Stress Enhances the Synthesis of Secondary Plant Products: The Impact of Stress-Related Over-Reduction on the Accumulation of Natural Products
TL;DR: Spice and medicinal plants grown under water deficiency conditions reveal much higher concentrations of relevant natural products compared with identical plants of the same species cultivated with an ample water supply, and a putative mechanistic concept considering general plant physiological and biochemical aspects is presented.
Abstract: Spice and medicinal plants grown under water deficiency conditions reveal much higher concentrations of relevant natural products compared with identical plants of the same species cultivated with an ample water supply. For the first time, experimental data related to this well-known phenomenon have been collected and a putative mechanistic concept considering general plant physiological and biochemical aspects is presented. Water shortage induces drought stress-related metabolic responses and, due to stomatal closure, the uptake of CO2 decreases significantly. As a result, the consumption of reduction equivalents (NADPH + H(+)) for CO2 fixation via the Calvin cycle declines considerably, generating a large oxidative stress and an oversupply of reduction equivalents. As a consequence, metabolic processes are shifted towards biosynthetic activities that consume reduction equivalents. Accordingly, the synthesis of reduced compounds, such as isoprenoids, phenols or alkaloids, is enhanced.
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TL;DR: Application of molecular biology tools and techniques are facilitating understanding the signaling processes and pathways involved in the SMs production at subcellular, cellular, organ and whole plant systems during in vivo and in vitro growth, with application in metabolic engineering of biosynthetic pathways intermediates.
Abstract: In the growth condition(s) of plants, numerous secondary metabolites (SMs) are produced by them to serve variety of cellular functions essential for physiological processes, and recent increasing evidences have implicated stress and defense response signaling in their production. The type and concentration(s) of secondary molecule(s) produced by a plant are determined by the species, genotype, physiology, developmental stage and environmental factors during growth. This suggests the physiological adaptive responses employed by various plant taxonomic groups in coping with the stress and defensive stimuli. The past recent decades had witnessed renewed interest to study abiotic factors that influence secondary metabolism during in vitro and in vivo growth of plants. Application of molecular biology tools and techniques are facilitating understanding the signaling processes and pathways involved in the SMs production at subcellular, cellular, organ and whole plant systems during in vivo and in vitro growth, with application in metabolic engineering of biosynthetic pathways intermediates.
618 citations
TL;DR: The characterization of transcriptome changes in Sangiovese berry after PFD highlights, on one hand, the stronger effect of environment than treatment on the whole berry transcriptome rearrangement during development and, on the other, expands existing knowledge of the main molecular and biochemical modifications occurring in defoliated vines.
Abstract: Leaf removal is a grapevine canopy management technique widely used to modify the source-sink balance and/or microclimate around berry clusters to optimize fruit composition. In general, the removal of basal leaves before flowering reduces fruit set, hence achieving looser clusters, and improves grape composition since yield is generally curtailed more than proportionally to leaf area itself. Albeit responses to this practice seem quite consistent, overall vine performance is affected by genotype, environmental conditions, and severity of treatment. The physiological responses of grape varieties to defoliation practices have been widely investigated, and just recently a whole genome transcriptomic approach was exploited showing an extensive transcriptome rearrangement in berries defoliated before flowering. Nevertheless, the extent to which these transcriptomic reactions could be manifested by different genotypes and growing environments is entirely unexplored. To highlight general responses to defoliation vs. different locations, we analyzed the transcriptome of cv. Sangiovese berries sampled at four development stages from pre-flowering defoliated vines in two different geographical areas of Italy. We obtained and validated five markers of the early defoliation treatment in Sangiovese, an ATP-binding cassette transporter, an auxin response factor, a cinnamyl alcohol dehydrogenase, a flavonoid 3-O-glucosyltransferase and an indole-3-acetate beta-glucosyltransferase. Candidate molecular markers were also obtained in another three grapevine genotypes (Nero d'Avola, Ortrugo, and Ciliegiolo), subjected to the same level of selective pre-flowering defoliation (PFD) over two consecutive years in their different areas of cultivation. The flavonol synthase was identified as a marker in the pre-veraison phase, the jasmonate methyltransferase during the transition phase and the abscisic acid receptor PYL4 in the ripening phase. The characterization of transcriptome changes in Sangiovese berry after PFD highlights, on one hand, the stronger effect of environment than treatment on the whole berry transcriptome rearrangement during development and, on the other, expands existing knowledge of the main molecular and biochemical modifications occurring in defoliated vines. Moreover, the identification of candidate genes associated with PFD in different genotypes and environments provides new insights into the applicability and repeatability of this crop practice, as well as its possible agricultural and qualitative outcomes across genetic and environmental variability.
