Dutch Elm Disease in the 21st Century

A special issue of Journal of Fungi (ISSN 2309-608X).

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 15203

Special Issue Editors


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Guest Editor
Centre for Forest Research and Institute for Integrative and Systems Biology, Université Laval, 1030 Avenue de la Médecine, Québec, QC, Canada
Interests: forest pathology; tree–fungus interactions; dutch elm disease; ophiostomatales; fungal genomics

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Guest Editor
Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, BOX 49, 23053 Alnarp, Sweden
Interests: forest pathology; tree resistance; fungal endophytes; invasive pathogens; sustainable forest management
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Special Issue Information

Dear Colleagues,

Dutch elm disease (DED) was first recorded in 1919 and was rapidly recognized to be of fungal origin by scientists at the Willie Commelin Scholten laboratory who fulfilled Koch’s postulates. Within the next 100 years, two successive pandemics of DED killed hundreds of millions of elms native to Europe, western Asia, and North America. The pandemics were caused by the Ascomycetes Ophiostoma ulmi and O. novo-ulmi after they had been acquired by elm bark beetles. The advent of O. novo-ulmi was a landmark event in the evolution of DED as this very aggressive pathogen is also highly fit and has rapidly displaced the less aggressive O. ulmi.

This Special Issue will be a combination of original research works and review articles with particular emphasis on the biology, ecology, and molecular genetics of DED fungi and elms – thereby advancing our understanding of these tree pathogens that are still impacting elm populations worldwide

Prof. Dr. Louis Bernier
Dr. Johanna Witzell
Guest Editors

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Keywords

  • Ophiostoma spp.
  • Ulmus spp.
  • genomics
  • fungal biology
  • ecology
  • plant–pathogen interactions
  • integrated pest management

Published Papers (6 papers)

