Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth

Plant secondary (or specialized) metabolites mediate important interactions in both the rhizosphere and the phyllosphere. If and how such compartmentalized functions interact to determine plant–environment interactions is not well understood. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth when plants are grown in soils with very low available iron but enhance growth in soils with higher available iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions and in the presence of chelated iron but enhance herbivore growth in the presence of free iron in the growth medium. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with potential consequences for plant resistance in variable environments.

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Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth

10.1101/2021.05.14.444261 ◽

2021 ◽

Author(s):

Lingfei Hu ◽

Zhenwei Wu ◽

Christelle AM Robert ◽

Ouyang Xiao ◽

Tobias Zuest ◽

...

Keyword(s):

Secondary Metabolites ◽

Soil Chemistry ◽

Insect Pest ◽

Plant Secondary Metabolites ◽

Fall Armyworm ◽

Free Form ◽

Larval Performance ◽

Primary Metabolism ◽

Iron Deficient ◽

The Impact

Specialized metabolites mediate important interactions in both the rhizosphere and the phyllosphere. How this compartmentalized multifunctionality influences plant-environment interactions is unknown. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth in soils with low bioavailable iron but enhance growth in soils with higher bioavailable iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions but enhance herbivore growth when iron is present in its free form. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with major consequences for plant health in variable environments.

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The Gut Microbiota in Camellia Weevils Are Influenced by Plant Secondary Metabolites and Contribute to Saponin Degradation

mSystems ◽

10.1128/msystems.00692-19 ◽

2020 ◽

Vol 5 (2) ◽

Cited By ~ 1

Author(s):

Shouke Zhang ◽

Jinping Shu ◽

Huaijun Xue ◽

Wei Zhang ◽

Yabo Zhang ◽

...

Keyword(s):

Secondary Metabolites ◽

Microbial Communities ◽

Bacterial Communities ◽

Insect Pest ◽

Plant Secondary Metabolites ◽

Sole Source ◽

Chemical Defenses ◽

Plant Interactions ◽

Content Type ◽

Tea Saponin

ABSTRACT The camellia weevil (CW [Curculio chinensis]) is a notorious host-specific predator of the seeds of Camellia species in China, causing seed losses of up to 60%. The weevil is capable of overcoming host tree chemical defenses, while the mechanisms of how these beetles contend with the toxic compounds are still unknown. Here, we examined the interaction between the gut microbes of CW and camellia seed chemistry and found that beetle-associated bacterial symbionts mediate tea saponin degradation. We demonstrate that the gut microbial community profile of CW was significantly plant associated, and the gut bacterial community associated with CW feeding on Camellia oleifera seeds is enriched with genes involved in tea saponin degradation compared with those feeding on Camellia sinensis and Camellia reticulata seeds. Twenty-seven bacteria from the genera Enterobacter, Serratia, Acinetobacter, and Micrococcus subsisted on tea saponin as a sole source of carbon and nitrogen, and Acinetobacter species are identified as being involved in the degradation of tea saponin. Our results provide the first metagenome of gut bacterial communities associated with a specialist insect pest of Camellia trees, and the results are consistent with a potential microbial contribution to the detoxification of tree-defensive chemicals. IMPORTANCE The gut microbiome may play an important role in insect-plant interactions mediated by plant secondary metabolites, but the microbial communities and functions of toxic plant feeders are still poorly characterized. In the present study, we provide the first metagenome of gut bacterial communities associated with a specialist weevil feeding on saponin-rich and saponin-low camellia seeds, and the results reveal the correlation between bacterial diversity and plant allelochemicals. We also used cultured microbes to establish their saponin-degradative capacity outside the insect. Our results provide new experimental context to better understand how gut microbial communities are influenced by plant secondary metabolites and how the resistance mechanisms involving microbes have evolved to deal with the chemical defenses of plants.

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Secondary Metabolites, Ferulic Acid and p-Hydroxybenzoic Acid Induced Toxic Effects on Photosynthetic Process in Rumex acetosa L.

