Abstract
For a long time, plants have been considered as healing agents for treating and preventing different diseases. These beneficial effects are mainly attributed to phenolic compounds. Phenolic compounds have as a basic structure one or more hydroxyl groups (–OH) attached to an aromatic ring. They are classified in two groups: flavonoids and phenolic acids. The regular intake of plant-based foods rich in phenolic compounds has been associated to the prevention and treatment of diseases such as Alzheimer’s, Parkinson’s, cardiovascular problems, atherosclerosis, metabolic syndrome, diabetes, and many types of cancer. Therefore, their demand has increased, so plants are now being used as biofactories for their production. By exposing plants to abiotic and biotic stress, phenolic compounds are synthesized in response to ROS overproduction. Their production has also been raised by increasing the expression of genes involved in phenolic compounds metabolic pathways. Present chapters address the use of biotic and abiotic stress as well as genetic engineering tools for increasing phenolic content in different plants.
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20.1 Introduction
Around 80% of people living in developing countries consider their native plants as the main healing agent for treating and preventing different diseases. This healing power has been attributed to their antioxidant activity and associated to the presence of phenolic compounds (Abdul Qadir et al. 2017).
Phenolic compounds are divided in two groups: flavonoids and phenolic acids. They are among the most investigated phytochemicals in both medicinal and nutritional areas (Del Rio et al. 2010).
Phenols were first isolated in 1834 by Friedlieb Ferdinand Runge and used as a wound dressing, antiseptic, and disinfectant in Germany. One of the first registers was in 1865 where the surgeon Joseph Lister employed them in a tibia fracture surgery (Hugo 1978). Currently, over 8000 different naturally occurring phenolic compounds are known, and the list grows (Tsao 2010).
The main sources of flavonoids are parsley (Petroselinum crispum), celery (Apium graveolens), chamomile (Matricaria chamomilla), Ginkgo biloba, mint (Mentha arvensis), and red pepper (Capsicum annum) (Panche et al. 2016). While the main sources of phenolic acids are green tea (Camellia sinensis), coffee, berries, red wine, and whole cereals such as wheat (Triticum spp.), rice (Oryza sativa), corn (Zea mays), and oats (Avena sativa) (Weichselbaum and Buttriss 2010).
20.2 Chemical Characteristics
Phenolics are comprised in a wide array of compounds derived from the secondary metabolism of plants (Kutchan et al. 2015). Phenolic compounds have as a basic structure one or more hydroxyl groups (–OH) attached to an aromatic ring (Fig. 20.1). The presence of the hydrogen in the –OH groups makes phenolic compounds weak labile acids. Phenolic compounds can be ubiquitously found throughout the plant kingdom where they are usually present as esters or glycosides.
Nowadays, scientific literature uses the terms “phenolic compounds” and “polyphenols” to refer to the widespread subclasses of phenolic compounds, which are grouped according to their chemical characteristics related to their structure and type of compound. However, phenolic compounds are metabolically speaking, only metabolites derived from the shikimate phenylpropanoid and/or the polyketide pathways, with one or more phenolic rings and lacking of nitrogen-based functional groups (Quideau et al. 2011).
Phenolic compounds are the subject of many studies since they have been implicated in a myriad of health-promoting properties. The chronic intake of plant-based foods rich in phenolic compounds has been associated to an onset/prevention of noncommunicable diseases such as Alzheimer’s, Parkinson’s, cardiovascular problems, atherosclerosis, metabolic syndrome, diabetes, and many types of cancer (Del Rio et al. 2010; Fraga et al. 2010; Ozcan et al. 2014). These bioactive effects are attributed to the physicochemical properties related within the phenol functional group, which allows the –OH group to act as hydrogen-bond donor or as an acceptor (Quideau et al. 2011).
20.3 Classification
Phenolic compounds are a diverse group of organic compounds; at least 8000 phenolic structures have been elucidated. Phenolics have an important role in the protection of the plants against biotic or abiotic stress. These molecules are present in most plant tissues, for example, leaves, roots, and edible parts of the plant such as fruits (de la Rosa et al. 2019). Furthermore, phenolics can be found in nature conjugated to sugar moieties and organic acids.
There are several ways to classify phenolic compounds, and nowadays there is not a general agreement in how to categorize them. Besides, their classification can be dependent on the molecule’s different properties. For example, (1) classifying phenolic compounds by their solubility is convenient for explaining the metabolic fate of phenolic compounds since it depends greatly on this property (Santana-Gálvez and Jacobo-Velázquez 2018); (2) based on the chemical structure, phenolic compounds can be categorized by the number of aromatic rings (Fig. 20.2), and this classification has been previously detailed (Santana-Gálvez and Jacobo-Velázquez 2018).
Phenolic compounds can be also classified in flavonoids and non-flavonoids. Flavonoids are the most abundant phenolics in plant kingdom. Its presence in nature is more commonly found in leaves and the skin of fruits (Crozier et al. 2009). The basic structure of flavonoids consists of 15 carbon atoms arranged in 2 phenyl rings named as A and B, linked through a heterocyclic pyran ring named as ring C (Fig. 20.3).
Flavonoids are subdivided into six groups of families, differing in their degree of oxidation and pattern of substitution of the C ring, whereas individual compounds in each family are differentiated by the pattern of hydroxylation and methylation of the rings A and B. The six groups of flavonoids are flavones, flavonols, flavonones, isoflavones, anthocyanidins, and flavan-3-ols (de la Rosa et al. 2019). From these subgroups, flavonols are the most abundant flavonoids; the most representative flavonols are kaempferol, myricetin, quercetin, and isorhamentin (Crozier et al. 2009).
On the other hand, non-flavonoids consist of phenolic acids, stilbenes, lignans, and tannins (Oliveira et al. 2014). The most representative phenolic acid is gallic acid and acts as a precursor for the synthesis of other non-flavonoids such as hydrolysable tannins and stilbenes (Crozier et al. 2009).
20.4 Health-Promoting Properties
20.4.1 Neurodegenerative Diseases
The overrun of the endogenous antioxidant system due to free radicals is one of the main factors involved in the onset of neurodegenerative diseases (Poprac et al. 2017). The adoption of a Mediterranean diet has been associated with a lower incidence of neurodegenerative diseases due to the inclusion of foods such as wine (Valls-Pedret et al. 2015).
