Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm
The Ascomycete <i>Ophiostoma novo-ulmi</i> threatens elm populations worldwide. The molecular mechanisms underlying its pathogenicity and virulence are still largely uncharacterized. As part of a collaborative study of the <i>O. novo-ulmi</i>-elm interactome, we analyzed the...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-06-01
|
| Series: | Journal of Fungi |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2309-608X/8/6/637 |
| _version_ | 1797485599760842752 |
|---|---|
| author | Martha Nigg Thais C. de Oliveira Jorge L. Sarmiento-Villamil Paul Y. de la Bastide Will E. Hintz Sherif M. Sherif Mukund Shukla Louis Bernier Praveen K. Saxena |
| author_facet | Martha Nigg Thais C. de Oliveira Jorge L. Sarmiento-Villamil Paul Y. de la Bastide Will E. Hintz Sherif M. Sherif Mukund Shukla Louis Bernier Praveen K. Saxena |
| author_sort | Martha Nigg |
| collection | DOAJ |
| description | The Ascomycete <i>Ophiostoma novo-ulmi</i> threatens elm populations worldwide. The molecular mechanisms underlying its pathogenicity and virulence are still largely uncharacterized. As part of a collaborative study of the <i>O. novo-ulmi</i>-elm interactome, we analyzed the <i>O. novo-ulmi</i> ssp. <i>americana</i> transcriptomes obtained by deep sequencing of messenger RNAs recovered from <i>Ulmus americana</i> saplings from one resistant (Valley Forge, VF) and one susceptible (S) elm genotypes at 0 and 96 h post-inoculation (hpi). Transcripts were identified for 6424 of the 8640 protein-coding genes annotated in the <i>O. novo-ulmi</i> nuclear genome. A total of 1439 genes expressed in planta had orthologs in the PHI-base curated database of genes involved in host-pathogen interactions, whereas 472 genes were considered differentially expressed (DEG) in S elms (370 genes) and VF elms (102 genes) at 96 hpi. Gene ontology (GO) terms for processes and activities associated with transport and transmembrane transport accounted for half (27/55) of GO terms that were significantly enriched in fungal genes upregulated in S elms, whereas the 22 GO terms enriched in genes overexpressed in VF elms included nine GO terms associated with metabolism, catabolism and transport of carbohydrates. Weighted gene co-expression network analysis identified three modules that were significantly associated with higher gene expression in S elms. The three modules accounted for 727 genes expressed in planta and included 103 DEGs upregulated in S elms. Knockdown- and knockout mutants were obtained for eight <i>O. novo-ulmi</i> genes. Although mutants remained virulent towards <i>U. americana</i> saplings, we identified a large repertoire of additional candidate <i>O. novo-ulmi</i> pathogenicity genes for functional validation by loss-of-function approaches. |
| first_indexed | 2024-03-09T23:21:07Z |
| format | Article |
| id | doaj.art-0f12f6f1dd0a45678e8d86d5dfe37d62 |
| institution | Directory Open Access Journal |
| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-09T23:21:07Z |
| publishDate | 2022-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Journal of Fungi |
| spelling | doaj.art-0f12f6f1dd0a45678e8d86d5dfe37d622023-11-23T17:25:24ZengMDPI AGJournal of Fungi2309-608X2022-06-018663710.3390/jof8060637Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American ElmMartha Nigg0Thais C. de Oliveira1Jorge L. Sarmiento-Villamil2Paul Y. de la Bastide3Will E. Hintz4Sherif M. Sherif5Mukund Shukla6Louis Bernier7Praveen K. Saxena8Centre d’Étude de la Forêt (CEF) and Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, QC G1V 0A6, CanadaCentre d’Étude de la Forêt (CEF) and Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, QC G1V 0A6, CanadaCentre d’Étude de la Forêt (CEF) and Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, QC G1V 0A6, CanadaDepartment of Biology, Centre for Forest Biology, University of Victoria, Victoria, BC V8W 2Y2, CanadaDepartment of Biology, Centre for Forest Biology, University of Victoria, Victoria, BC V8W 2Y2, CanadaAlson H. Smith Jr. Agricultural Research and Extension Center, School of Plant and Environmental Sciences, Virginia Tech, Winchester, VA 22602, USADepartment of Plant