413 citations
Cites background from "Stress Enhances the Synthesis of Se..."
...It is well known that terpenoids metabolism contributes to plant adaptation to the environment, in particular solar exposure, UV-B radiation (Gil et al., 2013; Zhang et al., 2014) and drought (Deluc et al., 2009; Selmar and Kleinwachter, 2013; Savoi et al., 2016)....
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TL;DR: Hormonal interactions between plants and animals illustrate how sophisticated and complex biochemical interrelationships can become, and a chapter on higher-plant-higher-plant interactions makes it clear that secondary compounds of plants may be weapons of offence as well as defence.
Abstract: It is a great pleasure welcome the second edition of Professor Harborne’s pioneering work on biochemical ecology. This introductory text provides the reader with a clear and fascinating account of ways in which living organisms can become adapted to their environments and to each other at the biochemical level. Adaptations of plants to drought and flooding, to high and low temperatures, to changes in ionic concentrations and to the presence in the soil of potentially toxic levels of natural and synthetic chemicals are all discussed. The roles of secondary plant compounds in attracting pollinators to flowers, in stimulating insects to feed on particular plant species or in deterring them from feeding on others are reviewed. The effects of plant toxins on animals and the biochemical responses that may be elicited in these animals by such toxins are described, as are animal pheromones and defence substances. Hormonal interactions between plants and animals illustrate how sophisticated and complex biochemical interrelationships can become, and a chapter on higher-plant-higher-plant interactions makes it clear that secondary compounds of plants may be weapons of offence as well as defence, one species synthesizing and releasing into the environment a compound capable of inhibiting growth in its rivals. Phytoalexin production by higher plants in response to invasion by fungi and pathotoxin production by invading micro-organisms are discussed in a final chapter on higherplant-lower-plant interactions. I recommend this book without reservation. The previous edition was not only used, but enjoyed, by my students. It appealed to both the chemically and the biologically inclined, and I believe that the new edition is a worthy successor. At f5.80 it is very good value.
358 citations
TL;DR: It is important to understand the molecular mechanisms regulating cyanogenesis so that the impact of future environmental challenges can be anticipated and efforts are directed toward their removal to improve food safety.
Abstract: Cyanogenic glycosides (CNglcs) are bioactive plant products derived from amino acids. Structurally, these specialized plant compounds are characterized as α-hydroxynitriles (cyanohydrins) that are stabilized by glucosylation. In recent years, improved tools within analytical chemistry have greatly increased the number of known CNglcs by enabling the discovery of less abundant CNglcs formed by additional hydroxylation, glycosylation, and acylation reactions. Cyanogenesis—the release of toxic hydrogen cyanide from endogenous CNglcs—is an effective defense against generalist herbivores but less effective against fungal pathogens. In the course of evolution, CNglcs have acquired additional roles to improve plant plasticity, i.e., establishment, robustness, and viability in response to environmental challenges. CNglc concentration is usually higher in young plants, when nitrogen is in ready supply, or when growth is constrained by nonoptimal growth conditions. Efforts are under way to engineer CNglcs into some...
