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Title: The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

Abstract

SUMMARYThe genusTrichodermacontains fungi with high relevance for humans, with applications in enzyme production for plant cell wall degradation and use in biocontrol. Here, we provide a broad, comprehensive overview of the genomic content of these species for “hot topic” research aspects, including CAZymes, transport, transcription factors, and development, along with a detailed analysis and annotation of less-studied topics, such as signal transduction, genome integrity, chromatin, photobiology, or lipid, sulfur, and nitrogen metabolism inT. reesei,T. atroviride, andT. virens, and we open up new perspectives to those topics discussed previously. In total, we covered more than 2,000 of the predicted 9,000 to 11,000 genes of eachTrichodermaspecies discussed, which is >20% of the respective gene content. Additionally, we considered available transcriptome data for the annotated genes. Highlights of our analyses include overall carbohydrate cleavage preferences due to the different genomic contents and regulation of the respective genes. We found light regulation of many sulfur metabolic genes. Additionally, a new Golgi 1,2-mannosidase likely involved inN-linked glycosylation was detected, as were indications for the ability ofTrichodermaspp. to generate hybrid galactose-containingN-linked glycans. The genomic inventory of effector proteins revealed numerous compounds unique toTrichoderma, and these warrant further investigation. We found interesting expansions in theTrichodermagenus in severalmore » signaling pathways, such as G-protein-coupled receptors, RAS GTPases, and casein kinases. A particularly interesting feature absolutely unique toT. atrovirideis the duplication of the alternative sulfur amino acid synthesis pathway.« less


Citation Formats

Schmoll, Monika, Dattenböck, Christoph, Carreras-Villaseñor, Nohemí, Mendoza-Mendoza, Artemio, Tisch, Doris, Alemán, Mario Ivan, Baker, Scott E., Brown, Christopher, Cervantes-Badillo, Mayte Guadalupe, Cetz-Chel, José, Cristobal-Mondragon, Gema Rosa, Delaye, Luis, Esquivel-Naranjo, Edgardo Ulises, Frischmann, Alexa, Gallardo-Negrete, Jose de Jesus, García-Esquivel, Monica, Gomez-Rodriguez, Elida Yazmin, Greenwood, David R., Hernández-Oñate, Miguel, Kruszewska, Joanna S., Lawry, Robert, Mora-Montes, Hector M., Muñoz-Centeno, Tania, Nieto-Jacobo, Maria Fernanda, Nogueira Lopez, Guillermo, Olmedo-Monfil, Vianey, Osorio-Concepcion, Macario, Piłsyk, Sebastian, Pomraning, Kyle R., Rodriguez-Iglesias, Aroa, Rosales-Saavedra, Maria Teresa, Sánchez-Arreguín, J. Alejandro, Seidl-Seiboth, Verena, Stewart, Alison, Uresti-Rivera, Edith Elena, Wang, Chih-Li, Wang, Ting-Fang, Zeilinger, Susanne, Casas-Flores, Sergio, and Herrera-Estrella, Alfredo. The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species. United States: N. p., 2016. Web. doi:10.1128/MMBR.00040-15.
Schmoll, Monika, Dattenböck, Christoph, Carreras-Villaseñor, Nohemí, Mendoza-Mendoza, Artemio, Tisch, Doris, Alemán, Mario Ivan, Baker, Scott E., Brown, Christopher, Cervantes-Badillo, Mayte Guadalupe, Cetz-Chel, José, Cristobal-Mondragon, Gema Rosa, Delaye, Luis, Esquivel-Naranjo, Edgardo Ulises, Frischmann, Alexa, Gallardo-Negrete, Jose de Jesus, García-Esquivel, Monica, Gomez-Rodriguez, Elida Yazmin, Greenwood, David R., Hernández-Oñate, Miguel, Kruszewska, Joanna S., Lawry, Robert, Mora-Montes, Hector M., Muñoz-Centeno, Tania, Nieto-Jacobo, Maria Fernanda, Nogueira Lopez, Guillermo, Olmedo-Monfil, Vianey, Osorio-Concepcion, Macario, Piłsyk, Sebastian, Pomraning, Kyle R., Rodriguez-Iglesias, Aroa, Rosales-Saavedra, Maria Teresa, Sánchez-Arreguín, J. Alejandro, Seidl-Seiboth, Verena, Stewart, Alison, Uresti-Rivera, Edith Elena, Wang, Chih-Li, Wang, Ting-Fang, Zeilinger, Susanne, Casas-Flores, Sergio, & Herrera-Estrella, Alfredo. The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species. United States. doi:10.1128/MMBR.00040-15.