The total phenolic compounds in red wine reaches up to 1000 mg/kg. These components exert their antioxidant activity by directly scavenging the reactive oxygen species (ROS) and nitrogen oxygen species (NOS), and by inducing phase II detoxifying enzymes via nuclear factor E2-related factor 2 (Nrf2) activation over in vitro models (Rodriguez-Morato et al. 2015). For the particular case of Parkinson’s disease, (−)-epigallocatechin-3-gallate, the most abundant polyphenol found in tea, and quercetin also found in red wine, protects against oxidative hippocampal neurodegeneration at the time that inhibits L-DOPA (dopamine precursor) methylation on in vivo models (Kang et al. 2013). As for Alzheimer’s, phenolic acids and polyphenols modified by microbiota inhibit amyloid β aggregation, which is associated to cognitive decile in Alzheimer’s disease (Pistollato et al. 2016).
20.4.2 Inflammation
Inflammation is a natural defense process that recognizes harmful environmental stimuli (Neagu et al. 2018). Phenolic compounds such as epicatechin and caffeic acid, found in red Cannonau wine, diminish the intestinal inflammation induced by dietary oxysterols, which are cholesterol auto-oxidation products that may lead to colorectal cancer by preventing the induction of NF-κB-dependent inflammatory events (Guina et al. 2015).
Oleocanthal is a phenolic compound isolated from virgin olive oil with an anti-inflammatory property similar to ibuprofen. It represents 10% of the olive oil phenolic fraction, and it inhibits cyclooxygenase pathway over in vitro monocytes and monocyte-derived macrophages (Lucas et al. 2011). Kaempferol is another phenolic compound with autoinflammatory activity and highly found in golden root (Rhodiola sachalinensis). It reduced nitric oxide production by inhibiting nitric oxide synthase over in vitro LPS-stimulated RAW 264.7 cells (Choe et al. 2012).
20.4.3 Cancer
Cancer is characterized by a loss of cell death capacity and an uncontrolled cell division (Wong 2011). One of the main responsible for cancer onset is ROS, known to regulate signaling molecules required for cell cycle progression and to control the expression of various tumor suppressor genes. Phenolic compounds such as the anthocyanin delphinidin induce apoptosis and cell cycle arrest in several types of cancer by the suppression of the NF-κB pathway. Another target for cancer treatment is matrix metalloproteinase, an enzyme capable of degrade extracellular matrix. It is regulated by peonidin-3-glucoside (Zhou et al. 2016). Many other phenolic compounds have been studied, mainly over in vitro cancer models where cinnamic acid, caffeic acid, coumaric acid, and ferulic acid outstand for their antiproliferative effect over melanoma, prostate, and breast cancer, respectively (Anantharaju et al. 2016).
20.4.4 Cardiovascular Health
The term “cardiovascular diseases” encompasses a set of conditions among which peripheral arterial disease, coronary heart disease, venous thromboembolism, and congenital heart diseases stand out. Foods such as garlic, onion, ginger, and dark chocolate were consumed for a long time for their cardioprotective effect. Know it is known that these effects are due to the high antioxidant contents mainly due to phenolic acid, flavonoids, lignans, and stilbenes (Olas 2017). A high source of stilbenes is grape pomace. Consuming it for 7 days has cardioprotective effects against isoprenaline-induced infarct-like lesion. The effect is associated to the stilbenes trans- and cis-resveratrol, glycosylated derivatives of resveratrol, trans- and cis-piceid, piceatannol, and viniferins (resveratrol dimmers), which reduce oxidative stress (Balea et al. 2018).
20.4.5 Diabetes
The fungi Phellinus igniarius is a rich source of 7,8-dihydroxycoumarin, 3,4-dihydroxybenzalacetone, 7,3′-dihydroxy-5′-methoxyisoflavone, and inoscavin C. These phenolics are considered as potent antidiabetic compounds. All of them increase glucose uptake over in vitro models by up to 2.34-fold. They activate GLUT4 translocation via AMPK pathway modulation (Zheng et al. 2018). Another source of antidiabetic phenolic compounds is Senecio biafrae leaves rich in gallic, chlorogenic, and caffeic acid as well as rutin, quercetin, and kaempferol. Together, these compounds inhibit the activity of alpha-glucosidase preventing the conversion of complex carbohydrates in to simple glucose (Ajiboye et al. 2018).
20.4.6 Obesity
Obesity is a preventable condition characterized by overweight (Hruby and Hu 2015). Hydroxycinnamic acid is considered as a potential compound for the management of obesity health complications. It inhibits macrophage infiltration and NF-kB activation in obese animals. Also, it inhibits the expression of adipokines TNF-α at the time that prevents adipocyte differentiation (Alam et al. 2016). Also, the polyphenols flavan-3-ols, epigallocatechin gallate, genistein, daidzein, curcumin, resveratrol, and quercetin glycosides found mainly in black tea, green tea, soybean, turmeric, grapes, and onion, respectively, have been largely studied and recognized for their control in body weight and fat accumulation. This compound promotes energy dissipation by activating brown adipose tissue, increasing energy expenditure (Mele et al. 2017).
20.4.7 Hyperlipidemia
Hyperlipidemia is caused by an excess of cholesterol, triglycerides, or both, in the bloodstream (Karr 2017). Cinnamon polyphenols are able to inhibit hyperlipidemia in high-fat diet-fed rats by enhancing the expression of the transcription factors SREBP-1c, LXRs, NF-κB, and Nrf2 as well as enzymes such as ACLY and FAS involved in lipid metabolism (Tuzcu et al. 2017).
The most abundant phenolics identified in cinnamon are catechin, (−)-epigallocatechin gallate, syringic acid, gallic acid, vanillic acid, and p-coumaric acid (Lv et al. 2012). Recent studies have shown that Clinacanthus nutans leaves, a medicinal plant endemic to Asia, given to rats for 7 weeks, attenuate the oxidative stress through increasing serum antioxidant activity and upregulating the expression of hepatic antioxidant genes. The effects are attributed to protocatechuic acid (Sarega et al. 2016).
20.4.8 Osteoprotective
Osteoporosis is characterized by bone mass decrease, which can lead to fractures. For a long time, ferns such as Drynaria species have been used to prevent bone loss, specially its rhizome. The active compounds were unknown until recently, where chlorogenic acid, syringic acid, trans-ferulic acid, (−)-epigallocatechin, epigallocatechin gallate, quercetin dehydrate, and luteolin were identified in Drynaria extracts. These extracts increase the cell viability of osteoblastic cells by around 40%, promoting a high cellular density (Kang et al. 2014).
Also, genistein aglycone, a soybean isoflavone, has been known for a long time as a phytochemical that induces bone formation and resorption through the osteoprotegerin-sRANKL system (Bitto et al. 2010). The medicinal effect of some phenolic compounds is described in Table 20.1.