314 citations
TL;DR: This study reveals that grapevine berries respond to drought by modulating several secondary metabolic pathways, and particularly, by stimulating the production of phenylpropanoids, the carotenoid zeaxanthin, and of volatile organic compounds such as monoterpenes, with potential effects on grape and wine antioxidant potential, composition, and sensory features.
Abstract: Secondary metabolism contributes to the adaptation of a plant to its environment. In wine grapes, fruit secondary metabolism largely determines wine quality. Climate change is predicted to exacerbate drought events in several viticultural areas, potentially affecting the wine quality. In red grapes, water deficit modulates flavonoid accumulation, leading to major quantitative and compositional changes in the profile of the anthocyanin pigments; in white grapes, the effect of water deficit on secondary metabolism is still largely unknown. In this study we investigated the impact of water deficit on the secondary metabolism of white grapes using a large scale metabolite and transcript profiling approach in a season characterized by prolonged drought. Irrigated grapevines were compared to non-irrigated grapevines that suffered from water deficit from early stages of berry development to harvest. A large effect of water deficit on fruit secondary metabolism was observed. Increased concentrations of phenylpropanoids, monoterpenes, and tocopherols were detected, while carotenoid and flavonoid accumulations were differentially modulated by water deficit according to the berry developmental stage. The RNA-sequencing analysis carried out on berries collected at three developmental stages—before, at the onset, and at late ripening—indicated that water deficit affected the expression of 4,889 genes. The Gene Ontology category secondary metabolic process was overrepresented within up-regulated genes at all the stages of fruit development considered, and within down-regulated genes before ripening. Eighteen phenylpropanoid, 16 flavonoid, 9 carotenoid, and 16 terpenoid structural genes were modulated by water deficit, indicating the transcriptional regulation of these metabolic pathways in fruit exposed to water deficit. An integrated network and promoter analyses identified a transcriptional regulatory module that encompasses terpenoid genes, transcription factors, and enriched drought-responsive elements in the promoter regions of those genes as part of the grapes response to drought. Our study reveals that grapevine berries respond to drought by modulating several secondary metabolic pathways, and particularly, by stimulating the production of phenylpropanoids, the carotenoid zeaxanthin, and of volatile organic compounds such as monoterpenes, with potential effects on grape and wine antioxidant potential, composition, and sensory features.
226 citations
Cites background from "Stress Enhances the Synthesis of Se..."
...[29]), including the recent studies in grapevine leaves...
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References
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TL;DR: During normally-encountered degrees of water deficit the capacity of the antioxidant systems and their ability to respond to increased active oxygen generation may be sufficient to prevent overt expression of damage.
Abstract: Water deficits cause a reduction in the rate of photosynthesis. Exposure to mild water deficits, when relative water content (RWC) remains above 70%, primarily causes limitation to carbon dioxide uptake because of stomatal closure. With greater water deficits, direct inhibition of photosynthesis occurs. In both cases limitation of carbon dioxide fixation results in exposure of chloroplasts to excess excitation energy. Much of this can be dissipated by various photoprotective mechanisms. These include dissipation as heat via carotenoids, photorespiration, CAM idling and, in some species, leaf movements and other morphological features which minimize light absorption. The active oxygen species superoxide and singlet oxygen are produced in chloroplasts by photoreduction of Oxygen and energy transfer from triplet excited chlorophyll to oxygen, respectively. Hydrogen peroxide and hydroxyl radicals can form as a result of the reactions of superoxide. All these species are reactive and potentially damaging, causing lipid peroxidation and inactivation of enzymes. They are normally scavenged by a range of antioxidants and enzymes which are present in the chloroplast and other subcellular compartments. When carbon dioxide fixation is limited by water deficit, the rate of active oxygen formation increases in chloroplasts as