Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity

Science ◽  
2021 ◽  
Vol 371 (6526) ◽  
pp. 255-260
Author(s):  
Jiancai Li ◽  
Rayko Halitschke ◽  
Dapeng Li ◽  
Christian Paetz ◽  
Haichao Su ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Chemical Defenses ◽  
Toxic Waste ◽  
Nicotiana Attenuata ◽  
Plant Chemical Defense ◽  
Herbivore Defense ◽  
Plant Chemical ◽  
In The Wild ◽  
Sphingolipid Biosynthesis ◽  
Diterpene Biosynthesis

Many plant specialized metabolites function in herbivore defense, and abrogating particular steps in their biosynthetic pathways frequently causes autotoxicity. However, the molecular mechanisms underlying their defense and autotoxicity remain unclear. Here, we show that silencing two cytochrome P450s involved in diterpene biosynthesis in the wild tobacco Nicotiana attenuata causes severe autotoxicity symptoms that result from the inhibition of sphingolipid biosynthesis by noncontrolled hydroxylated diterpene derivatives. Moreover, the diterpenes’ defensive function is achieved by inhibiting herbivore sphingolipid biosynthesis through postingestive backbone hydroxylation products. Thus, by regulating metabolic modifications, tobacco plants avoid autotoxicity and gain herbivore defense. The postdigestive duet that occurs between plants and their insect herbivores can reflect the plant’s solutions to the “toxic waste dump” problem of using potent chemical defenses.

scholarly journals Ecological Implications of Organic Mulches in Arboriculture: A Mechanistic Pathway Connecting the Use of Organic Mulches with Tree Chemical Defenses

2009 ◽  
Vol 35 (4) ◽  
pp. 211-217
Author(s):  
Javier Lugo-Perez ◽  
John Lloyd
Keyword(s):  
Resource Availability ◽  
Urban Areas ◽  
Chemical Defenses ◽  
Plant Performance ◽  
Plant Chemical Defense ◽  
Experimental Conditions ◽  
Indirect Benefits ◽  
Plant Resource ◽  
Mechanistic Pathway ◽  
Plant Chemical

In addition to the aesthetic and practical benefits of mulching, studies have shown indirect benefits of organic mulches to tree establishment and growth. These indirect benefits are associated with direct improvements on soil water and nutrient availability by mulches. The generalization of the organic mulches benefit to soil and trees has been questioned by several studies showing contradictory results under different experimental conditions and mulching materials. In addition, overall benefits for trees may be overlooked by focusing studies on some aspects of plant performance (e.g., plant growing rate) while ignoring others (e.g., plant chemical defense). This paper reviews studies showing how organic mulches can directly affect plant resource availability in the soil, presenting evidence from the literature that illustrates the influence of organic mulches on plant resource availability can also affect tree photosynthate allocation dynamics with direct consequences on plant chemical defenses. Based on the reviewed literature, presented here is a mechanistic pathway to illustrate how organic mulches can influence plant resources in the soil, and in turn how that can affect tree physiology and tree-insect interactions in urban areas.

Lack of rapid monoterpene turnover in rooted plants: implications for theories of plant chemical defense

Oecologia ◽  
1991 ◽  
Vol 87 (3) ◽  
pp. 373-376 ◽  
Author(s):  
Charles A. Mihaliak ◽  
Jonathan Gershenzon ◽  
Rodney Croteau
Keyword(s):  
Chemical Defense ◽  
Plant Chemical Defense ◽  
Plant Chemical

scholarly journals Sphingolipid biosynthesis upregulation by TOR complex 2–Ypk1 signaling during yeast adaptive response to acetic acid stress

2016 ◽  
Vol 473 (23) ◽  
pp. 4311-4325 ◽  
Author(s):  
Joana F. Guerreiro ◽  
Alexander Muir ◽  
Subramaniam Ramachandran ◽  
Jeremy Thorner ◽  
Isabel Sá-Correia
Keyword(s):  
Acetic Acid ◽  
Protein Kinase ◽  
Cellular Response ◽  
Molecular Mechanisms ◽  
Acid Stress ◽  
Acid Tolerance ◽  
Industrial Biotechnology ◽  
Acetic Acid Tolerance ◽  
Spoilage Yeasts ◽  
Sphingolipid Biosynthesis

