Molecular pathology of forest trees for a long time lagged behind parallel studies on agricultural crop pathology. Recent technological advances have significantly contributed to the observed progress in this field. The first powerful impulse was provided by the completion of the black cottonwood genome sequence in 2006. Genomes of several other important tree species will be completed within a short time. Simultaneously, application of transcriptomics and next-generation sequencing (NGS) has resulted in the rapid accumulation of a vast amount of data on molecular interactions between trees and their microbial parasites. This review provides an overview of our current knowledge about these responses of forest trees to their pathogens, highlighting the achievements of the past decade, discussing the current state of the field, and emphasizing the prospects and challenges for the near future.
Summary At the end of the cell cycle, the plant cell wall is deposited within a membrane compartment referred to as the cell plate. Little is known about the biogenesis of this transient membrane compartment. We have positionally cloned and characterized a novel Arabidopsis gene, CLUB, identified by mutation. CLUB/AtTRS130 encodes a putative TRAPPII tethering factor. club mutants are seedling‐lethal and have a canonical cytokinesis‐defective phenotype, characterized by the appearance of bi‐ or multinucleate cells with cell wall stubs, gaps and floating walls. Confocal microscopy showed that in club mutants, KNOLLE‐positive vesicles formed and accumulated at the cell equator throughout cytokinesis, but failed to assemble into a cell plate. Similarly, electron micrographs showed large vesicles loosely connected as patchy, incomplete cell plates in club root tips. Neither the formation of KNOLLE‐positive vesicles nor the delivery of these vesicles to the cell equator appeared to be perturbed in club mutants. Thus, the primary defect in club mutants appears to be an impairment in cell plate assembly. As a putative tethering factor required for cell plate biogenesis, CLUB/AtTRS130 helps to define the identity of this membrane compartment and comprises an important handle on the regulation of cell plate assembly.
BackgroundDuring their lifetime, conifer trees are exposed to numerous herbivorous insects. To protect themselves against pests, trees have developed a broad repertoire of protective mechanisms. Many of the plant’s defence reactions are activated upon an insect attack, and the underlying regulatory mechanisms are not entirely understood yet, in particular in conifer trees. Here, we present the results of our studies on the transcriptional response and the volatile compounds production of Scots pine (Pinus sylvestris) upon the large pine weevil (Hylobius abietis) feeding.ResultsTranscriptional response of Scots pine to the weevil attack was investigated using a novel customised 36.4 K Pinus taeda microarray. The weevil feeding caused large-scale changes in the pine transcriptome. In total, 774 genes were significantly up-regulated more than 4-fold (p ≤ 0.05), whereas 64 genes were significantly down-regulated more than 4-fold. Among the up-regulated genes, we could identify genes involved in signal perception, signalling pathways, transcriptional regulation, plant hormone homeostasis, secondary metabolism and defence responses. The weevil feeding on stem bark of pine significantly increased the total emission of volatile organic compounds from the undamaged stem bark area. The emission levels of monoterpenes and sesquiterpenes were also increased. Interestingly, we could not observe any correlation between the increased production of the terpenoid compounds and expression levels of the terpene synthase-encoding genes.ConclusionsThe obtained data provide an important insight into the transcriptional response of conifer trees to insect herbivory and illustrate the massive changes in the host transcriptome upon insect attacks. Moreover, many of the induced pathways are common between conifers and angiosperms. The presented results are the first ones obtained by the use of a microarray platform with an extended coverage of pine transcriptome (36.4 K cDNA elements). The platform will further facilitate the identification of resistance markers with the direct relevance for conifer tree breeding.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1546-9) contains supplementary material, which is available to authorized users.