20.5 Strategies to Enhance Phenolic Compounds in Plants
Nowadays phenolic compounds are of greater interest. Their demand has increased by several factors such as a lot of studies attributing them potential health benefits, consumer health concerns, as well as an increased rate of diseases related to aging. Plants are the main source for obtaining phenolic compounds, so techniques have been introduced to increase the plant phenolic content (Ameer et al. 2017). Among them, the use of abiotic and biotic conditions has been found to increase the bioactive compounds such as polyphenols and flavonoids in response to ROS overproduction. By exposing different types of plants to these types of stresses, vegetable tissues with higher antioxidant capacity can be obtained (Abdi et al. 2019; Khan et al. 2019). Another strategy for phenolic increase in plants is genetic manipulation, which has recently emerged since the biosynthetic pathways for phenolic production have been unveiled. Therefore, the expression of genes involved in all of them, especially transcription factors that allow the control of specific enzymes, has been engineered as a promising strategy for medicinal plant production.
These three topics will be discussed in detail throughout this chapter.
20.5.1 Abiotic Stress and Phenolic Compounds in Plants
Plants are continuously subjected to different types of stresses, affecting their normal growth, for example, adverse abiotic conditions such as cold, heat, drought, excess of salt or toxic metals, as well as nutrient imbalance (Zhu 2016).
Abiotic stresses are major limiting factors and responsible for enormous crop yield losses worldwide (Jorge et al. 2016), so omics and biology tools have been used to elucidate the pathways responding to different abiotic stresses conditions.
Over the time, it has been found that these types of stresses are mainly mediated by the overproduction of signaling molecules such as ROS and phytohormones like methyl jasmonate and ethylene. These trigger the overproduction of some phytochemical compounds, for example phenolics, promoting its accumulation (Jacobo-Velázquez and Cisneros-Zevallos 2012).
Phenolic compounds are highly valued biomolecules, so different strategies have been applied to increase its production, including the induction of adverse abiotic conditions. This strategy has been suggested as a replacement of genetic tools; technologies are still considered hazardous.
In Fig. 20.4, the abiotic stress strategies employed for phenolic overproduction in plants are classified.
20.6 Radiation
20.6.1 Light
Visible light is the electromagnetic spectrum visible to the human eye, from 380 to 740 nm. Visible light overexposure triggers strategies of photoprotection to counteract the damage, so it induces photosynthesis to occur, therefore promoting other metabolic pathways to increase (Younis et al. 2010).
Given the above, light-emitting diodes (LEDs) have been used lately to produce crops with special features, including improved nutritional profiles. Red and blue light going from 625–740 to 400–500 nm, respectively, is the most used spectra.
Monochromatic blue LED stimulates the biosynthesis of total phenolics and flavonoids in 2-week-old cherry tomato seedlings after 4 weeks exposure. Total phenolic and flavonoid content increased up to 33.33 and 75%, respectively (Kim et al. 2014). The same happens when applying blue LED over red leaf lettuce plants (Johkan et al. 2010).
In addition of being used for the increase of total phenolic content, LEDs have also been tested for raising particular compounds concentration. Blue and red LEDs tested separately promoted the accumulation of particular compounds in peas. After 4 days exposure, red LED increased catechin content by 14.3%, while chlorogenic acid and rutin content were increased by 26.3 and 18%, respectively, when applying blue LED (Liu et al. 2016).
Besides blue and red LEDs, the white one has been tested. Kale sprouts grown under white or blue LEDs showed an increase of total phenolic compounds of 34.55% and 69.09%, respectively. On the other side, the particular contents of anthocyanin in white, red, and blue LED-exposed grown sprouts were 8.69-, 5.94-, and 18.16-fold higher, respectively, as compared to nonexposed sprouts (Qian et al. 2016).
The combined effect of LEDs has also been evaluated. Blue and red LED increases total phenolic concentration in Sunmang and Grand Rapid lettuces by 55% and twofold, respectively (Son and Oh 2013). Also, chlorogenic acid, vitexin, rutin, quercetin, cyanidin 3-O-glucoside, and cyanidin 3-O-rutinoside concentrations are increased in Tartary buckwheat submitted to blue- and red-combined LED treatment (Seo et al. 2015).
The mechanism by which light radiation exposure works is by overexpressing FtDFR and FtANS. These genes are overexpressed up to 7.1-fold.
20.6.2 UV
Ultraviolet (UV) radiation is classified as UV-A, UV-B, and UV-C, in the range of 320–400, 280–320, and 100–280 nm, respectively (Edward et al. 2014). The application of UV rays affects plants by changing the normal metabolic pathways of photosynthesis, cell division, and any other process related to plant growth and development (Surjadinata et al. 2017). These effects are mainly promoted by reactive species accumulation which induces the expression of antioxidant genes already linked to the UV resistance 8 locus pathway. The above results in the activation of the plant defense system, including the triggering of the phenylpropanoid metabolism which results in the accumulation of secondary metabolites such as phenolic antioxidants. Consequently, UV radiation has been proposed, alone or in combination, as a cheap tool to enhance phenolic compound content in horticultural crops during postharvest life (Formica-Oliveira et al. 2017).
Lettuce, a very important crop worldwide, has been used as a plant factory to accumulate phenolic compounds. Total phenolic content (especially anthocyanins) and total antioxidant capacity were increased by 30 and 40%, respectively, without growth inhibition after 4 d UV-A exposure. The above was attributed to an increase in phenylalanine ammonia lyase (PAL) gene expression (a key gateway gene for the biosynthesis of phenolic compounds), and therefore PAL activity was increased (Lee et al. 2013). PAL is the first enzyme in the phenylpropanoid pathway.
On the other hand, UV-B applied to plants such as Vitis vinifera grape skin after defoliation and until harvest, alters the expression of 121 phenylpropanoid biosynthesis-related genes, including VvFLS1, VvGT5, VvGT6, VvHY5–1, VvHY5–2, and VvRU. Also, PAL and chalcone synthase gene expression was increased. These gene products are involved in the flavonol and monoterpenoid biosynthetic pathways. Among the compounds which concentration was highly increased by UV-B light application, there was syringic acid, caffeoyl tartaric acid, and resveratrol, which increased by 13%, 40%, and twofold, respectively, as compared to nonexposed plants (Rodríguez-Calzada et al. 2019).