excess excitation energy, not dissipated fay the photoprotective mechanisms, is used to form superoxide and singlet oxygen. However, photorespiratory hydrogen peroxide production in peroxisomes decreases. Increased superoxide can be detected by EPR (electron paramagnetic resonance) in chloroplasts from droughted plants. Stiperoxide formation leads to changes suggestive of oxidative damage including lipid peroxidation and a decrease in ascorbate. These changes are not, however, apparent until severe water deficits develop, and they could also be interpreted as secondary effects of water deficit-induced senescence or wounding. Non-lethal water deficits often result in increased activity of superoxide dismutase, glutathione reductase and monodehydroascorbate reductase. Increased capacity of these protective enzymes may be part of a general antioxidative response in plants involving regulation of protein synthesis or gene expression. Since the capacity of these enzymes is also increased by other treatments which cause oxidative damage, and which alter the balance between excitation energy input and carbon dioxide fixation such as low temperature and high irradiance, it is suggested that water deficit has the same effect. Light levels that are not normally excessive do become excessive and photoprotective/antioxidative systems are activated. Some of the photoprotective mechanisms themselves could result in active oxygen formation. Photoinhibitory damage also includes a component of oxidative damage. During normally-encountered degrees of water deficit the capacity of the antioxidant systems and their ability to respond to increased active oxygen generation may be sufficient to prevent overt expression of damage. Desiccation-tolerant tissues such as bryophytes, lichens, spores, seeds, some algae and a few vascular plant leaves can survive desiccation to below 30-40% RWC, A component of desiccation damage in seeds and bacteria is oxygen-dependent. Desiccation causes oxidation of glutathione, a major antioxidant, and appearance of a free radical signal detected by EPR in a number of tissues suggesting that oxidative damage has occurred. In photosynthetic cells damage may arise from photooxidation. Disruption of membrane-bound electron tranport systems in partially hydrated tissue could lead to reduction of oxygen to superoxide. Oxidation of lipids and sulphydryl groups may also occur in dry tissue. Tolerant cells recover upon rehydration and arc able to reduce their glutathione pool. Non-tolerant species go on to show further oxidative damage including lipid peroxidation. It is difficult to attribute this subsequent damage to the cause or effect of death. Embryos in seeds lose desiccation tolerance soon after imbibition. This is associated with membrane damage that has been attributed to superoxide-mediated deesterification of phospholipids and loss of lipophilic antioxidants. These effects are discussed in relation to other mechanisms involved in desiccation tolerance. Contents Summary 27 I. Introduction 28 II. Generation of active oxygen and defence mechanisms in plant cells 29 III. The effect of water deficit on photosynthesis 31 IV. Mechanisms for active oxygen generation during water deficit 36 V. Evidence for oxidative damage during water deficit 39 VI. Desiccation 47 VII. Conclusions 52 Acknowledgements 53 References 53.
2,008 citations
"Stress Enhances the Synthesis of Se..." refers background in this paper
...(SOD) and ascorbate peroxidase (APX), which is characteristic of stress conditions....
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...1); gene expression of typical stress response enzymes, such as SOD and APX, is strongly up-regulated (Mittler and Zilinskas 1994, Acar et al. 2001, Gratao et al. 2005)....
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...The latter is subsequently reduced to water by APX (Smirnoff 1993, Shalata et al. 2001) (Fig....
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...Additional mechanisms which prevent over-reduction of the photosynthetic transport chain are based on the effective reoxidation of NADPH + H+ via photorespiration (Smirnoff 1993, Wingler et al. 2000) or the xanthophyll cycle (Lin et al. 2002, Latowski et al. 2004)....
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...Abbreviations: APX, ascorbate peroxidase; Chl, chlorophyll; GABA, g-aminobutyric acid; SOD, superoxide dismutase....
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TL;DR: Investigating plants under stress can learn about the plasticity of metabolic pathways and the limits to their functioning, and questions of an ecological and evolutionary nature need investigation.
