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Title: Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina

Abstract

Ustilaginomycotina is home to a broad array of fungi including important plant pathogens collectively called smut fungi. Smuts are biotrophs that produce characteristic perennating propagules called teliospores, one of which, Ustilago maydis, is a model genetic organism. Broad exploration of smut biology has been hampered by limited phylogenetic resolution of Ustilaginiomycotina as well as an overall lack of genomic data for members of this subphylum. In this study, we sequenced eight Ustilaginomycotina genomes from previously unrepresented lineages, deciphered ordinal-level phylogenetic relationships for the subphylum, and performed comparative analyses. Unlike other Basidiomycota subphyla, all sampled Ustilaginomycotina genomes are relatively small and compact. Ancestral state reconstruction analyses indicate that teliospore formation was present at the origin of the subphylum. Divergence time estimation dates the divergence of most extant smut fungi after that of grasses (Poaceae). However, we found limited conservation of well-characterized genes related to smut pathogenesis from U. maydis, indicating dissimilar pathogenic mechanisms exist across other smut lineages. The genomes of Malasseziomycetes are highly diverged from the other sampled Ustilaginomycotina, likely due to their unique history as mammal-associated lipophilic yeasts. Despite extensive genomic data, the phylogenetic placement of this class remains ambiguous. Although the sampled Ustilaginomycotina members lack many core enzymesmore » for plant cell wall decomposition and starch catabolism, we identified several novel carbohydrate active enzymes potentially related to pectin breakdown. Finally, ~50% of Ustilaginomycotina species-specific genes are present in previously undersampled and rare lineages, highlighting the importance of exploring fungal diversity as a resource for novel gene discovery.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [4];  [5];  [6];  [1]
  1. Purdue Univ., West Lafayette, IN (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Aix-Marseille Univ., and CNRS, Marseille (France); Institut National de la Recherche Agronomique (INRA), Marseille (France)
  4. Aix-Marseille Univ., and CNRS, Marseille (France); Institut National de la Recherche Agronomique (INRA), Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  6. Oregon State Univ., Corvallis, OR (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1543987
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Molecular Biology and Evolution
Additional Journal Information:
Journal Volume: 35; Journal Issue: 8; Journal ID: ISSN 0737-4038
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
Biochemistry & Molecular Biology; Evolutionary Biology; Genetics & Heredity

Citation Formats

Kijpornyongpan, Teeratas, Mondo, Stephen J., Barry, Kerrie, Sandor, Laura, Lee, Juna, Lipzen, Anna, Pangilinan, Jasmyn, LaButti, Kurt, Hainaut, Matthieu, Henrissat, Bernard, Grigoriev, Igor V., Spatafora, Joseph W., and Aime, M. Catherine. Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina. United States: N. p., 2018. Web. doi:10.1093/molbev/msy072.
Kijpornyongpan, Teeratas, Mondo, Stephen J., Barry, Kerrie, Sandor, Laura, Lee, Juna, Lipzen, Anna, Pangilinan, Jasmyn, LaButti, Kurt, Hainaut, Matthieu, Henrissat, Bernard, Grigoriev, Igor V., Spatafora, Joseph W., & Aime, M. Catherine. Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina. United States. doi:10.1093/molbev/msy072.
Kijpornyongpan, Teeratas, Mondo, Stephen J., Barry, Kerrie, Sandor, Laura, Lee, Juna, Lipzen, Anna, Pangilinan, Jasmyn, LaButti, Kurt, Hainaut, Matthieu, Henrissat, Bernard, Grigoriev, Igor V., Spatafora, Joseph W., and Aime, M. Catherine. Tue . "Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina". United States. doi:10.1093/molbev/msy072. https://www.osti.gov/servlets/purl/1543987.
@article{osti_1543987,
title = {Broad Genomic Sampling Reveals a Smut Pathogenic Ancestry of the Fungal Clade Ustilaginomycotina},
author = {Kijpornyongpan, Teeratas and Mondo, Stephen J. and Barry, Kerrie and Sandor, Laura and Lee, Juna and Lipzen, Anna and Pangilinan, Jasmyn and LaButti, Kurt and Hainaut, Matthieu and Henrissat, Bernard and Grigoriev, Igor V. and Spatafora, Joseph W. and Aime, M. Catherine},
abstractNote = {Ustilaginomycotina is home to a broad array of fungi including important plant pathogens collectively called smut fungi. Smuts are biotrophs that produce characteristic perennating propagules called teliospores, one of which, Ustilago maydis, is a model genetic organism. Broad exploration of smut biology has been hampered by limited phylogenetic resolution of Ustilaginiomycotina as well as an overall lack of genomic data for members of this subphylum. In this study, we sequenced eight Ustilaginomycotina genomes from previously unrepresented lineages, deciphered ordinal-level phylogenetic relationships for the subphylum, and performed comparative analyses. Unlike other Basidiomycota subphyla, all sampled Ustilaginomycotina genomes are relatively small and compact. Ancestral state reconstruction analyses indicate that teliospore formation was present at the origin of the subphylum. Divergence time estimation dates the divergence of most extant smut fungi after that of grasses (Poaceae). However, we found limited conservation of well-characterized genes related to smut pathogenesis from U. maydis, indicating dissimilar pathogenic mechanisms exist across other smut lineages. The genomes of Malasseziomycetes are highly diverged from the other sampled Ustilaginomycotina, likely due to their unique history as mammal-associated lipophilic yeasts. Despite extensive genomic data, the phylogenetic placement of this class remains ambiguous. Although the sampled Ustilaginomycotina members lack many core enzymes for plant cell wall decomposition and starch catabolism, we identified several novel carbohydrate active enzymes potentially related to pectin breakdown. Finally, ~50% of Ustilaginomycotina species-specific genes are present in previously undersampled and rare lineages, highlighting the importance of exploring fungal diversity as a resource for novel gene discovery.},
doi = {10.1093/molbev/msy072},
journal = {Molecular Biology and Evolution},
number = 8,
volume = 35,
place = {United States},
year = {2018},
month = {5}
}

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