Scots pine (Pinus sylvestris) secretes a number of small, highly-related, disulfide-rich proteins (Sp-AMPs) in response to challenges with fungal pathogens such as Heterobasidion annosum, although their biological role has been unknown. Here, we examined the expression patterns of these genes, as well as the structure and function of the encoded proteins. Northern blots and quantitative real time PCR showed increased levels of expression that are sustained during the interactions of host trees with pathogens, but not non-pathogens, consistent with a function in conifer tree defenses. Furthermore, the genes were up-regulated after treatment with salicylic acid and an ethylene precursor, 1-aminocyclopropane-1-carboxylic-acid, but neither methyl jasmonate nor H 2 O 2 induced expression, indicating that Sp-AMP gene expression is independent of the jasmonic acid signaling pathways. The cDNA encoding one of the proteins was cloned and expressed in Pichia pastoris. The purified protein had antifungal activity against H. annosum, and caused morphological changes in its hyphae and spores. It was directly shown to bind soluble and insoluble β-(1,3)-glucans, specifically and with high affinity. Furthermore, addition of exogenous glucan is linked to higher levels of Sp-AMP expression in the conifer. Homology modeling and sequence comparisons suggest that a conserved patch on the surface of the globular Sp-AMP is a carbohydrate-binding site that can accommodate approximately four sugar units. We conclude that these proteins belong to a new family of antimicrobial proteins that are likely to act by binding the glucans that are a major component of fungal cell walls.
Root and butt rot caused by members of the Heterobasidion annosum species complex is the most economically important disease of conifer trees in boreal forests. Wood decay in the infected trees dramatically decreases their value and causes considerable losses to forest owners. Trees vary in their susceptibility to Heterobasidion infection, but the genetic determinants underlying the variation in the susceptibility are not well-understood. We performed the identification of Norway spruce genes associated with the resistance to Heterobasidion parviporum infection using genome-wide exon-capture approach. Sixty-four clonal Norway spruce lines were phenotyped, and their responses to H. parviporum inoculation were determined by lesion length measurements. Afterwards, the spruce lines were genotyped by targeted resequencing and identification of genetic variants (SNPs). Genome-wide association analysis identified 10 SNPs located within 8 genes as significantly associated with the larger necrotic lesions in response to H. parviporum inoculation. The genetic variants identified in our analysis are potential marker candidates for future screening programs aiming at the differentiation of disease-susceptible and resistant trees.
Heterobasidion annosum is widely known as a major root and butt rot pathogen of conifer trees, but little information is available on its interaction with the roots of herbaceous angiosperm plants. We investigated the infection biology of H. annosum during challenge with the angiosperm model Arabidopsis and monitored the host response after exposure to different hormone elicitors, chemicals (chitin, glucan and chitosan) and fungal species that represent diverse basidiomycete life strategies [e.g., pathogen (H. annosum), saprotroph (Stereum sanguinolentum) and mutualist (Lactarius rufus)]. The results revealed that the tree pathogen (H. annosum) and the saprotroph (S. sanguinolentum) could infect the Col-8 (Columbia) ecotype of Arabidopsis in laboratory inoculation experiments. Germinated H. annosum spores had appressorium-like penetration structures attached to the surface of the Arabidopsis roots. Subsequent invasive fungal growth led to the disintegration of the vascular region of the root tissues. Progression of root rot symptoms in Arabidopsis was similar to the infection development that was previously documented in Scots pine seedlings. Scots pine PsDef1 and Arabidopsis DEFLs (AT5G44973.1) and PDF1.2 were induced at the initial stage of the infection. However, differences in the expression patterns of the defensin gene homologs from the two plant groups were observed under various conditions, suggesting functional differences in their regulation. The potential use of the H. annosum-Arabidopsis pathosystem as a model for studying forest tree diseases is discussed.
In the forest of Northern Hemisphere, the fungi Heterobasidion annosum sensu lato cause severe root and stem rot diseases, dramatically reducing the wood quality of conifer trees. The hallmark of the host response during the infection process is the formation of necrotic lesions and reaction zones. To characterize physiochemical and molecular features of the necrotic lesion, we conducted artificial inoculations on Norway spruce plants at different developmental stages: seedlings, young and mature trees. The results were further compared against data available on the formation of reaction zones. Strong necrosis browning or enlarged necrotic lesions were observed in infected tissues. This was accompanied by elevated pH. However, the increased pH, around 6.0 in necrotic lesions was not as high as that documented in reaction zones, above 7.0 as marked by the intensity of the blue colour in response to 2,6-dichlorophenol indophenol dye. Peroxidase activity increased in infected plants and RNA-seq analysis of necrotic lesions showed marked up-regulation of defense-related genes. Our findings highlight similarities and differences between the reaction zone and necrotic lesion formation in response of conifer trees to biotic stress.
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