Biomolecules ◽

10.3390/biom11020233 ◽

2021 ◽

Vol 11 (2) ◽

pp. 233

Author(s):

M. Iftikhar Hussain ◽

Manuel J. Reigosa

Keyword(s):

Energy Dissipation ◽

Secondary Metabolites ◽

Ferulic Acid ◽

Photon Energy ◽

Plant Secondary Metabolites ◽

Photochemical Quenching ◽

Hydroxybenzoic Acid ◽

Absorbed Energy ◽

Rumex Acetosa ◽

The Impact

The elimination of broadleaf weeds from agricultural fields has become an urgent task in plant and environment protection. Allelopathic control is considered a potential approach because of its exclusive and ecological safety measures. Plant secondary metabolites also called allelochemicals are released from plant leaves, roots, stem, bark, flowers and play significant roles in soil rhizosphere signaling, chemical ecology, and plant defense. The present study was carried out to evaluate the impact of two allelochemicals; ferulic acid (FA) and p-hydroxybenzoic acid (pHBA) on photosynthetic characteristics; Fv/Fm: efficiency of photosystem II photochemistry in the dark-adapted state; ΦPSII: photosynthetic quantum yield; NPQ, non-photochemical quenching; qP, photochemical quenching, and photon energy dissipation (1−qP)/NPQ in Rumex acetosa following 6 days exposure. R. acetosa seedlings were grown in perlite culture, irrigated with Hoagland solution and treated with allelopathic compounds FA and pHBA and were evaluated against the photosynthetic attributes. Both compounds behaved as potent inhibitors of photosynthetic traits such as Fv/Fm, ΦPSII, qP, and NPQ in R. acetosa. Photon energy dissipation (1−qP)/NPQ increased significantly from days 3 to 6. Higher dissipation of absorbed energy indicates the inactivation state of reaction centers and their inability to effectively use the absorbed energy in photosynthesis. These results indicated the potential allelopathic application of FA and pHBA for control of broadleaf weed, Rumex acetosa.

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Plant secondary metabolites as defenses, regulators and primary metabolites- The blurred functional trichotomy

10.31219/osf.io/6ba7r ◽

2020 ◽

Author(s):

Matthias Erb ◽

Daniel J. Kliebenstein

Keyword(s):

Secondary Metabolites ◽

Plant Growth ◽

Plant Secondary Metabolites ◽

Trophic Levels ◽

Primary Metabolism ◽

Plant Metabolites ◽

Small Molecular Weight ◽

Primary Metabolites ◽

Environmental Selection ◽

Plant Environment

The plant kingdom produces hundreds of thousands of small molecular weight organic compounds. Based on their assumed functions, the research community has classified them into three overarching groups: primary metabolites which are directly required for plant growth, secondary (or specialized) metabolites which mediate plant-environment interactions and hormones which regulate organismal processes, including metabolism. For decades, this functional trichotomy has shaped theory and experimentation in plant biology. However, evidence is accumulating that the boundaries between the different types of metabolites are blurred. An increasing number of mechanistic studies demonstrate that secondary metabolites are multifunctional and can act as potent regulators of plant growth and defense. Secondary metabolites are also re-integrated into primary metabolism, thus behaving like primary metabolites sensu lato. Several adaptive scenarios may have favored this functional diversity for secondary metabolites, including signaling robustness and cost-effective storage and recycling. Secondary metabolite multi-functionality can provide new explanations for ontogenetic patterns of defense production and can refine our understanding of plant-herbivore interactions, in particular by accounting for the discovery that adapted herbivores misuse plant secondary metabolites for multiple purposes, some of which mirror their functions in plants. In conclusion, recent work unveils the limits of our current classification system for plant metabolites and suggests that viewing them as integrated components of metabolic networks that are dynamically shaped by environmental selection pressures and transcend multiple trophic levels can improve our understanding of plant metabolism and plant-environment interactions.

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Translating physiological signals to changes in feeding behaviour in mammals and the future effects of global climate change

Animal Production Science ◽

10.1071/an14487 ◽

2015 ◽

Vol 55 (3) ◽

pp. 272 ◽

Cited By ~ 16

Author(s):

Ben D. Moore ◽

Natasha L. Wiggins ◽

Karen J. Marsh ◽

M. Denise Dearing ◽

William J. Foley

Keyword(s):

Climate Change ◽

Secondary Metabolites ◽

Global Climate Change ◽

Nutrient Intake ◽

Feeding Behaviour ◽

Global Climate ◽

Plant Secondary Metabolites ◽

The Other ◽

Physiological Signals ◽

The Impact

Mammals cannot avoid ingesting secondary metabolites, often in significant amounts. Thus, their intake must be regulated to avoid intoxication. Three broad mechanisms have been described by which this can be achieved. These are conditioned aversions mediated by nausea, non-conditioned aversions and the recognition of limits to detoxification. Although there is some overlap between these, we know little about the way that mechanisms of toxin avoidance interact with regulation of nutrient intake and whether one has priority over the other. Nonetheless, regulation of meal length and inter-meal length allows the intake of some plant secondary metabolites to be matched with an animal’s capacity for detoxification and its nutritional requirements. Toxicity itself is not a fixed limitation and recent work suggests that ambient temperature can be a major determinant of the toxicity of plant secondary metabolites, largely through effects on liver function. These effects are likely to be of major importance in predicting the impact of global climate change on herbivores.

