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.
Minimizing losses to pests and diseases is essential for producing sufficient food to feed the world's rapidly growing population. The necrotrophic fungus Botrytis cinerea triggers devastating pre-and post-harvest yield losses in tomato (Solanum lycopersicum). Current control methods are based on the pre-harvest use of fungicides, which are limited by strict legislation. This investigation tested whether induction of resistance by b-aminobutyric acid (BABA) at different developmental stages provides an alternative strategy to protect post-harvest tomato fruit against B. cinerea. Soildrenching plants with BABA once fruit had already formed had no impact on tomato susceptibility to B. cinerea. However, BABA application to seedlings significantly reduced post-harvest infection of fruit. This resistance response was not associated with a yield reduction; however, there was a delay in fruit ripening. Untargeted metabolomics revealed differences between fruit from water-and BABA-treated plants, demonstrating that BABA triggered a defence-associated metabolomics profile that was long lasting. Targeted analysis of defence hormones suggested a role of abscisic acid (ABA) in the resistance phenotype. Post-harvest application of ABA to the fruit of water-treated plants induced susceptibility to B. cinerea. This phenotype was absent from the ABA-exposed fruit of BABA-treated plants, suggesting a complex role of ABA in BABA-induced resistance. A final targeted metabolomic analysis detected trace residues of BABA accumulated in the red fruit. Overall, it was demonstrated that BABA induces post-harvest resistance in tomato fruit against B. cinerea with no penalties in yield.
This article is protected by copyright. All rights reserved II. Stage 1: the regulatory role of pathogen-induced epigenetic change III. Stage 2: genetic consequences of the stress-induced mobilome IV. Stage 3: evolutionary consequences of stress-induced (epi)genetic change V. Conclusions and translation to crop protection Acknowledgements References
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.
Stress can alter important plant life-history traits. Here, we report the long-term effects of the stress hormone jasmonic acid (JA) on the defence phenotype, transcriptome and DNAmethylome of Arabidopsis. Three weeks after transient JA signalling activity, 5-week-old plants retained induced resistance (IR) against herbivory but showed enhanced susceptibility to necrotrophic and biotrophic pathogens. Transcriptome analysis of these plants revealed priming and/or up-regulation of JA-dependent defence genes but repression of ethyleneand salicylic acid-dependent genes. Long-term JA-IR against herbivory was associated with shifts in glucosinolate composition and required MYC2/3/4 transcription factors, DNA (de)methylation pathways and the small RNA (sRNA)-binding protein ARGONOUTE1 (AGO1). Although methylome analysis did not reveal consistent changes in DNA methylation near MYC2/3/4-controlled genes, JA-treated plants were specifically enriched with hypomethylated ATREP2 transposable elements (TEs), while ATREP2-derived sRNAs showed increased association with AGO1. Our results indicate that AGO1-associated sRNAs from hypomethylated ATREP2 TEs trans-regulate long-lasting memory of JAdependent immunity.
Norway spruce (Picea abies) is an economically and ecologically important tree species that grows across northern and central Europe. Treating Norway spruce with jasmonate has long‐lasting beneficial effects on tree resistance to damaging pests, such as the European spruce bark beetle Ips typographus and its fungal associates. The (epi)genetic mechanisms involved in such long‐lasting jasmonate induced resistance (IR) have gained much recent interest but remain largely unknown. In this study, we treated 2‐year‐old spruce seedlings with methyl jasmonate (MeJA) and challenged them with the I. typographus vectored necrotrophic fungus Grosmannia penicillata. MeJA treatment reduced the extent of necrotic lesions in the bark 8 weeks after infection and thus elicited long‐term IR against the fungus. The transcriptional response of spruce bark to MeJA treatment was analysed over a 4‐week time course using mRNA‐seq. This analysis provided evidence that MeJA treatment induced a transient upregulation of jasmonic acid, salicylic acid and ethylene biosynthesis genes and downstream signalling genes. Our data also suggests that defence‐related genes are induced while genes related to growth are repressed by methyl jasmonate treatment. These results provide new clues about the potential underpinning mechanisms and costs associated with long‐term MeJA‐IR in Norway spruce.
Stress exposure can have long-lasting impacts on ecologically relevant life-history traits in plants. Here, we have investigated the long-term impacts of the stress hormone jasmonic acid (JA) on the defence phenotype, transcriptome and DNA methylome of Arabidopsis thaliana. Three weeks after transient JA signalling activity in seedlings, 5-week-old plants retained induced resistance (IR) against herbivory but showed enhanced susceptibility to necrotrophic and biotrophic pathogens. Transcriptome analysis revealed that JA seedling treatment causes prolonged priming and/or up-regulation of JA-dependent defence genes but repression of ethylene- and salicylic acid-dependent genes. Long-term JA-IR against herbivory was dependent on MYC2/3/4 transcription factors and DNA (de)methylation pathways. Although DNA methylome analysis did not reveal consistent changes in DNA methylation near MYC2/3/4-controlled defence genes, plants from JA-treated seedlings showed enrichment of differentially methylated regions at ATREP2 transposable elements (TEs). Our study points to a trans-acting mechanism whereby hypomethylated TEs mediate long-lasting epigenetic memory of JA-dependent immunity.
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