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

Nature Microbiology volume 8, pages 1668–1681 (2023)Cite this article

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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.

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Fig. 1: Genome statistics and reconstruction of ancestral genome sizes for 15 Armillaria species and 5 Physalacriaceae outgroups.
Fig. 2: Plant biomass degradation related genes in Armillaria.
Fig. 3: HGTs into Armillaria and the Physalacriaceae family.
Fig. 4: Enrichment of DEGs of wood-decay, pathogenicity, stress response and other gene families in six RNA-seq datasets.
Fig. 5: PiSSPs of A. luteobubalina induce cell death in host plants.

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Data availability

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.

Code availability

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

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Acknowledgements

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.

Author information

Author notes

  1. Huei-Mien Ke

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

Authors and Affiliations

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

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

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

    Neha Sahu & Simang Champramary

  3. 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

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

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

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

    Johanna Wong-Bajracharya & Krista L. Plett

  6. Biodiversity Research Center, Academia Sinica, Taipei, Taiwan

    Huei-Mien Ke & Isheng Jason Tsai

  7. 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

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

    Sándor Kocsubé

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

    Sándor Kocsubé

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

    Elodie Drula

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

    Elodie Drula

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

    Bernard Henrissat

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

    Bernard Henrissat

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

    Francis M. Martin

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

    Christoffer Bugge Harder

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

    Christoffer Bugge Harder

  17. Swiss Federal Research Institute WSL, Birmensdorf, Switzerland

    Daniel Rigling

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

    Kathryn L. Ford & Gary D. Foster

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

    Igor V. Grigoriev

  20. 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.

Corresponding author

Correspondence to László G. Nagy.

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The authors declare no competing interests.

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Peer review information

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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Extended data

Extended Data Fig. 1 Summary of gene losses and gains from COMPARE mappings.

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

Extended Data Fig. 2 GO terms enriched in duplicated genes.

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

Extended Data Fig. 3 Plant biomass degradation related genes in Armillaria.

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

Source data

Extended Data Fig. 4 Expression of HT and VT genes in A. ostoyae developmental transcriptome.

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

Extended Data Fig. 5 Experimental setup.

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.

Extended Data Fig. 6 Enrichment of differentially expressed genes of selected gene families in 6 RNA-Seq datasets.

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

Extended Data Fig. 7 Expression heatmaps in A. luteobubalina.

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

Extended Data Fig. 8 Pathogenicity-induced SSP expression and conservation in A. luteobubalina.

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

Extended Data Fig. 9 Copy numbers and conservation of Armlut1_1348401.

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

Source data

Extended Data Fig. 10 Copy numbers and conservation of Armlut1_1165297.

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 information

Supplementary Information

Supplementary Figs. 1–12 and Note 1.

Reporting Summary

Peer Review File

Supplementary Table 1

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

Supplementary Table 2

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

Supplementary Table 3

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.

Supplementary Table 4

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

Supplementary Table 5

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

Supplementary Table 6

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

Source data

Source Data Fig. 1

Statistical data for genome statistics in Fig. 1.

Source Data Fig. 2

Statistical data for box plot in Fig. 2b.

Source Data Fig. 3

Statistical data for Fig. 3a,c.

Source Data Fig. 4

Statistical data for Fig. 4a,b.

Source Data Fig. 5

Unprocessed raw pictures for Fig. 5b.

Source Data Extended Data Fig. 1/Table 1

Statistical data for Extended Data Fig. 1b.

Source Data Extended Data Fig. 2/Table 2

Statistical data for Extended Data Fig. 2.

Source Data Extended Data Fig. 3/Table 3

Statistical data for Extended Data Fig. 3.

Source Data Extended Data Fig. 4/Table 4

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

Source Data Extended Data Fig. 6/Table 6

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

Source Data Extended Data Fig. 7/Table 7

Statistical data for Extended Data Fig. 7.

Source Data Extended Data Fig. 8/Table 8

Statistical data for Extended Data Fig. 8.

Source Data Extended Data Fig. 9/Table 9

Statistical data for Extended Data Fig. 9b.

Source Data Extended Data Fig. 10/Table 10

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 8, 1668–1681 (2023). https://doi.org/10.1038/s41564-023-01448-1

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