The exposure to UV-C also increases resveratrol production in grapes, especially in Vitis amurensis and Vitis labrusca grapes. The mechanism is by PAL and stilbene synthase increased expression, where PAL is the first enzyme of the phenylpropanoid pathway, and stilbene synthase is responsible for catalyzing the reaction of resveratrol formation. Also, chalcone synthase gen had higher expressions. As for epigenetic changes, UC-V decreases methylation levels of VaSTS2, VaSTS6, and VaSTS10 genes (Tyunin and Kiselev 2016). The above has also been documented for other plants such as shell ginger (Alpinia zerumbet) and in lemon pomace (Xuan et al. 2016; Papoutsis et al. 2016).
The effect of different types of UV radiation has been compared. For example, UV-A and UV-B over broccoli sprouts both particularly change their phenolic profiles. Applying UV-A during 120 min increased gallic acid hexoside I (~14%), 4-O-caffeoylquinic acid (~42%), gallic acid derivative (~48%), and 1-sinapoyl-2,2-diferulolyl-gentiobiose (~61%), and by applying UV-B, sinapoyl malate (~12%), gallotannic acid (~48%), and 5-sinapoyl-quinic acid (~121%) were increased (Moreira-Rodríguez et al. 2017).
UV irradiation must be exploited for the production of functional foods rich in bioactive phytochemicals. This has been highly recognized and utilized for sunscreens and cosmetics production (Takshak and Agrawal 2019).
The results obtained in terms of phenolic accumulation in different plant materials by applying radiation are summarized in Table 20.2.
20.7 Temperature
20.7.1 Cold
Cold stress has been applied to different plant materials. It is classified as either chilling or freezing, above and below 0 °C, respectively (Pareek et al. 2017). This condition promotes stress, affecting physiological, biochemical, molecular, and developmental processes of plants. Different results have been found when it comes to cold stress and phenolics plant production. In some cases, the content increases, but in others it is reduced or maintained. These will depend mainly on the intensity and duration of the stress, as well as on the plant material (Hajihashemi et al. 2018).
For example, when exposing Vitis vinifera leaves at 7 °C during a week, a reduction in total phenolic content of up to 22.05% has been observed, especially in caffeic acid, p-coumaric acid, ferulic acid, and caffeic acid. Also, tannin content of Vitis vinifera leaves exposed below 0 °C was reduced up to 15.9% (Król et al. 2015).
On the contrary, low temperatures increase phenolic content in other plants such as kale, cabbage, papaya, and olive tree leaves. In Kale and cabbage stored at 12 °C, phenolic content was increased by 65.71 and 60%, respectively, as compared to normal temperature conditions (Soengas et al. 2018). Regarding to Maradol papaya, storing it at chilling conditions (1 °C) promotes phenolic accumulation compared with those stored at normal 25 °C conditions. The compounds increased after 8 days of storage were ferulic acid and caffeic acid by 40 and by twofold, respectively. As for freezing, olive tree leaves submitted below −7 °C for 15 days showed an increase in PAL expression by up to 4.8-fold, promoting a total phenolic increase of 12% (Ortega-García et al. 2008).
It was found that low-temperature exposure changed gene expression after 24 h treatment. Genes codifying for enzymes such as PAL and chalcone synthase were increased by 8- and 50-fold, respectively, and 4-coumarate, CoA ligase and chalcone isomerase, increased by threefold. The expression of these genes is back to normal after returning the plants to 25 °C during 2 days (Christie et al. 1994).
Also, in other plants such as chickpea, submitting the seeds to cold stress promoted an increased expression of PAL and cinnamyl alcohol dehydrogenase genes. This indicates the crucial role of phenylpropanoid pathway in creating cold tolerance (Rakei et al. 2016).
20.7.2 Heat
The main use of heat in food industry is for reducing microbial levels. Nevertheless, it has been found that a lot of biochemical pathways are overexpressed in plants subjected to high temperature which in turn increases phytochemicals synthesis (Zhu 2016).
Heat shock at 100 °C was applied over fresh-cut carrots, increasing their phenolic content by 73.98% after 7 days of the heat shock application. Nevertheless, after 10 days the content starts to decrease. Phenolic compound accumulation was due to phenylpropanoid pathway activation. The most increased compound in wounded carrot is caffeoylquinic acid (Alegria et al. 2012). Six wheat genotype seedlings submitted to 45 °C during 20 h showed an increase of total phenolic content by about 40% in all genotypes (Ahmad et al. 2014).
The production and accumulation of phenolics according due to high temperatures will depend on the vegetable tissue. For example, fresh-cut carrots and onions accumulate more phenolics at 20 °C, while celery does it at 10 °C (Xiaoan et al. 2017).
Heat effect, as for the other stresses, is mainly the same. During heat, cell disruption may occur, liberating cytosolic ATP into the extracellular matrix. This ATP is recognized by receptors in the far cell’s membrane increasing cytosolic Ca2+ concentrations, which activates NADPH oxidase and thus ROS and NOS production. ROS and NOS act as signals to activate PAL, and the plants answers back by producing antioxidant molecules as a defense system (Jacobo-Velázquez et al. 2011). The results obtained in terms of phenolic accumulation in some plant materials by applying different temperatures are summarized in Table 20.3.
20.8 Salinity
Around 20% of the world’s irrigated lands have an excess of salt content, known as salinity. Salinity affects plants in multiple ways, for example, blocking respiration, inhibiting photosynthesis, and disordering metabolism and growth processes (Zhao et al. 2017). Nutritional quality of buckwheat sprouts under salinity was estimated. Here, the exposure time (from 1 to 7 days) and the salt concentrations (10, 50, and 100 mM) were evaluated. It was concluded that the most extreme conditions (100 mM for 7 days) resulted in the most effective condition to increase the phenolics content by 153%. The main increased phenolics were isoorientin, orientin, rutin, and vitexin. Previous studies have shown most of the phenolic compounds are generated by the phenylpropanoid pathway, which is stimulated by biotic and abiotic stresses (Lim et al. 2012). This effect is also associated to the increased in plant hormones production, including jasmonic acid and its methylated derivate (methyl jasmonic acid). These hormones induce enzyme production involved in the phenylpropanoid pathway, including PAL, thereby resulting in the accumulation of phenolic compounds (Lim et al. 2012).
Biosynthesis of phenolics was also stimulated in other plants such as olive cultivar leaves by irrigating them every 3 days during 1 month with 125 mM NaCl. Salinity stimulated the biosynthesis of phenolics by increasing its total content up to 129%. From them, the content of oleuropein, the most abundant phenolic from olive tree and oil, was increased by 3.8-fold (Petridis et al. 2012a). Similarly, a high salinity concentration of 300 mM Nacl was evaluated over Salvia coccinea leaf, increasing the total phenolic content by 17% (Grzeszczuk et al. 2018).