Abstract: Environmental stresses come in many forms, yet the most prevalent stresses have in common their effect on plant water status. The availability of water for its biological roles as solvent and transport medium, as electron donor in the Hill reaction, and as evaporative coolant is often impaired by environmental conditions. Although plant species vary in their sensitivity and response to the decrease in water potential caused by drought, low temperature, or high salinity, it may be assumed that all plants have encoded capability for stress perception, signaling, and response. First, most cultivated species have wild relatives that exhibit excellent tolerance to abiotic stresses. Second, biochemical studies have revealed similarities in processes induced by stress that lead to accumulated metabolites in vascular and nonvascular plants, algae, fungi, and bacteria (Csonka, 1989; Galinski, 1993; Potts, 1994). These metabolites include nitrogen-containing compounds (proline, other amino acids, quaternary amino compounds, and polyamines) and hydroxyl compounds (sucrose, polyols, and oligosaccharides) (McCue and Hanson, 1990). Accumulation of any single metabolite is not restricted to taxonomic groupings, indicating that these are evolutionarily old traits. Third, molecular studies have revealed that a wide variety of species express a common set of genes and similar proteins (for example, Rab-related proteins and dehydrins) when stressed (Skriver and Mundy, 1990; Vilardell et al., 1994). Although functions for many of these genes have not yet been unequivocally assigned, it is likely, based on their characteristics, that these proteins play active roles in the response to stress. Learning about the biochemical and molecular mechanisms by which plants tolerate environmentat stresses is necessary for genetic engineering approaches to improving crop performance under stress. By investigating plants under stress, we can learn about the plasticity of metabolic pathways and the limits to their functioning. Also, questions of an ecological and evolutionary nature need investigation. Are the genes that confer salt tolerance on halophytes and/or drought tolerance on xerophytes evolutionarily ancient genes that have been selected against in saltand drought-sensitive plants (glycophytes) for the sake of productivity? Or have some species obtained nove1 genes in their evolutionary history that have enabled them to occupy stressful environments? How will the
1,763 citations
"Stress Enhances the Synthesis of Se..." refers background in this paper
...In addition, more severe environmental influences, such as various stress conditions, will also impact on the metabolic pathways responsible for the accumulation of secondary plant products (Bohnert et al. 1995)....
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Book•
01 Jan 1977
TL;DR: The Plant and Its Biochemical Adaptation to the Environment, and Higher Plant-Lower Plant Interactions: Phytoalexins and Phytotoxins.
Abstract: The Plant and Its Biochemical Adaptation to the Environment. Biochemistry of Plant Pollination. Plant Toxins and Their Effects on Animals. Hormonal Interactions Between Plants and Animals. Insect Feeding Preferences. Feeding Preferences of Vertebrates, Including Man. The Co-Evolutionary Arms Race: Plant Defence and Animal Response. Animal Pheromones and Defence Substances. Biochemical Interactions Between Higher Plants. Higher Plant-Lower Plant Interactions: Phytoalexins and Phytotoxins. Indices.
1,368 citations
TL;DR: It is proposed that the role of SDE1 is to synthesize a double-stranded RNA initiator of posttranscriptional gene silencing, according to this idea, when a virus induces posttranscriptal genesilencing, the virus-encoded RNA polymerase would produce the double-Stranded RNA and Sde1 would be redundant.