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Review on the Bio-insecticidal Properties of Some Plant Secondary Metabolites: Types, Formulations, Modes of Action, Advantages and Limitations

Asian Journal of Research in Zoology ◽

10.9734/ajriz/2020/v3i430099 ◽

2020 ◽

pp. 27-60

Author(s):

Ukoroije, Rosemary Boate ◽

Otayor, Richard Abalis

Keyword(s):

Secondary Metabolites ◽

Pest Management ◽

Insect Pests ◽

Insect Pest ◽

Crop Protection ◽

Plant Secondary Metabolites ◽

Antifeedant Activity ◽

Insect Pest Control ◽

Repeated Applications ◽

Synthetic Pesticides

Bio-pesticides are biological derived agents that are usually applied in a manner similar to synthetic pesticides but achieve pest management in an environmental friendly way. Bioinsecticides have the advantages of been reportedly eco-friendly both to man and the environment, are target specific, lack problem of residue, least persistent in environment, locally available, easily processed and inexpensive, though with the limitation of requiring repeated applications for the achievement of optimal control of insect pests while enhancing crop protection. The mode of action of bioinsecticides on insects includes repellent action, antifeedant activity, oviposition deterrent properties, growth and development inhibition, toxicity, attractants, sterility and death. Hence, bioinsecticides can be included in integrated pest management programs for crop protection and insect pest control. The review on biopesticidal properties of some plant secondary metabolites in the leaves, stems, bark, fruits, flowers, cloves, rhizomes, grains and seeds of plants and their interference with the growth, feeding, reproduction of insect pestsfor pest management has been elaborated.

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Assessment of impacts of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) on maize production in Ghana

Journal of Integrated Pest Management ◽

10.1093/jipm/pmaa015 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Djima Koffi ◽

Rosina Kyerematen ◽

Vincent Y Eziah ◽

Yaa Oguabi Osei-Mensah ◽

Kwame Afreh-Nuamah ◽

...

Keyword(s):

Spodoptera Frugiperda ◽

Management Practices ◽

Deciduous Forest ◽

Insect Pest ◽

Fall Armyworm ◽

Transitional Zone ◽

African Countries ◽

Maize Production ◽

Ecological Zones ◽

The Impact

Abstract Spodoptera frugiperda was considered an insect pest only in the Americas until its first report in African countries in 2016. In this study, farmers and agricultural officials in Ghana were interviewed on their perceptions and knowledge of the pest, on infestation and maize yield variations across years, and on management practices. Farms were inspected to determine the infestation level of 100 plants per hectare. Interviews revealed that farmers were familiar with the larval stages of this pest and noticed that the pest occurred throughout the year, but populations of S. frugiperda increased only during cropping seasons. Infestation levels reported by farmers in surveys were much lower in 2018 (30.38%) than in 2017 (80.92%). Farm inspections confirmed that infestation levels were much lower in 2018 (20.90%) than 2017 (73.70%). The belt formed by Guinea Savannah, Transitional Zone, and Semi-Deciduous Forest Agro-Ecological Zones (AEZs) recorded the highest infestations while the lowest were observed from the Sudan Savannah and Tropical Rain Forest AEZs. Insecticides were the most commonly used tactic to manage populations of this new pest. Maize yields increased across Ghana between 2013 and 2015 from 1.52 to 1.73 t/ha, decreased between 2015 and 2017 to 1.55 t/ha, and increased to 1.69 t/ha in 2018. The impact of fall armyworm injury to maize production is discussed.

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The Effect of Diet on the Composition and Stability of Proteins Secreted by Honey Bees in Honey

Insects ◽

10.3390/insects10090282 ◽

2019 ◽

Vol 10 (9) ◽

pp. 282 ◽

Cited By ~ 5

Author(s):

Oleg Lewkowski ◽

Carmen I. Mureșan ◽

Dirk Dobritzsch ◽

Matthew Fuszard ◽

Silvio Erler

Keyword(s):

