Deciphering the Genome-Wide Transcriptomic Changes during Interactions of Resistant and Susceptible Genotypes of American Elm with Ophiostoma novo-ulmi.

Md Tabibul Islam,Louis Bernier,Amandeep Kaur Dhaliwal,Sherif M Sherif,Martha Nigg,Jose Freixas Coutin,Mukund Shukla,Praveen K Saxena

doi:10.3390/jof8020120

Md Tabibul Islam, Louis Bernier + Show 6 more

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https://doi.org/10.3390/jof8020120

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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 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.

Highlights

Ophiostoma species (i.e., Ophiostoma novo-ulmi and Ophiostoma ulmi) are the fungal pathogens causing Dutch elm disease (DED), which is a lethal vascular wilt disease of elms worldwide including American elm (Ulmus americana) [1,2]
In North America, overland spread of DED from infected to healthy elms is facilitated by the native elm bark beetle (Hylurgopinus rufipes) and its European counterpart (Scolytus multistriatus), and the symptoms first appear on upper crown branches as wilting and yellowing leaves [4,5,6]
The plants of American elm genotypes with contrasting resistance to DED were inoculated with yeast spores of O. novo-ulmi (Onu), which germinated within the stem, where hyphae grew and spread through xylem vessels, inducing their cavitational embolism [30,31]

Summary

Introduction

Ophiostoma species (i.e., Ophiostoma novo-ulmi and Ophiostoma ulmi) are the fungal pathogens causing Dutch elm disease (DED), which is a lethal vascular wilt disease of elms worldwide including American elm (Ulmus americana) [1,2]. In North America, overland spread of DED from infected to healthy elms is facilitated by the native elm bark beetle (Hylurgopinus rufipes) and its European counterpart (Scolytus multistriatus), and the symptoms first appear on upper crown branches as wilting and yellowing leaves [4,5,6]. When the bark is peeled off infected branches, longitudinal, brown-colored streaks in the outer rings of the sapwood are visible, and it is the most distinctive symptom of DED observed in the field. These fungi spread within stems and roots of living elms both by passive transport of spores and by the mycelial growth of colonies initiated by spores that germinate in the xylem. Dutch elm disease fungi can infect healthy elms adjacent to a diseased elm through root grafts [7,8]

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