Comparative Gene Expression Analysis Reveals Mechanism of Pinus contorta Response to the Fungal Pathogen Dothistroma septosporum

Abstract

Many conifers have distributions that span wide ranges in both biotic and abiotic conditions, but the basis of response to biotic stress has received much less attention than response to abiotic stress. In this study, we investigated the gene expression response of lodgepole pine (Pinus contorta) to attack by the fungal pathogen Dothistroma septosporum, which causes Dothistroma needle blight (DNB), a disease that has caused severe climate-related outbreaks in northwestern British Columbia. We inoculated tolerant and susceptible pines with two D. septosporum isolates and analyzed the differentially expressed genes, differential exon usage, and co-expressed gene modules using RNA-seq data. We found a rapid and strong transcriptomic response in tolerant lodgepole pine samples inoculated with one D. septosporum isolate, and a late and weak response in susceptible samples inoculated with another isolate. We mapped 43 of the DEG- or gene-module-identified genes to the reference plant-pathogen interaction pathway deposited in KEGG database. These genes are present in PAMP-triggered and effector-triggered immunity pathways. Genes comprising pathways and gene modules had signatures of strong selective constraint, while the highly expressed genes in tolerant samples appear to have been favored by selection to counterattack the pathogen. We identified candidate resistance genes that may respond to D. septosporum effectors. Taken together, our results show that gene expression response to D. septosporum infection in lodgepole pine varies both among tree genotypes and pathogen strains, and involves both known candidate genes and a number of genes with previously unknown functions.

Apoplastic effector candidates of a foliar forest pathogen trigger cell death in host and non-host plants

“…Importantly, the high level of conservation of effectors across fungal taxa, and conservation of plant responses across angiosperms and gymnosperms suggests that much of what the scientific community has learned about plant-pathogen interactions involving angiosperm systems may also be relevant to gymnosperms. A similar conclusion was reached by studying pine responses to D. septosporum infection 37 . There also appear to be common 'core' interactions that could be exploited to give broad host-range resistance.…”

“…Although screening with pathogen effectors based on genome data (effectoromics) has fast-tracked identification of resistant angiosperm crop varieties with corresponding immune receptors, it is not known whether a similar effectoromics-based approach could be applied to improve forest health given the longer life-cycles of forest trees, and the complexity of factors affecting disease resistance 36 . However, a recent transcriptomics study of Pinus contorta responses to infection with D. septosporum showed up-regulation of pine genes involved in Ca 2+ and MAPK defence signalling pathways as well as pathogen-specific defence responses 37 . Signatures of selection were identified in candidate immune receptors ( R genes), suggesting adaptation to the pathogen and the importance of specific interactions between pathogen effectors and host immune receptors in pine defence to D. septosporum .…”

Apoplastic effector candidates of a foliar forest pathogen trigger cell death in host and non-host plants

“…Importantly, the high level of conservation of effectors across fungal taxa, and conservation of plant responses across angiosperms and gymnosperms suggests that much of what the scientific community has learned about plant-pathogen interactions involving angiosperm systems may also be relevant to gymnosperms. A similar conclusion was reached by studying pine responses to D. septosporum infection 23 . There also appear to be common ‘core’ interactions that could be exploited to give broad host-range resistance.…”

“…Although screening with pathogen effectors based on genome data (effectoromics) has fast-tracked identification of resistant angiosperm crop varieties with corresponding immune receptors, it is not known whether a similar effectoromics-based approach could be applied to improve forest health given the longer life-cycles of forest trees, and the complexity of factors affecting disease resistance 38 . However, a recent transcriptomics study of Pinus contorta responses to infection with D. septosporum showed up-regulation of pine genes involved in Ca 2+ and MAPK defence signalling pathways as well as pathogen-specific defence responses 23 . Signatures of selection were identified in candidate immune receptors ( R genes), suggesting adaptation to the pathogen and the importance of specific interactions between pathogen effectors and host immune receptors in pine defence to D. septosporum .…”

“…The extracellular D. septosporum effector Ecp2-1 was recently suggested to be an avirulence factor which elicits defence responses in pine 22 . A recent study of Pinus contorta defence responses to D. septosporum 23 identified upregulation of pine genes associated with IP-triggered immunity, and candidate immune receptor ( R ) genes showing positive selection, strongly suggesting the importance of D. septosporum effectors in triggering host defence. Here, we focused on candidate apoplastic effectors of D. septosporum that might be involved in a successful infection and/or triggering host defence.…”