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Research

12 pages, 3135 KiB  
Article
Vaccination of Elms against Dutch Elm Disease—Are the Associated Epiphytes and Endophytes Affected?
by Johanna Witzell, Caroline Sunnerstam and Tobias Hansson
J. Fungi 2023, 9(3), 297; https://doi.org/10.3390/jof9030297 - 24 Feb 2023
Viewed by 1406
Abstract
Dutch elm disease (DED) is causing extensive mortality of ecologically and culturally valuable elm trees (Ulmus spp.). Treatment of elms with the biological vaccine Dutch Trig® has been found to provide effective protection against DED by stimulating the defensive mechanisms of [...] Read more.
Dutch elm disease (DED) is causing extensive mortality of ecologically and culturally valuable elm trees (Ulmus spp.). Treatment of elms with the biological vaccine Dutch Trig® has been found to provide effective protection against DED by stimulating the defensive mechanisms of the trees. We hypothesized that the same mechanisms could also affect non-target organisms associated with elms. We explored the possible effects of vaccination on epiphytes (mainly lichens) and fungal endophytes living in the bark and young xylem of treated elms. Epiphyte cover percentage was assessed visually using a grid placed on the trunks, and a culture-based approach was used to study endophytes. Epiphyte cover was lower on the trunks of vaccinated trees as compared with unvaccinated trees, but the difference was not statistically significant. The presence of slow-growing and uncommon endophytes seemed to be reduced in continuously vaccinated elms; however, the highest endophyte diversity was found in elms four years after cessation of the vaccination treatments. Our findings suggest that although vaccination may shape epiphyte and endophyte communities in elms, its impacts are not straightforward. More detailed studies are, therefore, needed to inform the sustainable application of the vaccine as a part of the integrated management of DED. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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20 pages, 2682 KiB  
Article
Independent Evolution Has Led to Distinct Genomic Signatures in Dutch Elm Disease-Causing Fungi and Other Vascular Wilts-Causing Fungal Pathogens
by Anna Fijarczyk, Louis Bernier, Monique L. Sakalidis, Carmen M. Medina-Mora and Ilga Porth
J. Fungi 2023, 9(1), 2; https://doi.org/10.3390/jof9010002 - 20 Dec 2022
Cited by 1 | Viewed by 1836
Abstract
Vascular wilts are important diseases caused by plant pathogenic fungi that result in the rapid death of their plant hosts. This is due to a systemic defense mechanism whereby the plant induces the compartmentalization of the infected vascular system in order to reduce [...] Read more.
Vascular wilts are important diseases caused by plant pathogenic fungi that result in the rapid death of their plant hosts. This is due to a systemic defense mechanism whereby the plant induces the compartmentalization of the infected vascular system in order to reduce the propagation of the fungus. The ascomycete class Sordariomycetes contains several species that cause vascular wilts in diverse plant hosts, and they can be classified into four taxonomic orders. The genetic mechanisms of pathogenesis have already been investigated in Fusarium and Verticillium species, but they have not yet been compared with other well-known wilt-causing species, especially fungi causing oak wilt or Dutch elm disease (DED). Here we analyzed 20 whole genome assemblies of wilt-causing fungi together with 56 other species using phylogenetic approaches to trace expansions and contractions of orthologous gene families and gene classes related to pathogenicity. We found that the wilt-causing pathogens evolved seven times, experiencing the largest fold changes in different classes of genes almost every time. However, some similarities exist across groups of wilt pathogens, particularly in Microascales and Ophiostomatales, and these include the common gains and losses of genes that make up secondary metabolite clusters (SMC). DED pathogens do not experience large-scale gene expansions, with most of the gene classes, except for some SMC families, reducing in number. We also found that gene family expansions in the most recent common ancestors of wilt pathogen groups are enriched for carbohydrate metabolic processes. Our study shows that wilt-causing species evolve primarily through distinct changes in their repertoires of pathogenicity-related genes and that there is the potential importance of carbohydrate metabolism genes for regulating osmosis in those pathogens that penetrate the plant vascular system. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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23 pages, 3243 KiB  
Article
Comparative Analysis of Transcriptomes of Ophiostoma novo-ulmi ssp. americana Colonizing Resistant or Sensitive Genotypes of American Elm
by 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 and Praveen K. Saxena
J. Fungi 2022, 8(6), 637; https://doi.org/10.3390/jof8060637 - 16 Jun 2022
Cited by 5 | Viewed by 2940
Abstract
The Ascomycete Ophiostoma novo-ulmi threatens elm populations worldwide. The molecular mechanisms underlying its pathogenicity and virulence are still largely uncharacterized. As part of a collaborative study of the O. novo-ulmi-elm interactome, we analyzed the O. novo-ulmi ssp. americana transcriptomes obtained by deep [...] Read more.
The Ascomycete Ophiostoma novo-ulmi threatens elm populations worldwide. The molecular mechanisms underlying its pathogenicity and virulence are still largely uncharacterized. As part of a collaborative study of the O. novo-ulmi-elm interactome, we analyzed the O. novo-ulmi ssp. americana transcriptomes obtained by deep sequencing of messenger RNAs recovered from Ulmus americana 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 O. novo-ulmi 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 O. novo-ulmi genes. Although mutants remained virulent towards U. americana saplings, we identified a large repertoire of additional candidate O. novo-ulmi pathogenicity genes for functional validation by loss-of-function approaches. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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15 pages, 2265 KiB  
Article
Different Responses in Vascular Traits between Dutch Elm Hybrids with a Contrasting Tolerance to Dutch Elm Disease
by Michal Moravčík, Miroslava Mamoňová, Vladimír Račko, Ján Kováč, Miloň Dvořák, Jana Krajňáková and Jaroslav Ďurkovič
J. Fungi 2022, 8(3), 215; https://doi.org/10.3390/jof8030215 - 22 Feb 2022
Cited by 2 | Viewed by 2012
Abstract
The ascomycetous fungus Ophiostoma novo-ulmi is the causative agent of the current Dutch elm disease (DED) pandemic, which has ravaged many tens of millions of European and North American elm trees. Host responses in vascular traits were studied in two Dutch elm hybrids, [...] Read more.