Salinity stress (5 dS/m) was applied to both susceptible and tolerant rice varieties. Total phenolics and flavonoids, as well as vanillin, ferulic acid, p-coumaric acid, and protocatechuic acid, were increased in tolerant varieties. Phenolic compounds were increased around 48% while flavonoids only 17.15%. In contrast they were markedly reduced in the susceptible cultivars (Jamalian et al. 2013). The enhancement in the synthesis of flavonoids and phenolics of strong tolerant varieties might be due to the adaptive mechanism of rice under salt stress. The presence of ferulic acid under osmotic stress may be related to the strengthening of the plant cell wall and the overall cell elongation. Also, they are possibly found in bounded forms with sugar or glycoside (Minh et al. 2016). It is believed that the salinity stress also enhances the phenolic compound production by the abscisic acid increased content in plants. The results obtained in terms of the phenolic accumulation in different plant materials by applying different salinity stresses are summarized in Table 20.4.
20.9 Chemical Stress
20.9.1 Oxidative
Oxidative stress is the result of unfavorable biotic and abiotic conditions. It also can be artificially induced by ROS such as superoxide (O2−) and hydrogen peroxide (H2O2) addition.
Common daisy (Bellis perennis L.) callus was submitted to 10 mM H2O2 for 10 h. The treatment with H2O2 allowed the detection of kaempferol, myricetin, quercetin, and isorhamnetin, compounds not detected in the control (0 mM H2O2). Also, total phenolic content was increased by 29.25% after H2O2 exposure. Furthermore, as a result of oxidative stress, SOD and CAT were increased.
It was found that CAT, SOD, total phenolic, total flavonoid, and proline activity had a significant positive correlation with the phenolic accumulation under H2O2 pretreatment. The in vitro culture methods under controlled laboratory conditions, such as the one studied in this investigation, have been of great interest for the production of bioactive molecules (Karakas et al. 2015).
20.9.2 Heavy Metals
Heavy metals are considered as one of the most dangerous pollutants (Morkunas et al. 2018). When plants are in the presence of these compounds, phytochemicals such as phenolic compounds are overproduced and accumulated to protect the plant against toxicity. When plants are exposed to heavy metals, phenolic compounds are mostly increased, since they function as metal chelators and participate in ROS scavenging (Malčovská et al. 2014).
Cadmium (Cd2+) and lead (Pb2+) exposure (50 and 10 ppm, respectively) during 2 weeks increased the total phenolics in corn (Zea mays) leaves by around 41.17 and 47%, respectively. The main phenolic compounds increased were chlorogenic acid and rutin; on the other hand, the level of other compounds such as caffeic acid and ferulic acid was decreased (Kısa et al. 2016). Another heavy metal evaluated over plants is nickel (Ni). When exposing chamomile (Matricaria chamomilla) to 120 μM Ni during 10 days, polyphenol oxidase activity was decreased, but an increase in the total phenolic compounds (by 18%) and in PAL activity as well as in shikimate dehydrogenase was observed. Another enzyme production, such as cinnamyl alcohol dehydrogenase, was not affected. Also, in leaf rosettes it was detected an increase in chlorogenic acid accumulation (9.02%), as well as protocatechuic acid (7.47%) (a compound with chelating strength) and caffeic acid (153%) (Kováčik et al. 2007).
Transcriptional and post-transcriptional analysis of soybean and lupine roots exposed to Cd2+ (25 mg/l) or Pb2+ (350 mg/l) was carried out. Here, it was found that under heavy metal stress, there was a transcriptional and post-transcriptional control of PAL expression. For soybean, both metals increased PAL expression, while for lupin only Pb2+. Due to the above, it is concluded that heavy metal stress imposed by Cd2+ and Pb2+ can cause an induction in the phenylpropanoid pathways of soybean and lupin (Pawlak-Sprada et al. 2011).
Cd2+ effect (5 μg/g soil) was also evaluated over Erica andevalensis. This heavy metal increased cinnamic acid derivatives (by threefold), epigallocatechin (81.78%), and rutin (32.32%). Nevertheless, when cadmium concentration was increased up to 50 ug/g, the synthesis and release of phenolics were reduced. So, the excess of cadmium may reduce the synthesis of phenolics to avoid deleterious effect caused by the phenoxyl radicals’ production. The overall results showed that the phenolic compounds play an important role in the cadmium defense of E. andevalensis (Márquez-García et al. 2012).
Maize plants (Zea mays L.) have also been exposed to a Cd2+ stress (50 μM). Hydroponically grown maize superoxide radicals were increased by up to 1.6-fold. Nevertheless, total phenolic content in maize leaf was barely increased by this Cd2+ concentration. It is thought that the presence of high amounts of Cd2+ is related to the phenolics involvement in lignin biosynthesis, affecting the pool of free phenols in the plant tissue, which has also been reported in cucumber plants (Malčovská et al. 2014).
Besides Cd2+, Pb2+, and Ni, other heavy metals such as cobalt (Co2+) and silver (Ag+) have been tested. Solutions of 5 μM of Co2+, Ag + , and Cd2+ have been added to Vitis vinifera cell suspension cultures. An increase of 3-O-glucosyl-resveratrol up to 1.6-fold after 4 h exposure was observed, not affecting cell viability. Cell viability was only affected when heavy metal concentrations increased up to 25 μM (Cai et al. 2013). Other studies in terms of phenolic accumulation in different plant materials by applying different heavy metals are summarized in Table 20.5.
20.10 Mineral Deficiency and Excess
Plants need at least 14 minerals to grow optimally. If there is a deficit or an excess of one of them, crop yield may be affected. There are some minerals required in large amounts (nitrogen, phosphorus, potassium, calcium, magnesium, and sulfur), while others are needed to a lesser extent (chlorine, boron, iron, manganese, copper, zinc, nickel, and molybdenum). It has been observed that the concentration of nutrient elements, such as minerals, is related with the accumulation of plant defense metabolites.
The excess of minerals such as copper (Cu) has a pronounced effect increasing PAL, shikimate dehydrogenase, cinnamyl alcohol dehydrogenase, polyphenol oxidase, and ascorbate peroxidase activity in chamomile plants exposed to 10 uM Cu during 7 days. Due to this, protocatechuic acid, p-OH benzoic, vanillic acid, syringic acid, p-coumaric acid, ferulic acid, and chlorogenic acid were increased by 63.47, 137.5, 44, 33.55, 76.38, 58.33, and 107%, respectively (Kováčik et al. 2009).