1,139 citations
"Stress Enhances the Synthesis of Se..." refers methods or result in this paper
...Using the whole-plant criterion, the data presented by de Abreu and Mazzafera (2005) showed that in Hypericum brasiliense, the concentration and total amount of phenolic compounds were drastically enhanced in plants grown under drought stress in comparison with the control plants. Despite the fact that the stressed plants were smaller, the product of biomass and natural product concentration yields a 10% increase in the total content of phenolic compounds found in the stressed plants. Furthermore, a similar conclusion can be drawn when evaluating the results of Nogués et al. (1998), who reported a significant increase in the concentration of phenolic compounds in stressed pea (Pisum sativum). The authors found that although the total biomass of the pea plants grown under drought stress was only one-third of that of those cultivated under standard conditions, the overall anthocyanin content (product of biomass and anthocyanin concentration, i.e. the anthocyanins g FW) was around 25% higher in the stressed plants compared with the unstressed plants. In contrast, the total amount of flavanoids was nearly the same, whether the plants were grown under drought stress or under non-stress conditions. In red sage (Salvia miltiorrhiza), the overall content, i.e. the total amount per plant, of furoquinones even decreased slightly under drought stress conditions, although there was a significant increase in their concentration (Liu et al. 2011). With respect to terpenoids, there have been many reports showing that—apart from the drought stress-related increase in their concentration (terpenes g biomass) putatively due to the reduction in dry weight—there was also an effective increase in the terpenoid content on the whole-plant basis. In this manner, the large, drought stress-related increase in monoterpene concentration in sage (Salvia officinalis) was much greater than the corresponding loss in biomass (Nowak et al. 2010). Accordingly, in sage suffering moderate drought stress, the total content of monoterpenes per plant was significantly higher than in the well-watered controls. In contrast, Manukyan (2011), who detected only a slight drought stressrelated increase in monoterpene concentration (terpenes g biomass) in catmint and lemon balm plants, calculated and reported a stress-related decrease in the total content of terpenoids per plant in Melissa officinalis, Nepeta cataria and Salvia officinalis....
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...Using the whole-plant criterion, the data presented by de Abreu and Mazzafera (2005) showed that in Hypericum brasiliense, the concentration and total amount of phenolic compounds were drastically enhanced in plants grown under drought stress in comparison with the control plants....
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...By using virus-induced gene silencing (VIGS), phytoene desaturase, a key enzyme in carotene biosynthesis (Cunningham and Gantt 1998), is commonly used as a marker for successful gene silencing (Dalmay et al. 2000, Turnage et al. 2002)....
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...Using the whole-plant criterion, the data presented by de Abreu and Mazzafera (2005) showed that in Hypericum brasiliense, the concentration and total amount of phenolic compounds were drastically enhanced in plants grown under drought stress in comparison with the control plants. Despite the fact that the stressed plants were smaller, the product of biomass and natural product concentration yields a 10% increase in the total content of phenolic compounds found in the stressed plants. Furthermore, a similar conclusion can be drawn when evaluating the results of Nogués et al. (1998), who reported a significant increase in the concentration of phenolic compounds in stressed pea (Pisum sativum)....
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TL;DR: It is now established that the rate of C02 assimilation in the leaves is depressed at moderate water deficits, mostly as a consequence of stomatal closure, and carbon assimilation may diminish to values close to zero without any significant decline in mesophyll photosynthetic capacity.
Abstract: This review focuses on the effects of water deficits on photosynthesis and partitioning of assimilates at the leaf level. It is now established that the rate of C02 assimilation in the leaves is depressed at moderate water deficits, mostly as a consequence of stomatal closure. In fact, depending on the species and on the nature of dehydration, carbon assimilation may diminish to values close to zero without any significant decline in mesophyll photosynthetic capacity. This remarkable resistance of the photosynthetic apparatus to water deficits became apparent after the measurement of photosynthesis at saturating C02 concentrations was made possible. Whenever light or heat stress are superimposed a decline in mesophyll photosynthesis may occur as a result of a 'down-regulation' process, which seems to vary among genotypes. A major secondary effect of dehydration on photosynthetic carbon metabolism is the change in partitioning of recently fixed carbon towards sucrose, which occurs in a number of species in parallel to the increase in starch breakdown. This increase in compounds of low molecular weight may contribute to an osmotic adjustment. Controlling mechanisms involved in this process deserve further investigation.
1,093 citations
"Stress Enhances the Synthesis of Se..." refers background in this paper
...Water shortage induces partial stomatal closure (Chaves 1991), increasing diffusion resistance for all gases....
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