Agriculture, Gosling Research Institute for Plant Preservation (GRIPP), University of Guelph, Guelph, ON N1G 2W1, CanadaCentre d’Étude de la Forêt (CEF) and Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, QC G1V 0A6, CanadaDepartment of Plant Agriculture, Gosling Research Institute for Plant Preservation (GRIPP), University of Guelph, Guelph, ON N1G 2W1, CanadaThe Ascomycete <i>Ophiostoma novo-ulmi</i> threatens elm populations worldwide. The molecular mechanisms underlying its pathogenicity and virulence are still largely uncharacterized. As part of a collaborative study of the <i>O. novo-ulmi</i>-elm interactome, we analyzed the <i>O. novo-ulmi</i> ssp. <i>americana</i> transcriptomes obtained by deep sequencing of messenger RNAs recovered from <i>Ulmus americana</i> saplings from one resistant (Valley Forge, VF) and one susceptible (S) elm genotypes at 0 and 96 h post-inoculation (hpi). Transcripts were identified for 6424 of the 8640 protein-coding genes annotated in the <i>O. novo-ulmi</i> nuclear genome. A total of 1439 genes expressed in planta had orthologs in the PHI-base curated database of genes involved in host-pathogen interactions, whereas 472 genes were considered differentially expressed (DEG) in S elms (370 genes) and VF elms (102 genes) at 96 hpi. Gene ontology (GO) terms for processes and activities associated with transport and transmembrane transport accounted for half (27/55) of GO terms that were significantly enriched in fungal genes upregulated in S elms, whereas the 22 GO terms enriched in genes overexpressed in VF elms included nine GO terms associated with metabolism, catabolism and transport of carbohydrates. Weighted gene co-expression network analysis identified three modules that were significantly associated with higher gene expression in S elms. The three modules accounted for 727 genes expressed in planta and included 103 DEGs upregulated in S elms. Knockdown- and knockout mutants were obtained for eight <i>O. novo-ulmi</i> genes. Although mutants remained virulent towards <i>U. americana</i> saplings, we identified a large repertoire of additional candidate <i>O. novo-ulmi</i> pathogenicity genes for functional validation by loss-of-function approaches.https://www.mdpi.com/2309-608X/8/6/637Dutch elm disease<i>Ophiostoma novo-ulmi</i>RNA-Seqpathogenicityvirulencemutants |
| spellingShingle | Martha Nigg Thais C. de Oliveira Jorge L. Sarmiento-Villamil Paul Y. de la Bastide Will E. Hintz Sherif M. Sherif Mukund Shukla Louis Bernier Praveen K. Saxena Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm Journal of Fungi Dutch elm disease <i>Ophiostoma novo-ulmi</i> RNA-Seq pathogenicity virulence mutants |
| title | Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm |
| title_full | Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm |
| title_fullStr | Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm |
| title_full_unstemmed | Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm |
| title_short | Comparative Analysis of Transcriptomes of <i>Ophiostoma novo-ulmi</i> ssp. <i>americana</i> Colonizing Resistant or Sensitive Genotypes of American Elm |
| title_sort | comparative analysis of transcriptomes of i ophiostoma novo ulmi i ssp i americana i colonizing resistant or sensitive genotypes of american elm |
| topic | Dutch elm disease <i>Ophiostoma novo-ulmi</i> RNA-Seq pathogenicity virulence mutants |
| url | https://www.mdpi.com/2309-608X/8/6/637 |
| work_keys_str_mv | AT marthanigg comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT thaiscdeoliveira comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT jorgelsarmientovillamil comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT paulydelabastide comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT willehintz comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT sherifmsherif comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT mukundshukla comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT louisbernier comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm AT praveenksaxena comparativeanalysisoftranscriptomesofiophiostomanovoulmiisspiamericanaicolonizingresistantorsensitivegenotypesofamericanelm |