Cu excess effect has also been evaluated over other plants. It has been reported that 1.0 uM of Cu increases total phenolic content by 19% in rosemary leaves (Rosmarinus officinalis L.), compared to normal levels. Cu excess in sorghum also increases total phenolic content (Hejazi et al. 2012). Cu levels of 0.5 mM in red cabbage increased anthocyanin concentrations by 126.7% due to oxidative stress induction and enhancement of thiobarbituric acid reactive substances in all the plant, suggesting that these flavonoids are synthesized to neutralize ROS (Posmyk et al. 2009). The excess of some minerals induces other many alterations in plants, for example, it affects the uptake of other essential nutrients.
Mineral deficiency also alters the content of phenolic compounds. Nitrogen and potassium deficiency in American ginseng increases the concentration of vanillic acid, p-coumaric acid, and trans-cinnamic acid. Nevertheless, the opposite effect was observed after phosphorus deficiency, where total phenolic content decreased (Du et al. 2011).
Nitrogen deprivation during 19 days on tomato (Solanum lycopersicum) leaf increases chlorogenic acid and rutin by 136 and 117%, respectively. It was reported that this increase in phenolic compounds was maintained even when the plant was again exposed to normal nitrogen levels (Bénard et al. 2011). When nitrogen deprivation is combined with an exposure to 12 °C for 8 days, flavonoids levels are also enhanced. The responsible are structural genes in the phenylpropanoid and flavonoid pathway enhancement. From this, eight of the ten structural genes involved in flavonol metabolism showed enhanced expression, including phenylalanine ammonia lyase, chalcone synthase, flavanone 3-hydroxylase, and flavonol synthase (Løvdal and Lillo 2009).
Data in terms of phenolic accumulation in different plant materials by submitting them to mineral excess or deficiency is summarized in Table 20.6.
20.11 Water
20.11.1 Flooding
Flooding, also known as submergence, is a scenario where the plant is totally or partially immersed in water. Due to limited oxygen uptake, anaerobic metabolism may result in the accumulation of phytochemical end-products generated for the plant to survive. Different varieties of sweet potatoes, Taoyuan 2, Sushu 18, and Simon 1, have been tested after flooding treatments where flavonoid content was increased by 11, 4, and 4%, respectively (Lin et al. 2006). More studies are required in this and other plant species to investigate the underlying mechanism.
20.11.2 Drought
Water deficiency promotes a change in biological processes such as photosynthesis, respiration, nutrient metabolism, and secondary metabolism which results in reduced plant growth and also in phytochemicals accumulation (Jaleel et al. 2009; Marchese et al. 2010).
Agave salvia, a plant used in the central and north regions of Mexico for the elaboration of alcoholic beverages, has been exposed to drought conditions not showing differences in its phenolic profile, nor in the concentration as compared to normal conditions. This is because Agave salmiana is a stress-tolerant plant, so its phenylpropanoid biosynthesis is not affected (Puente-Garza et al. 2017).
In the case of plants such as Vitis vinifera, a change in their phenolic content was seen after drought stress. Vitis vinifera roots and leaves under drought stress showed a reduction in total phenolic compounds by 9 and 30%, respectively. Caffeic acid, p-coumaric acid, and ferulic acid were the main phenolic compounds affected. The above promote a lowering on the antioxidant potential (Król et al. 2014). This reduction may be explained by the phenylpropanoid and shikimate pathway enzymes reducing their activity under drought stress, which has been observed in other plants.
On the contrary, other plants increase its phenolic compound production to avoid the oxidative damage caused by the lack of water, mainly those not used to drought conditions.
Plants such as Aristotelia chilensis, a berry native to Chile, increased anthocyanin concentration by upregulation of key anthocyanin pathway genes such as dihydroflavonol 4-reductase, UDP-glucose: flavonoid 3-O-glucosyl transferase (UFGT) and MYB R2R3-type transcription factors such as Myeloblastosis A1 (MybA1) and Myeloblastosis 5A (González-Villagra et al. 2018). This mechanism of enhanced phenolic compounds due to drought stress has also been observed in Achillea species and Amaranthus tricolor, where a 75% of water supply reduction increased the total phenolic and total flavonoid content by up and twofold and 38%, respectively (Sarker and Oba 2018). Also, a reduction of 67% water supply in olive tree (Olea europaea) increased the phenolic compounds by around 35% (Petridis et al. 2012a).
After a long drought stress exposure of 3 weeks, Codonopsis lanceolata leaf and roots showed a total phenolic content increase up to 150%, being the predominant compounds catechin, benzoic acid, chlorogenic acid, ferulic acid, gallic acid, rutin, and vanillic acid. The responsible mechanism was an overexpression of 5-enolpyruvylshikimate-3-phosphate (EPSP) synthase, an enzyme in the shikimate pathway, involved in the synthesis of aromatic amino acids such as phenylalanine and tyrosine, the precursors in the phenylpropanoid biosynthesis (Ghimire et al. 2017).
Gene expression is also very affected after drought stress in plants such as potato, where PAL, HCT, HQT, C3H, CHS, CHI, F3H, DFR, and AN1expression was induced, which is related to an altered sucrose flux. The overexpression of HQT has also been documented in Solanaceae species exposed to drought, like in the case of tomatoes, where chlorogenic acid is accumulated in response that overexpression of HQT (André et al. 2009). The results obtained in terms of phenolic accumulation in different plant materials by submitting them to water deficiency are summarized in Table 20.7.
20.12 Wounding
Wounding methods have been applied as postharvest strategies for increasing phenolic content in different plants. Potato tubers are one of them. They were sliced, pie-cutted, or shredded followed by 144 h at 10 °C storage. The highest phenolic compound content was found in sliced potato tubers, where the content of these compounds increased by twofold. The most abundant phenolic compounds were chlorogenic acid (CGA), neo-chlorogenic acid (neo-CGA), and crypto-chlorogenic acid (crypto-CGA). Wounding stressed potato could be used as a starting material for the extraction of high-value antioxidant phenolic compounds with potential applications in the pharmaceutical and dietary supplement industries (Torres-Contreras et al. 2014).
One of the vegetables more studied in terms of wounding is carrots, where it has been found that the higher the wounding intensity, the higher the phenolic accumulation. It is possible to increase the total phenolic content by 2.5-fold and the antioxidant capacity to 12.4-fold when wounding at 23.5 cm2/g. By this it is induced the synthesis of chlorogenic acid and 3,5-dicaffeoylquinic acid (Surjadinata and Cisneros-Zevallos 2012).