Secondary Metabolites ◽

Protein Quality ◽

Plant Secondary Metabolites ◽

Nitrogen Sources ◽

Specific Protein ◽

Nutritional Composition ◽

Food Sources ◽

Sugar Solution ◽

Feeding Regimes ◽

The Impact

Honey proteins are essential bee nutrients and antimicrobials that protect honey from microbial spoilage. The majority of the honey proteome includes bee-secreted peptides and proteins, produced in specialised glands; however, bees need to forage actively for nitrogen sources and other basic elements of protein synthesis. Nectar and pollen of different origins can vary significantly in their nutritional composition and other compounds such as plant secondary metabolites. Worker bees producing and ripening honey from nectar might therefore need to adjust protein secretions depending on the quality and specific contents of the starting material. Here, we assessed the impact of different food sources (sugar solutions with different additives) on honey proteome composition and stability, using controlled cage experiments. Honey-like products generated from sugar solution with or without additional protein, or plant secondary metabolites, differed neither in protein quality nor in protein quantity among samples. Storage for 4 weeks prevented protein degradation in most cases, without differences between food sources. The honey-like product proteome included several major royal jelly proteins, alpha-glucosidase and glucose oxidase. As none of the feeding regimes resulted in different protein profiles, we can conclude that worker bees may secrete a constant amount of each bee-specific protein into honey to preserve this highly valuable hive product.

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The Impact of Cadmium on Photosynthetic Performance and Secondary Metabolites in the Lichens Parmelia sulcata, Flavoparmelia caperata and Evernia prunastri

Acta Botanica Croatica ◽

10.1515/botcro-2016-0034 ◽

2016 ◽

Vol 75 (2) ◽

pp. 186-193 ◽

Cited By ~ 1

Author(s):

Ana Maslać ◽

Maja Maslać ◽

Mirta Tkalec

Keyword(s):

Secondary Metabolites ◽

Metal Pollution ◽

Usnic Acid ◽

Photosynthetic Performance ◽

Cadmium Exposure ◽

Primary Metabolism ◽

Evernia Prunastri ◽

Parmelia Sulcata ◽

Flavoparmelia Caperata ◽

The Impact

Abstract Lichens are one of the most common air quality bioindicators. Airborne heavy metal pollution causes various physiological changes in lichens, but sensitivity to metal pollution is species specific. In this research, three lichen species (Parmelia sulcata, Flavoparmelia caperata and Evernia prunastri) were exposed to cadmium (50 mg L−1) in laboratory conditions. Photosynthetic efficiency of photosystem II and content of secondary metabolites were determined after one, three and eight days of exposure. In all investigated species treatment of lichen thalli with cadmium significantly changed Fv/Fm and RFd only after eight days of exposure. Quantification of metabolites showed a decreased content of the medullary depsidones salazinic acid (in P. sulcata) and protocetraric acid (in F. caperata) but increased content of cortical depside atranorin (in P. sulcata) and dibenzofurane usnic acid (in F. caperata) after cadmium exposure. However, no changes in secondary metabolites were found in E. prunastri. Results show that investigated species are relatively resistant to short-term cadmium-exposure and that secondary metabolites could have an important role in the protection of primary metabolism from negative cadmium impacts, at least in some species.

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Variation in root secondary metabolites is shaped by past climatic conditions

10.1101/2020.01.25.919654 ◽

2020 ◽

Author(s):

Zoe Bont ◽

Tobias Züst ◽

Meret Huber ◽

Matthias Erb

Keyword(s):

Secondary Metabolites ◽

Abiotic Factors ◽

Plant Secondary Metabolites ◽

Climatic Conditions ◽

List Type ◽

Heritable Trait ◽

Root Herbivore ◽

Herbivore Pressure ◽

The Impact

AbstractPlants can adapt to changing environments by adjusting the production and maintenance of diverse sets of bioactive secondary metabolites. To date, the impact of past climatic conditions relative to other factors such as soil abiotic factors and herbivore pressure on the evolution of plant secondary metabolites is poorly understood, especially for plant roots.We explored associations between root latex secondary metabolites in 63 Taraxacum officinale populations across Switzerland and past climatic conditions, soil abiotic parameters, and root herbivore pressure. To assess the contribution of environmental effects, root secondary metabolites were measured in F0 plants in nature and F2 plants under controlled greenhouse conditions.Concentrations of root latex secondary metabolites were most strongly associated with past climatic conditions, while current soil abiotic factors or root herbivore pressure did not show a clear association with root latex chemistry. Results were identical for natural and controlled conditions, suggesting heritable trait variation rather than environmental plasticity as underlying factor.Synthesis. We conclude that climatic conditions likely play a major role in the evolution of root secondary metabolites. Direct abiotic effects are likely underlying this pattern, hinting at a novel role of root latex metabolites the tolerance of abiotic stress.

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