Schmoll, Monika, Dattenböck, Christoph, Carreras-Villaseñor, Nohemí, Mendoza-Mendoza, Artemio, Tisch, Doris, Alemán, Mario Ivan, Baker, Scott E., Brown, Christopher, Cervantes-Badillo, Mayte Guadalupe, Cetz-Chel, José, Cristobal-Mondragon, Gema Rosa, Delaye, Luis, Esquivel-Naranjo, Edgardo Ulises, Frischmann, Alexa, Gallardo-Negrete, Jose de Jesus, García-Esquivel, Monica, Gomez-Rodriguez, Elida Yazmin, Greenwood, David R., Hernández-Oñate, Miguel, Kruszewska, Joanna S., Lawry, Robert, Mora-Montes, Hector M., Muñoz-Centeno, Tania, Nieto-Jacobo, Maria Fernanda, Nogueira Lopez, Guillermo, Olmedo-Monfil, Vianey, Osorio-Concepcion, Macario, Piłsyk, Sebastian, Pomraning, Kyle R., Rodriguez-Iglesias, Aroa, Rosales-Saavedra, Maria Teresa, Sánchez-Arreguín, J. Alejandro, Seidl-Seiboth, Verena, Stewart, Alison, Uresti-Rivera, Edith Elena, Wang, Chih-Li, Wang, Ting-Fang, Zeilinger, Susanne, Casas-Flores, Sergio, and Herrera-Estrella, Alfredo. Wed . "The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species". United States. doi:10.1128/MMBR.00040-15.
@article{osti_1333999,
title = {The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species},
author = {Schmoll, Monika and Dattenböck, Christoph and Carreras-Villaseñor, Nohemí and Mendoza-Mendoza, Artemio and Tisch, Doris and Alemán, Mario Ivan and Baker, Scott E. and Brown, Christopher and Cervantes-Badillo, Mayte Guadalupe and Cetz-Chel, José and Cristobal-Mondragon, Gema Rosa and Delaye, Luis and Esquivel-Naranjo, Edgardo Ulises and Frischmann, Alexa and Gallardo-Negrete, Jose de Jesus and García-Esquivel, Monica and Gomez-Rodriguez, Elida Yazmin and Greenwood, David R. and Hernández-Oñate, Miguel and Kruszewska, Joanna S. and Lawry, Robert and Mora-Montes, Hector M. and Muñoz-Centeno, Tania and Nieto-Jacobo, Maria Fernanda and Nogueira Lopez, Guillermo and Olmedo-Monfil, Vianey and Osorio-Concepcion, Macario and Piłsyk, Sebastian and Pomraning, Kyle R. and Rodriguez-Iglesias, Aroa and Rosales-Saavedra, Maria Teresa and Sánchez-Arreguín, J. Alejandro and Seidl-Seiboth, Verena and Stewart, Alison and Uresti-Rivera, Edith Elena and Wang, Chih-Li and Wang, Ting-Fang and Zeilinger, Susanne and Casas-Flores, Sergio and Herrera-Estrella, Alfredo},
abstractNote = {SUMMARYThe genusTrichodermacontains fungi with high relevance for humans, with applications in enzyme production for plant cell wall degradation and use in biocontrol. Here, we provide a broad, comprehensive overview of the genomic content of these species for “hot topic” research aspects, including CAZymes, transport, transcription factors, and development, along with a detailed analysis and annotation of less-studied topics, such as signal transduction, genome integrity, chromatin, photobiology, or lipid, sulfur, and nitrogen metabolism inT. reesei,T. atroviride, andT. virens, and we open up new perspectives to those topics discussed previously. In total, we covered more than 2,000 of the predicted 9,000 to 11,000 genes of eachTrichodermaspecies discussed, which is >20% of the respective gene content. Additionally, we considered available transcriptome data for the annotated genes. Highlights of our analyses include overall carbohydrate cleavage preferences due to the different genomic contents and regulation of the respective genes. We found light regulation of many sulfur metabolic genes. Additionally, a new Golgi 1,2-mannosidase likely involved inN-linked glycosylation was detected, as were indications for the ability ofTrichodermaspp. to generate hybrid galactose-containingN-linked glycans. The genomic inventory of effector proteins revealed numerous compounds unique toTrichoderma, and these warrant further investigation. We found interesting expansions in theTrichodermagenus in several signaling pathways, such as G-protein-coupled receptors, RAS GTPases, and casein kinases. A particularly interesting feature absolutely unique toT. atrovirideis the duplication of the alternative sulfur amino acid synthesis pathway.},