Other vegetables such as lettuce, cilantro, cabbage, green beans, apples, plums, peaches, strawberries, bell peppers, asparagus, celery, carrots, radishes, potatoes, and jicama have been submitted to wounding stress and exogenous ethylene and methyl jasmonate. The combination of wound stress and phytohormones resulted in increased PAL activity in some vegetables. Nevertheless, the response was tissue-dependent since the phenolic content of asparagus, cabbage, apples, tomatoes, and pears was not affected (Heredia and Cisneros-Zevallos 2009). Wounded vegetables that are included in most people regular diet may be considered as an inexpensive source to obtain phenolic compounds and thereby to promote the increase in antioxidants ingest.
20.13 Biotic Stress and Phenolic Compounds in Plants (Gabriela)
Phenolic compounds are synthesized by the secondary metabolism of plants, and it is used as a mechanism of defense against different biotic and abiotic stress. The metabolic pathways for the synthesis of phenolic compounds and other secondary metabolites can be manipulated, specifically promote their synthesis. Therefore, the study of the methods that enhance the production of secondary metabolites is currently of scientific interest. Biotic elicitors are molecules produced by living organisms, such fungus or formed by the plant itself. Plant cell cultures have been used to study the potential of some elicitors in the production of phenolic compounds. Chitosan has been the most reported biotic elicitor in the recent years. Chitosan is a polysaccharide composed of β-(1–4)-linked d-glucosamine and N-acetyl-d-glucosamine randomly distributed within the polymer. This polysaccharide is a structural component of the cell wall of fungi which are pathogens to plants. In plants, chitosan acts as elicitor of plant defensive mechanisms (Cheung et al. 2015; Ferri and Tassoni 2011).
The application of chitosan and irrigation frequencies has been evaluated for the enhancement of essential oils and phenolic content of Salvia officinalis L. The foliar application of chitosan (0.5 g/L) and reduced irrigation showed the maximum concentration of phenolic compounds in Salvia officinalis L. (Vosoughi et al. 2018). Chitosan has been applied as elicitor in many plants. For instance, in spinach, chitosan (0.1 mg/mL) increased the content of phenolic and flavonoids, with an increase in the antioxidant activity (Singh 2016). Other biotic elicitors are yeasts, and they have been evaluated and compared to the action of chitosan. Yeast and chitosan were evaluated as the biotic stressors on Rumex cyprius and showed to enhance the phenolic accumulation with an increase in the antioxidant activity. The maximum antioxidant activity was obtained with yeasts at 200 and 400 mg/mL, whereas the level of chitosan was not a determinant of the antioxidant activity since the low and high levels showed significant results. Furthermore, yeast showed to promote the formation of new phenolics such as gallic and chlorogenic acid (Al Khateeb et al. 2016). Furthermore, low concentration of yeast (50 mg/L) has been reported to enhance the production of phenolic compounds in adventitious root cultures of Polygonum multiflorum (Ho et al. 2018b).
The mechanism of action of fungal chitosan is the induction of the activities of defensive enzymes, as showed in Zanthoxylum bungeanum stems, where this effect triggers the total phenolic content production (Li et al. 2016). Therefore, fungal elicitors can stimulate the secondary metabolite production. These elicitors can enhance the enzymatic activity of defensive enzymes such as PAL and chalcone isomerase (Simic et al. 2015).
20.14 Genetic Enhancement of Phenolic Compounds in Plants
As it has been previously mentioned, several strategies have been studied to enhance the content of phenolic compounds in plants, most of them involve physiological approaches such as manipulation of biotic and abiotic stresses in plants to trigger the metabolic biosynthetic pathways leading to the overproduction of phenolic compounds. These works have combined high-throughput massive DNA sequencing and metabolic profiling technologies, leading to the development of a new area of study called phytochemical genomics. Thus, the physiological manipulation of phenolic compounds enhancement has led to the discovery of the metabolic pathway of phenolics biosynthesis through the identification of key genes involved in the phenolic pathway (Saito 2013). On this subject, there are different genomic techniques from which plants can be genetically modified. Eckerstorfer et al. (2019) listed some of the most widely used GM techniques such as “genome editing with site-directed nucleases, genome editing directed by synthetic oligonucleotides, RNA directed DNA methylation, cisgenesis and intragenesis, transgrafting, agro-infiltration, haploid induction and accelerated breeding.” For a more detailed research on this matter, we recommend the work by Eckerstorfer et al. (2019). A summary of recent studies regarding functional genomics on enhancement of phytochemical content of plants is found on Table 20.8. However, even though genomic manipulation is a promising technique to enhance phenolic compounds in crops and medicinal plants, the regulatory framework in the world limits its widespread distribution. In this regard, some authors have published strategies and recommendations for countries that desire to regulate GMO applications; nonetheless, regulation frameworks vary among countries; thus there is currently no international harmonization (Eckerstorfer et al. 2019). Release of GMOs is regulated by government agencies; for instance, the US Department of Agriculture, the Food and Drug Administration, and the Environmental Protection Agency are the organizations that regulate release of GMO in the USA; Europe is regulated by the European Food Safety Authority; England is regulated by the Department for Environment Food and Rural Affairs; Mexico is regulated by the Federal Commission for the Protection Against Sanitary Risk (Eckerstorfer et al. 2019; Estados Unidos Mexicanos 2005). On this subject, Ichim (2019) stated that Romania was one of the first European countries adopting GM crops for commercial cultivation; however after 17 years, cultivation stopped, but it’s excepted to continue with this activity in spite of the European Union block on authorization regarding the cultivation of GM crops. Up to date, France, Germany, Poland, Italy, Austria, Hungary, Lithuania, Latvia, Bulgaria, and Greece are European countries that still restrict the cultivation of GM crops (Ichim 2019). Restrictions arise not due to concerns regarding safety to human and animal health but to concerns regarding the release in the environment of authorized or unauthorized GM crops (Rostoks et al. 2019).
20.15 Conclusions
Phenolic compounds are in great demand, mainly for their potential in treating and preventing noncommunicable diseases. Harvest and postharvest exposure to unfavorable conditions such as abiotic stress can be used as an alternative to accumulate total or specific phenolic compounds in different plant materials. By abiotic stress exposure, high commercially valued plants with high antioxidant activity can be produced. These adverse conditions mediate the overproduction of signaling molecules, such as reactive oxygen species and phytohormones like methyl jasmonate and ethylene, triggering the overproduction of phenolics, mainly by the overexpression of phenylalanine ammonia lyase, the enzyme involved in the first step of the phenylpropanoid metabolism. The production and accumulation of phenolic compounds by abiotic stress induction depend on the stimulus intensity as well as on the vegetable tissue. Generally, the more the plant is removed from its comfort zone, the greater the production of these phytochemicals. One of the most promising strategies of abiotic stress induction is by wounding plant matrices. This strategy that can be even carried out household to increase the consumption of antioxidant compounds.