Acetic acid-induced inhibition of yeast growth and metabolism limits the productivity of industrial fermentation processes, especially when lignocellulosic hydrolysates are used as feedstock in industrial biotechnology. Tolerance to acetic acid of food spoilage yeasts is also a problem in the preservation of acidic foods and beverages. Thus understanding the molecular mechanisms underlying adaptation and tolerance to acetic acid stress is increasingly important in industrial biotechnology and the food industry. Prior genetic screens for Saccharomyces cerevisiae mutants with increased sensitivity to acetic acid identified loss-of-function mutations in the YPK1 gene, which encodes a protein kinase activated by the target of rapamycin (TOR) complex 2 (TORC2). We show in the present study by several independent criteria that TORC2–Ypk1 signaling is stimulated in response to acetic acid stress. Moreover, we demonstrate that TORC2-mediated Ypk1 phosphorylation and activation is necessary for acetic acid tolerance, and occurs independently of Hrk1, a protein kinase previously implicated in the cellular response to acetic acid. In addition, we show that TORC2–Ypk1-mediated activation of l-serine:palmitoyl-CoA acyltransferase, the enzyme complex that catalyzes the first committed step of sphingolipid biosynthesis, is required for acetic acid tolerance. Furthermore, analysis of the sphingolipid pathway using inhibitors and mutants indicates that it is production of certain complex sphingolipids that contributes to conferring acetic acid tolerance. Consistent with that conclusion, promoting sphingolipid synthesis by adding exogenous long-chain base precursor phytosphingosine to the growth medium enhanced acetic acid tolerance. Thus appropriate modulation of the TORC2–Ypk1–sphingolipid axis in industrial yeast strains may have utility in improving fermentations of acetic acid-containing feedstocks.

scholarly journals Cardenolides, toxicity, and the costs of sequestration in the coevolutionary interaction between monarchs and milkweeds

2021 ◽  
Vol 118 (16) ◽  
pp. e2024463118
Author(s):  
Anurag A. Agrawal ◽  
Katalin Böröczky ◽  
Meena Haribal ◽  
Amy P. Hastings ◽  
Ronald A. White ◽  
...  
Keyword(s):  
Danaus Plexippus ◽  
Monarch Butterfly ◽  
Chemical Defenses ◽  
Trade Off ◽  
Asclepias Curassavica ◽  
Plant Chemical ◽  
Whole Plants ◽  
Benefits And Costs

For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring–containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch’s neural Na+/K+-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch’s typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs of sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.

scholarly journals Combined metabolome and transcriptome analysis reveals key components of complete desiccation tolerance in an anhydrobiotic insect

2020 ◽  
Vol 117 (32) ◽  
pp. 19209-19220 ◽  
Author(s):  
Alina Ryabova ◽  
Richard Cornette ◽  
Alexander Cherkasov ◽  
Masahiko Watanabe ◽  
Takashi Okuda ◽  
...  
Keyword(s):  
Transcriptome Analysis ◽  
Molecular Mechanisms ◽  
Adenosine Monophosphate ◽  
Pentose Phosphate ◽  
Toxic Waste ◽  
Mitochondrial Activity ◽  
Xanthurenic Acid ◽  
Metabolic Adaptations ◽  
Polypedilum Vanderplanki ◽  
Protective Proteins

Some organisms have evolved a survival strategy to withstand severe dehydration in an ametabolic state, called anhydrobiosis. The only known example of anhydrobiosis among insects is observed in larvae of the chironomidPolypedilum vanderplanki. Recent studies have led to a better understanding of the molecular mechanisms underlying anhydrobiosis and the action of specific protective proteins. However, gene regulation alone cannot explain the rapid biochemical reactions and independent metabolic changes that are expected to sustain anhydrobiosis. For this reason, we conducted a comprehensive comparative metabolome–transcriptome analysis in the larvae. We showed that anhydrobiotic larvae adopt a unique metabolic strategy to cope with complete desiccation and, in particular, to allow recovery after rehydration. We argue that trehalose, previously known for its anhydroprotective properties, plays additional vital roles, providing both the principal source of energy and also the restoration of antioxidant potential via the pentose phosphate pathway during the early stages of rehydration. Thus, larval viability might be directly dependent on the total amount of carbohydrate (glycogen and trehalose). Furthermore, in the anhydrobiotic state, energy is stored as accumulated citrate and adenosine monophosphate, allowing rapid reactivation of the citric acid cycle and mitochondrial activity immediately after rehydration, before glycolysis is fully functional. Other specific adaptations to desiccation include potential antioxidants (e.g., ophthalmic acid) and measures to avoid the accumulation of toxic waste metabolites by converting these to stable and inert counterparts (e.g., xanthurenic acid and allantoin). Finally, we confirmed that these metabolic adaptations correlate with unique organization and expression of the corresponding enzyme genes.

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