Biography

From an early age I have been curious about how and why thing work the way they do. I also found plants fascinating as they contribute so much to our lives: food, oxygen, shelter, medicines. I am particularly interested in plant secondary metabolism and how these metabolites contribute to plant success and human enjoyment of them.  During my PhD at the Univeristy of Florida I worked on characterizing the biosynthesis pathways of molecules that contribute to tomato flavor. I then moved to the University of British Columbia where I began researching spruce defense again insect pest and the biosynthesis of defense compounds. After receiving a Young Researcher Talent grant from the Norwegian Research Council, I came to NIBIO to study the molecular mechanism of spruce defense priming. Expertise: plant defense, molecular biology, plant biochemistry, functional genomics

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Abstract

Nursery-grown Norway spruce Picea abies seedlings are often heavily attacked by the pine weevil Hylobius abietis on clear-cuts the first years after planting. Because the seedlings are not resource-limited during the growing phase in the nursery they are expected to invest less in defence than naturally regenerated seedlings already present on the clear-cuts. The latter have had to cope with various environmental stressors that could make them invest more in defence. We tested if naturally regenerated plants have stronger chemical defences than nursery-grown plants. Nursery-grown plants were planted in-between naturally regenerated plants on fresh clear cuts, and phenolic and terpene compounds in the stem bark were measured after one growing season. To test both constitutive and inducible defences, plants were either wounded, painted with methyl jasmonate (MeJA) to induce defences, or given a combination of both treatments. Growth and pine weevil attacks of the plants were registered. Nursery-grown plants had higher total concentrations of phenolic compounds and lower concentrations of terpenes than naturally regenerated plants. These opposite responses were reflected in very different compound profiles in the two plant types. We suggest the differences between plant types to be results of differences in plant age, stress level, genetic origin or possibly a combination of these factors. Most compounds showed no response to wounding, MeJA-treatment or wounding and MeJA-treatment combined, but the terpenes 3-carene, eucalyptol, limonene and para-cymene had higher concentrations in MeJA-treated nursery-grown plants than in control plants. These compounds are known to be effective in conifer resistance against weevils and bark beetles. Overall, 27% of our 400 study plants had signs of pine weevil damage after 3 ½ months in the field. However, treatment or plant type had no significant effect on whether plants were attacked or not and this might have been a result of the relatively low overall level of attacks in this study. Further studies are needed to disentangle the importance of plant age, stress level, genetic origin and resource availability for chemical defence mechanisms of young Norway spruce plants, as strengthening the natural resistance of nursery plants may be increasingly important in a future with less pesticide use.

Abstract

Methyl jasmonate (MeJA) treatment elicits induced resistance (IR) against pests and diseases in Norway spruce (Picea abies). We recently demonstrated using mRNA-seq that this MeJA-IR is associated with both a prolonged upregulation of inducible defenses and defense priming. Gene expression can be regulated at both a transcrip-tional and post-transcriptional level by small RNAs, including microRNAs (miRNAs). Here we explore the effects of MeJA treatment and subsequent challenge by wounding on the Norway spruce miRNA transcriptome. We found clusters of prolonged down- or upregulated miRNAs as well as miRNAs whose expression was primed after MeJA treatment and subsequent wounding challenge. Differentially expressed miRNAs included miR160, miR167, miR172, miR319, and the miR482/2118 superfamily. The most prominent mRNA targets predicted to be differentially expressed by miRNA activity belonged to the nucleotide-binding site leucine-rich repeat (NBS- LRR) family. Among other predicted miRNA targets were genes regulating jasmonic acid biosynthesis. Our re-sults indicate that miRNAs have an important role in the regulation of MeJA-IR in Norway spruce.

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Abstract

We review a recently discovered white spruce (Picea glauca) chemical defense against spruce budworm (Choristoneura fumiferana) involving hydroxyacetophenones. These defense metabolites detected in the foliage accumulate variably as the aglycons, piceol and pungenol, or the corresponding glucosides, picein and pungenin. We summarize current knowledge of the genetic, genomic, molecular, and biochemical underpinnings of this defense and its effects on C. fumiferana. We present an update with new results on the ontogenic variation and the phenological window of this defense, including analysis of transcript responses in P. glauca to C. fumiferana herbivory. We also discuss this chemical defense from an evolutionary and a breeding context.

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Abstract

In response to various stimuli, plants acquire resistance against pests and/or pathogens. Such acquired or induced resistance allows plants to rapidly adapt to their environment. Spraying the bark of mature Norway spruce (Picea abies) trees with the phytohormone methyl jasmonate (MeJA) enhances resistance to tree‐killing bark beetles and their associated phytopathogenic fungi. Analysis of spruce chemical defenses and beetle colonization success suggests that MeJA treatment both directly induces immune responses and primes inducible defenses for a faster and stronger response to subsequent beetle attack. We used metabolite and transcriptome profiling to explore the mechanisms underlying MeJA‐induced resistance in Norway spruce. We demonstrated that MeJA treatment caused substantial changes in the bark transcriptional response to a triggering stress (mechanical wounding). Profiling of mRNA expression showed a suite of spruce inducible defenses are primed following MeJA treatment. Although monoterpenes and diterpene resin acids increased more rapidly after wounding in MeJA‐treated than control bark, expression of their biosynthesis genes did not. We suggest that priming of inducible defenses is part of a complex mixture of defense responses that underpins the increased resistance against bark beetle colonization observed in Norway spruce. This study provides the most detailed insights yet into the mechanisms underlying induced resistance in a long‐lived gymnosperm.

