, New South Wales, Australia

Johanna Wong-Bajracharya & Krista L. Plett

Biodiversity Research Center, Academia Sinica, Taipei, Taiwan

Huei-Mien Ke & Isheng Jason Tsai

US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

Steven Ahrendt, Anna Lipzen, Bill Andreopoulos, Jasmyn Pangilinan, Kerrie Barry, Kurt LaButti, Maxim Koriabine, Mi Yan, Robert Riley & Igor V. Grigoriev

Department of Microbiology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary

Sándor Kocsubé

ELKH-SZTE Fungal Pathogenicity Mechanisms Research Group, University of Szeged, Szeged, Hungary

Sándor Kocsubé

Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix-Marseille Université, Marseille, France

Elodie Drula

INRAE, UMR 1163, Biodiversité et Biotechnologie Fongiques, Marseille, France

Elodie Drula

DTU Bioengineering, Technical University of Denmark, Kongens Lyngby, Denmark

Bernard Henrissat

Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia

Bernard Henrissat

Université de Lorraine, INRAE, UMR 1136 ‘Interactions Arbres/Microorganismes’, Centre INRAE Grand Est – Nancy, Champenoux, France

Francis M. Martin

Department of Biology, Section of Terrestrial Ecology, University of Copenhagen, København Ø, Denmark

Christoffer Bugge Harder

Department of Biosciences, University of Oslo, Blindern, Oslo, Norway

Christoffer Bugge Harder

Swiss Federal Research Institute WSL, Birmensdorf, Switzerland

Daniel Rigling

School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol, UK

Kathryn L. Ford & Gary D. Foster

Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA

Igor V. Grigoriev

Department of Plant Pathology, The Ohio State University, Columbus, OH, USA

Jason Slot

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N.S., L.G.N., J.P. and G.S. conceived the study. N.S., B.I., J.W.-B., Z.M., K.L.P. and J.P. carried out the laboratory experiments, including DNA/RNA isolation for genome and transcriptome sequencing. N.S., Z.M., B.I., H.-M.K., S.K., E.D., B.B., B.H., M.V., S.C., I.J.T., J.S. and L.G.N. carried out data analysis. E.D. and B.H. annotated CAZymes for the genomes not available in JGI Mycocosm. N.S., J.S., Z.M., S.K. and L.G.N. analysed HGT events. S.A., T.-L.M., A.L., B.A., J.P., A.P., K.B., K.L., M.K., M.Y., R.R. and I.G.V. performed genome sequencing, assembly and annotation. J.P. and K.L.P. performed PiSSP experimental validation. K.L.F. and GDF contributed strains to the genome sequencing. C.B.H. contributed genomic data. L.G.N., N.S., J.P., F.M.M., J.S., S.K., G.S. and D.R. wrote the manuscript. All authors reviewed, checked and approved the manuscript.

Correspondence to László G. Nagy.

The authors declare no competing interests.

Nature Microbiology thanks Jonathan Schilling and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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a) Duplications (green) and losses (red) at each node for Dataset1. Bootstrap support values less than 80 are shown in blue. b) Transposable elements assessment for Armillaria and the Physalacriaceae.

Source data

Significantly enriched GO terms in the 1473 orthogroups, inferred by 2913 duplications at Armillaria MRCA. GO enrichment analysis was performed using one-sided Fisher’s test with the weight01 algorithm in the topGO package (R), with p-value ≤ 0.05 considered as significant. X-axis shows the percentage of significant genes from the total number of genes, y-axis shows p-values. Blue shows lower and red shows higher p-values. GO terms that had at least 30% of genes significant from the total number of genes are mentioned on the plot (see Supplementary Table 2 for the complete list of enriched GO terms).

Source data

Phylogenetic PCAs and their respective loading factors for PCWDE gene families. Species abbreviations are colored according to nutritional modes.

Source data

Violin plot showing gene expression of phylogenetically validated HT and VT genes in A. ostoyae fruiting body development transcriptome. Y-axis shows log2 transformed expression values, and x-axis shows the sample comparisons for each experiment.

Source data

Setup for the new RNA Seq experiments used in this study. a) Setup for the time-course experiment. b) Setup for the stem invasion assay.

The heatmap shows enrichment ratios for 23 gene groups (‘Ergothione: removed due to no enrichment) from aggregated differential gene expression data across 6 experiments (a - upregulated, b - downregulated genes). Y-axis shows the sample comparison for each dataset, with number of DEGs shown as a barplot at right. In the heatmap, warmer colors mean higher enrichment ratios (for complete list of odds ratios, see Supplementary Table 5).

Source data

Heatmaps showing gene expression along the time course in A. luteobubalina for gene families related to host immune suppression, oxidative stress, detoxification, and cytotoxicity. Warmer color depicts higher expression.

Source data

A) Heatmap shows log2 fold changes for annotated SSPs, upregulated in at least one-time point. Red shows higher and blue depicts lower logFC; followed by presence/absence matrix of homologs in 131 species (Dataset 2). X-axis shows ProteinIDs for both heatmap and presence/absence matrix. Y-axis shows sample comparisons in the heatmap; and species order in presence/absence matrix.

Source data

a) Summary of copy-numbers of the orthogroup OG0000784, comprising PiSSP Armlut1_1348401. b) Trimmed multiple sequence alignment of proteins in OG0000784.

Source data

a) Summary of copy-numbers of the orthogroup OG0000401, comprising PiSSP Armlut1_1165297. b) Trimmed multiple sequence alignment of proteins in OG0000401.

Source data

Supplementary Figs. 1–12 and Note 1.

New Armillaria genomes, list of species in each dataset used in this study, and their respective species trees.

Enriched genes in Armillaria duplications, and novel-core genes in Armillaria clade.

CAZymes and PCWDEs identified in Dataset 2, copy numbers of substrate-based PCWDEs in each species, PCA loadings from phylogenetic PCA, co-enriched CAZy OGs and their domain architecture.

HGTs in Physalacriaceae using AI and phylogenetic validation form gene trees.

DEGs in six RNA-seq experiments and odds ratio for different functional categories.

Expression data for A. luteobubalina SSPs in the in planta assay, and virulence factors and OG counts in stem invasion assays.

Statistical data for genome statistics in Fig. 1.

Statistical data for box plot in Fig. 2b.

Statistical data for Fig. 3a,c.

Statistical data for Fig. 4a,b.

Unprocessed raw pictures for Fig. 5b.

Statistical data for Extended Data Fig. 1b.

Statistical data for Extended Data Fig. 2.

Statistical data for Extended Data Fig. 3.

Statistical data for violin plot in Extended Data Fig. 4.

Statistical data for Extended Data Fig. 6a,b.

Statistical data for Extended Data Fig. 7.

Statistical data for Extended Data Fig. 8.

Statistical data for Extended Data Fig. 9b.

Statistical data for Extended Data Fig. 10b.

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Sahu, N., Indic, B., Wong-Bajracharya, J. et al. Vertical and horizontal gene transfer shaped plant colonization and biomass degradation in the fungal genus Armillaria. Nat Microbiol (2023). https://doi.org/10.1038/s41564-023-01448-1

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Received: 10 November 2022

Accepted: 11 July 2023

Published: 07 August 2023

DOI: https://doi.org/10.1038/s41564-023-01448-1

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