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Caarls, L.

Publications and source records attributed to Caarls, L..

6 recordsLinked to original sources

Nuclear NPR1 Modulates Salicylic Acid/Jasmonic Acid Crosstalk via Transcriptional Control of WRKY Transcription Factors

The plant hormones salicylic acid (SA) and jasmonic acid (JA) are major regulators of plant defense. They can antagonize each other's activity, enabling an optimized defense response. The SA master regulator NPR1 is a key player in this SA/JA crosstalk, although the mechanisms of NPR1-mediated SA/JA crosstalk remain only partly understood, especially regarding the ethylene-coregulated ERF branch of the JA pathway. Here, we investigated the function of NPR1 in SA/JA crosstalk using several Arabidopsis npr1 mutant variants. Assays using the NPR1-HBD and npr1-nls lines, expressing only cytosolic NPR1, revealed that NPR1 has a nuclear role in SA/JA crosstalk. RNA-seq analysis of lines expressing NPR1 mutated in residues Cys82 or Cys216, in which repression of the JA pathway was impaired while SA pathway induction remained mostly intact, identified 32 SA-responsive genes with reduced expression compared to Col-0, including four WRKY transcription factor genes. Of these, WRKY53 and WRKY70 could suppress expression of the JA marker gene PDF1.2 induced by ORA59, the master regulator of the ERF branch of the JA pathway, in a protoplast system. Additional SA-inducible WRKYs (WRKY50, WRKY54, WRKY63, and WRKY67) similarly suppressed ORA59-induced PDF1.2 expression, implicating WRKY63 and WRKY67 for the first time in SA/JA crosstalk and confirming earlier reports on the role of the other WRKY TFs. WRKY53 and WRKY67 were further shown to reduce accumulation of the ORA59 protein in protoplasts. Thus, our study indicated that NPR1 can regulate SA/JA crosstalk in the nucleus via transcriptional activation of genes encoding specific JA-repressing WRKY transcription factors.

molecular biology↗

Tetraose glycoalkaloids from potato can provide complete protection against fungi and insects

Plants with innate disease and pest resistance can contribute to more sustainable agriculture. Natural defence compounds produced by plants have the potential to provide a general protective effect against pathogens and pests, but they are not a primary target in resistance breeding. Here, we identified a wild relative of potato, Solanum commersonii, that provides us with unique insight in the role of glycoalkaloids in plant immunity. We cloned two atypical resistance genes that provide resistance to Alternaria solani and Colorado potato beetle through the production of tetraose steroidal glycoalkaloids. Moreover, we provide in vitro evidence to show that these compounds have potential against a range of different (potato pathogenic) fungi. This research links structural variation in steroidal glycoalkaloids to resistance against potato diseases and pests. Further research on the biosynthesis of plant defence compounds in different tissues, their toxicity, and the mechanisms for detoxification, can aid the effective use of such compounds to improve sustainability of our food production.

plant biology↗

Deciphering Brassica plant defence responses to cabbage white butterfly egg-associated molecular patterns

Brassica plants activate a strong hypersensitive response (HR)-like necrosis underneath eggs of cabbage white butterflies, but their molecular response to eggs is poorly understood. Here, we developed a method to generate egg wash to identify potential insect egg-associated molecular patterns (EAMPs) inducing HR-like necrosis. We found that egg wash, containing compounds from Pieris eggs, induced a similar response as eggs. We show that wash of hatched eggs, of egg glue, and of accessory reproductive glands (ARG) that produce this glue, also induced HR-like necrosis, whereas removal of the glue from eggs resulted in a reduced response. Eggs of Pieris butterflies induced callose deposition, production of reactive oxygen species and cell death in B. nigra and B. rapa leaf tissue, also in plants that did not express HR-like necrosis. Finally, only washes from Pieris eggs induced defence genes and ethylene production, whereas egg wash of a generalist moth did not. Our results indicate that EAMPs are in the egg glue and that the response in B. nigra is specific to Pieris species. Our study expands knowledge on the Brassica-Pieris-egg interaction, and paves the way for identification of EAMPs in Pieris egg glue and corresponding receptor in Brassica spp.

plant biology↗

Insect egg-killing: a new front on the evolutionary arms-race between Brassicaceae plants and Pierid butterflies

Evolutionary arms-races between plants and herbivores have been proposed to generate key innovations that can drive diversification of the interacting species. Recent studies reveal that plant traits that target herbivore insect eggs are widespread throughout the plant kingdom. Within the Brassicaceae family, some plants express a hypersensitive response (HR)-like necrosis underneath the eggs of specialist cabbage white butterflies (Pieridae) that leads to eggs desiccating or dropping of the leaf. Here, we studied the evolutionary basis of this trait, its egg-killing effect on and elicitation by specialist butterflies, by screening 31 Brassicaceae species and nine Pieridae species. We show that induction of HR-like necrosis by pierid egg deposition is clade-specific in the economically important Brassiceae tribe (Brassica crops and close-relatives) and in the first-branching genus Aethionema. The necrosis is elicited only by pierid butterflies that feed on Brassicaceae plants; four Pieris and Anthocharis cardamines butterflies, of which the larvae are specialists on Brassicaceae, elicited a HR-like necrosis. Eggs of pierid butterflies that feed on Rhamnaceae (Gonepteryx rhamni) or Fabaceae (Colias spp.) however, did not elicit such a leaf necrosis. Finally, eggs of Aglais io, a species of the sister group Nymphalidae, did not elicit any visible response. Counter-adaptations to HR-like necrosis might have evolved by insect deposition of eggs in clusters or on inflorescences. Our findings suggest that the plants egg-killing trait is a new front on the evolutionary arms-race between Brassicaceae and pierid butterflies beyond the well-studied chemical defence traits against caterpillars.

evolutionary biology↗

Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JA-isoleucine (JA-Ile) have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. As they are induced by JA we named them JASMONATE-INDUCED OXYGENASEs (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae. In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in over-accumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses.\n\nSIGNIFICANCE STATEMENTIn plants, the hormone jasmonic acid (JA) is synthesized in response to attack by pathogens and herbivores, leading to activation of defense responses. Rapidly following JA accumulation, the hormone is metabolized, presumably to prevent inhibitive effects of high JA levels on growth and development. The enzymes that directly inactivate JA were so far unknown. Here, we identify four jasmonate-induced oxygenases (JOXs) in Arabidopsis that hydroxylate jasmonic acid to form inactive 12-OH-JA. A mutant that no longer produces the four enzymes hyperaccumulates JA, exhibits reduced growth, and is highly resistant to attackers that are sensitive to JA-dependent defense. The JOX enzymes thus play an important role in determining the amplitude and duration of JA responses to balance the growth-defense tradeoff.

plant biology↗

Architecture and dynamics of the jasmonic acid gene regulatory network

The phytohormone jasmonic acid (JA) is a critical regulator of plant growth and defense. To significantly advance our understanding of the architecture and dynamics of the JA gene regulatory network, we performed high-resolution RNA-Seq time series analyses of methyl JA-treated Arabidopsis thaliana. Computational analysis unraveled in detail the chronology of events that occur during the early and later phases of the JA response. Several transcription factors, including ERF16 and bHLH27, were uncovered as early components of the JA gene regulatory network with a role in pathogen and insect resistance. Moreover, analysis of subnetworks surrounding the JA-induced transcription factors ORA47, RAP2.6L, and ANAC055 provided novel insights into their regulatory role of defined JA network modules. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints to novel regulators, and provides a valuable resource for future studies on the function of JA signaling components in plant defense and development.

plant biology↗