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Abstract

Plants can form an immunological memory known as defense priming, whereby exposure to a priming stimulus enables quicker or stronger response to subsequent attack by pests and pathogens. Such priming of inducible defenses provides increased protection and reduces allocation costs of defense. Defense priming has been widely studied for short‐lived model plants such as Arabidopsis, but little is known about this phenomenon in long‐lived plants like spruce. We compared the effects of pretreatment with sublethal fungal inoculations or application of the phytohormone methyl jasmonate (MeJA) on the resistance of 48‐year‐old Norway spruce (Picea abies) trees to mass attack by a tree‐killing bark beetle beginning 35 days later. Bark beetles heavily infested and killed untreated trees but largely avoided fungus‐inoculated trees and MeJA‐treated trees. Quantification of defensive terpenes at the time of bark beetle attack showed fungal inoculation induced 91‐fold higher terpene concentrations compared with untreated trees, whereas application of MeJA did not significantly increase terpenes. These results indicate that resistance in fungus‐inoculated trees is a result of direct induction of defenses, whereas resistance in MeJA‐treated trees is due to defense priming. This work extends our knowledge of defense priming from model plants to an ecologically important tree species.

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Abstract

As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.

Abstract

Bark beetles and their symbiotic bluestain fungi kill more trees than all other natural factors and cause great economic losses in Norway spruce and other conifers. The tree's natural defenses are the most important factor maintaining bark beetle-fungus complexes at low, endemic levels. Spraying Norway spruce trees with the plant hormone methyl jasmonate (MeJA) primes tree defenses without eliciting notable induced defenses, but enables the trees to respond much more quickly and strongly when challenged by bark beetles or fungi several weeks after treatment. This phenomenon, known as defense priming, is a form of acquired resistance that enables cost-effective and vigorous defense responses. In field experiments with 50-year-old clonal spruce trees terpene concentrations in the bark increased 60-fold within 24 h after mechanical wounding of MeJA primed trees, compared with a 13-fold increase in unprimed control trees. We also observed altered transcriptional patterns in primed trees using Illumina deep transcriptome sequencing. When wounded, primed trees launched vigorous induced defenses with significant differential regulation of gene transcripts, such as those involved in phenylpropanoid synthesis leading to lignification. Resistance-like genes, such as the NB-LRR coding genes, are also more rapidly induced in primed than in unprimed trees. Transcriptome results from primed but unwounded trees indicate an alteration in the state of the chromatin, resembling changes associated with the activity of the epigenetic machinery creating long-lasting epigenetic marks. We do not know yet how long the primed state is activated in Norway spruce, but our data so far indicate that it may last for at least 3 years.

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Abstract

Acetophenones are phenolic metabolites of plant species. A metabolic route for the biosynthesis and release of 2 defence‐related hydroxyacetophenones in white spruce (Picea glauca) was recently proposed to involve 3 phases: (a) biosynthesis of the acetophenone aglycons catalysed by a currently unknown set of enzymes, (b) formation and accumulation of the corresponding glycosides catalysed by a glucosyltransferase, and (c) release of the aglycons catalysed by a glucosylhydrolase (PgβGLU‐1). We tested if this biosynthetic model is conserved across Pinaceae and land plant species. We assayed and surveyed the literature and sequence databases for possible patterns of the presence of the acetophenone aglycons piceol and pungenol and their glucosides, as well as sequences and expression of Pgβglu‐1 orthologues. In the Pinaceae, the 3 phases of the biosynthetic model are present and differences in expression of Pgβglu‐1 gene orthologues explain some of the interspecific variation in hydroxyacetophenones. The phylogenetic signal in the metabolite phenotypes was low across species of 6 plant divisions. Putative orthologues of PgβGLU‐1 do not form a monophyletic group in species producing hydroxyacetophenones. The biosynthetic model for acetophenones appears to be conserved across Pinaceae, whereas convergent evolution has led to the production of acetophenone glucosides across land plants.

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Abstract

Acetophenones are phenolic compounds involved in the resistance of white spruce (Picea glauca) against spruce budworm (Choristoneura fumiferiana), a major forest pest in North America. The acetophenones pungenol and piceol commonly accumulate in spruce foliage in the form of the corresponding glycosides, pungenin and picein. These glycosides appear to be inactive against the insect but can be cleaved by a spruce b-glucosidase, PgbGLU-1, which releases the active aglycons. The reverse glycosylation reaction was hypothesized to involve a family 1 UDP-sugar dependent glycosyltransferase (UGT) to facilitate acetophenone accumulation in the plant. Metabolite and transcriptome profiling over a developmental time course of white spruce bud burst and shoot growth revealed two UGTs, PgUGT5 and PgUGT5b, that glycosylate pungenol. Recombinant PgUGT5b enzyme produced mostly pungenin, while PgUGT5 produced mostly isopungenin. Both UGTs also were active in vitro on select flavonoids. However, the context of transcript and metabolite accumulation did not support a biological role in flavonoid metabolism but correlated with the formation of pungenin in growing shoots. Transcript levels of PgUGT5b were higher than those of PgUGT5 in needles across different genotypes of white spruce. These results support a role of PgUGT5b in the biosynthesis of the glycosylated acetophenone pungenin in white spruce.

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Abstract

Plants are sessile organisms that lack a specialized immune system to cope with biotic and abiotic stress. Instead, plants have complex regulatory networks that determine the appropriate distribution of resources between the developmental and the defense programs. In the last years, epigenetic regulation of repeats and gene expression has evolved as an important player in the transcriptional regulation of stress‐related genes. Here, we review the current knowledge about how different stresses interact with different levels of epigenetic control of the genome. Moreover, we analyze the different examples of transgenerational epigenetic inheritance and connect them with the known features of genome epigenetic regulation. Although yet to be explored, the interplay between epigenetics and stress resistance seems to be a relevant and dynamic player of the interaction of plants with their environments.