doi = {10.1128/MMBR.00040-15},
journal = {Microbiology and Molecular Biology Reviews},
number = 1,
volume = 80,
place = {United States},
year = {Wed Feb 10 00:00:00 EST 2016},
month = {Wed Feb 10 00:00:00 EST 2016}
}
  • We sequenced and compared the genomes of the Dothideomycete fungal plant pathogens Cladosporium fulvum (Cfu) (syn. Passalora fulva) and Dothistroma septosporum (Dse) that are closely related phylogenetically, but have different lifestyles and hosts. Although both fungi grow extracellularly in close contact with host mesophyll cells, Cfu is a biotroph infecting tomato, while Dse is a hemibiotroph infecting pine. The genomes of these fungi have a similar set of genes (70percent of gene content in both genomes are homologs), but differ significantly in size (Cfu >61.1-Mb; Dse 31.2-Mb), which is mainly due to the difference in repeat content (47.2percent in Cfumore » versus 3.2percent in Dse). Recent adaptation to different lifestyles and hosts is suggested by diverged sets of genes. Cfu contains an tomatinase gene that we predict might be required for detoxification of tomatine, while this gene is absent in Dse. Many genes encoding secreted proteins are unique to each species and the repeat-rich areas in Cfu are enriched for these species-specific genes. In contrast, conserved genes suggest common host ancestry. Homologs of Cfu effector genes, including Ecp2 and Avr4, are present in Dse and induce a Cf-Ecp2- and Cf-4-mediated hypersensitive response, respectively. Strikingly, genes involved in production of the toxin dothistromin, a likely virulence factor for Dse, are conserved in Cfu, but their expression differs markedly with essentially no expression by Cfu in planta. Likewise, Cfu has a carbohydrate-degrading enzyme catalog that is more similar to that of necrotrophs or hemibiotrophs and a larger pectinolytic gene arsenal than Dse, but many of these genes are not expressed in planta or are pseudogenized. Overall, comparison of their genomes suggests that these closely related plant pathogens had a common ancestral host but since adapted to different hosts and lifestyles by a combination of differentiated gene content, pseudogenization, and gene regulation.« less
  • The class Dothideomycetes is one of the largest groups of fungi with a high level of ecological diversity including many plant pathogens infecting a broad range of hosts. Here, we compare genome features of 18 members of this class, including 6 necrotrophs, 9 (hemi)biotrophs and 3 saprotrophs, to analyze genome structure, evolution, and the diverse strategies of pathogenesis. The Dothideomycetes most likely evolved from a common ancestor more than 280 million years ago. The 18 genome sequences differ dramatically in size due to variation in repetitive content, but show much less variation in number of (core) genes. Gene order appearsmore » to have been rearranged mostly within chromosomal boundaries by multiple inversions, in extant genomes frequently demarcated by adjacent simple repeats. Several Dothideomycetes contain one or more gene-poor, transposable element (TE)-rich putatively dispensable chromosomes of unknown function. The 18 Dothideomycetes offer an extensive catalogue of genes involved in cellulose degradation, proteolysis, secondary metabolism, and cysteine-rich small secreted proteins. Ancestors of the two major orders of plant pathogens in the Dothideomycetes, the Capnodiales and Pleosporales, may have had different modes of pathogenesis, with the former having fewer of these genes than the latter. Many of these genes are enriched in proximity to transposable elements, suggesting faster evolution because of the effects of repeat induced point (RIP) mutations. A syntenic block of genes, including oxidoreductases, is conserved in most Dothideomycetes and upregulated during infection in L. maculans, suggesting a possible function in response to oxidative stress.« less