The ascomycetous fungus Ophiostoma novo-ulmi is the causative agent of the current Dutch elm disease (DED) pandemic, which has ravaged many tens of millions of European and North American elm trees. Host responses in vascular traits were studied in two Dutch elm hybrids, ‘Groeneveld’ and ‘Dodoens’, which show different vascular architecture in the secondary xylem and possess contrasting tolerances to DED. ‘Groeneveld’ trees, sensitive to DED, possessed a high number of small earlywood vessels. However, these trees showed a poor response to DED infection for the earlywood vascular characteristics. Following infection, the proportion of least vessels with a vessel lumen area less than 2500 µm2 decreased from 65.4% down to 53.2%. A delayed response in the increasing density of vessels showing a reduced size in the latewood prevented neither the rapid fungal spread nor the massive colonisation of the secondary xylem tissues resulting in the death of the infected trees. ‘Dodoens’ trees, tolerant to DED, possessed a low number of large earlywood vessels and showed a prominent and fast response to DED infection. Vessel lumen areas of newly formed earlywood vessels were severely reduced together with the vessel size : number ratio. Following infection, the proportion of least vessels with a vessel lumen area less than 2500 µm2 increased from 75.6% up to 92.9%. A trend in the increasing density of vessels showing a reduced size was maintained not only in the latewood that was formed in the year of infection but also in the earlywood that was formed in the consecutive year. The occurrence of fungal hyphae in the earlywood vessels that were formed a year following the infection was severely restricted, as revealed by X-ray micro-computed tomography imaging. Possible reasons responsible for a contrasting survival of ‘Groeneveld’ and ‘Dodoens’ trees are discussed. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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18 pages, 4533 KiB  
Article
Deciphering the Genome-Wide Transcriptomic Changes during Interactions of Resistant and Susceptible Genotypes of American Elm with Ophiostoma novo-ulmi
by Md Tabibul Islam, Jose Freixas Coutin, Mukund Shukla, Amandeep Kaur Dhaliwal, Martha Nigg, Louis Bernier, Sherif M. Sherif and Praveen K. Saxena
J. Fungi 2022, 8(2), 120; https://doi.org/10.3390/jof8020120 - 26 Jan 2022
Cited by 8 | Viewed by 2733
Abstract
Dutch elm disease (DED), caused by Ophiostoma novo-ulmi (Onu), is a destructive disease of American elm (Ulmus americana L.). The molecular mechanisms of resistance and susceptibility against DED in American elm are still largely uncharacterized. In the present study, we [...] Read more.
Dutch elm disease (DED), caused by Ophiostoma novo-ulmi (Onu), is a destructive disease of American elm (Ulmus americana L.). The molecular mechanisms of resistance and susceptibility against DED in American elm are still largely uncharacterized. In the present study, we performed a de novo transcriptome (RNA-sequencing; RNA-Seq) assembly of U. americana and compared the gene expression in a resistant genotype, ’Valley Forge’, and a susceptible (S) elm genotype at 0 and 96 h post-inoculation of Onu. A total of 85,863 non-redundant unigenes were identified. Compared to the previously characterized U. minor transcriptome, U. americana has 35,290 similar and 55,499 unique genes. The transcriptomic variations between ‘Valley Forge’ and ‘S’ were found primarily in the photosynthesis and primary metabolism, which were highly upregulated in the susceptible genotype irrespective of the Onu inoculation. The resistance to DED was associated with the activation of RPM1-mediated effector-triggered immunity that was demonstrated by the upregulation of genes involved in the phenylpropanoids biosynthesis and PR genes. The most significantly enriched gene ontology (GO) terms in response to Onu were response to stimulus (GO:0006950), response to stress (GO:0050896), and secondary metabolic process (GO:0008152) in both genotypes. However, only in the resistant genotype, the defense response (GO:0006952) was among the topmost significantly enriched GO terms. Our findings revealed the molecular regulations of DED resistance and susceptibility and provide a platform for marker-assisted breeding of resistant American elm genotypes. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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21 pages, 25100 KiB  
Article
Priming of Plant Defenses against Ophiostoma novo-ulmi by Elm (Ulmus minor Mill.) Fungal Endophytes
by Clara Martínez-Arias, Juan Sobrino-Plata, Luis Gil, Jesús Rodríguez-Calcerrada and Juan Antonio Martín
J. Fungi 2021, 7(9), 687; https://doi.org/10.3390/jof7090687 - 25 Aug 2021
Cited by 15 | Viewed by 2635
Abstract
Some fungal endophytes of forest trees are recognized as beneficial symbionts against stresses. In previous works, two elm endophytes from the classes Cystobasidiomycetes and Eurotiomycetes promoted host resistance to abiotic stress, and another elm endophyte from Dothideomycetes enhanced host resistance to Dutch elm [...] Read more.
Some fungal endophytes of forest trees are recognized as beneficial symbionts against stresses. In previous works, two elm endophytes from the classes Cystobasidiomycetes and Eurotiomycetes promoted host resistance to abiotic stress, and another elm endophyte from Dothideomycetes enhanced host resistance to Dutch elm disease (DED). Here, we hypothesize that the combined effect of these endophytes activate the plant immune and/or antioxidant system, leading to a defense priming and/or increased oxidative protection when exposed to the DED pathogen Ophiostoma novo-ulmi. To test this hypothesis, the short-term defense gene activation and antioxidant response were evaluated in DED-susceptible (MDV1) and DED-resistant (VAD2 and MDV2.3) Ulmus minor genotypes inoculated with O. novo-ulmi, as well as two weeks earlier with a mixture of the above-mentioned endophytes. Endophyte inoculation induced a generalized transient defense activation mediated primarily by salicylic acid (SA). Subsequent pathogen inoculation resulted in a primed defense response of variable intensity among genotypes. Genotypes MDV1 and VAD2 displayed a defense priming driven by SA, jasmonic acid (JA), and ethylene (ET), causing a reduced pathogen spread in MDV1. Meanwhile, the genotype MDV2.3 showed lower defense priming but a stronger and earlier antioxidant response. The defense priming stimulated by elm fungal endophytes broadens our current knowledge of the ecological functions of endophytic fungi in forest trees and opens new prospects for their use in the biocontrol of plant diseases. Full article
(This article belongs to the Special Issue Dutch Elm Disease in the 21st Century)
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