Another tool for phenolic compound overproduction is biotic stress, where elicitors are mainly used for increasing the production of phenolic compounds in plants cell culture. This is a promising strategy for the production and subsequent recovery and purification of compounds of interest, aiming to generate food supplements or drugs.
Because of the metabolic pathway for phenolic compounds synthesis is now known, genetic engineering has emerged as another option to increase their production. However, since the regulatory framework has not been developed enough, the use of this particular tool is still limited. Numerous in vivo and in vitro studies have shown the bioactivity of polyphenols, so increasing the consumption of these natural compounds emerges as a promising alternative for treating and preventing health disorders related to oxidative stress. Here, we discussed three alternatives to achieve it.
References
Abdi G, Shokrpour M, Karami L, Salami SA (2019) Prolonged water deficit stress and methyl Jasmonate-mediated changes in metabolite profile, flavonoid concentrations and antioxidant activity in peppermint (Mentha x piperita L.). Not Bot Horti Agrobot Cluj Napoca 47(1):70–80
Abdul Qadir M, Shahzadi SK, Bashir A, Munir A, Shahzad S (2017) Evaluation of phenolic compounds and antioxidant and antimicrobial activities of some common herbs. Int J Anal Chem 2017:1–6
Ahmad HS, Abbasi KY, Hameed HA, Hussain J (2014) Survey and documentation of medicinal plants traditionally used for different ailments in district Lodhran, Punjab. Pak J Med Plants Res 3(4):142
Ajiboye BO, Ojo OA, Okesola MA, Akinyemi AJ, Talabi JY, Idowu OT, Fadaka AO, Boligon AA, Anraku de Campos MMJFS, Nutrition (2018) In vitro antioxidant activities and inhibitory effects of phenolic extract of Senecio biafrae (Oliv and Hiern) against key enzymes linked with type II diabetes mellitus and Alzheimer’s disease. Food Sci Nutr 6(7):1803–1810
Al Khateeb W, Alu’datt M, Al Zghoul H, Kanaan R, El-Oqlah A, Lahham J (2016) Enhancement of phenolic compounds production in in vitro grown Rumex cyprius Murb. Acta Physiol Plant 39(1):14
Alam MA, Subhan N, Hossain H, Hossain M, Reza HM, Rahman MM, Ullah MOJN (2016) Hydroxycinnamic acid derivatives: a potential class of natural compounds for the management of lipid metabolism and obesity. Nutr Metab 13(1):27
Alegria C, Pinheiro J, Duthoit M, Gonçalves EM, Moldão-Martins M, Abreu M (2012) Fresh-cut carrot (cv. Nantes) quality as affected by abiotic stress (heat shock and UV-C irradiation) pre-treatments. LWT Food Sci Technol 48(2):197–203
Ameer K, Shahbaz HM, Kwon J-H (2017) Green extraction methods for polyphenols from plant matrices and their byproducts: a review. Compr Rev Food Sci Food Saf 16(2):295–315
Anantharaju PG, Gowda PC, Vimalambike MG, Madhunapantula SV (2016) An overview on the role of dietary phenolics for the treatment of cancers. Nutr J 1(1):99
André CM, Schafleitner R, Legay S, Lefèvre I, Aliaga CA, Nomberto G, Hoffmann L, Hausman J-F, Larondelle Y, Evers D (2009) Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry 70(9):1107–1116
Balea ŞS, Pârvu AE, Pop N, Marín FZ, Pârvu M (2018) Polyphenolic compounds, antioxidant, and cardioprotective effects of pomace extracts from Fetească Neagră cultivar. Oxidative Med Cell Longev 2018:1–11
Bénard C, Bourgaud F, Gautier H (2011) Impact of temporary nitrogen deprivation on tomato leaf phenolics. Int J Mol Sci 12(11):7971–7981
Bitto A, Polito F, Squadrito F, Marini H, D’Anna R, Irrera N, Minutoli L, Granese R, Altavilla D (2010) Genistein aglycone: a dual mode of action anti-osteoporotic soy isoflavone rebalancing bone turnover towards bone formation. Curr Med Chem 17(27):3007–3018
Cai Z, Kastell A, Speiser C, Smetanska I (2013) Enhanced resveratrol production in Vitis vinifera cell suspension cultures by heavy metals without loss of cell viability. Appl Biochem Biotechnol 171(2):330–340
Cheung RC, Ng TB, Wong JH, Chan WY (2015) Chitosan: an update on potential biomedical and pharmaceutical applications. Mar Drugs 13(8):5156–5186
Choe KI, Kwon JH, Park KH, Oh MH, Kim MH, Kim HH, Cho SH, Chung EK, Ha SY, Lee MW (2012) The antioxidant and anti-inflammatory effects of phenolic compounds isolated from the root of Rhodiola sachalinensis A. BOR Mol 17(10):11484–11494
Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194(4):541–549
Chung IM, Rekha K, Rajakumar G, Thiruvengadam M (2016) Production of glucosinolates, phenolic compounds and associated gene expression profiles of hairy root cultures in turnip (Brassica rapa ssp. rapa). 3Biotech 6(2):175
Crozier A, Jaganath IB, Clifford MN (2009) Dietary phenolics: chemistry, bioavailability and effects on health. Nat Prod Rep 26(8):1001–1043
de la Rosa LA, Moreno-Escamilla JO, Rodrigo-García J, Alvarez-Parrilla E (2019) Phenolic compounds. In: Yahia EM, Carrillo-Lopez A (eds) Postharvest physiology and biochemistry of fruits and vegetables. Woodhead Publishing, Duxford, pp 253–271
Del Rio D, Costa LG, Lean MEJ, Crozier A (2010) Polyphenols and health: what compounds are involved? Nutr Metab Cardiovasc Dis 20(1):1–6
Du J, Yang J, Jiao X, Gao W (2011) Effect of nitrogen, phosphorus and potassium deficiency on content of phenolic compounds in exudation of American ginseng. Zhongguo Zhong Yao Za Zhi 36(3):326–329
Eckerstorfer MF, Engelhard M, Heissenberger A, Simon S, Teichmann H (2019) Plants developed by new genetic modification techniques – comparison of existing regulatory frameworks in the EU and non-EU countries. Front Bioeng Biotechnol 7(26):1–16
Edward TL, Kirui M, Omolo JO, Ngumbu RG, Odhiambo PM (2014) Effect of ultraviolet-A (UV-A) and ultraviolet-C (UV-C) light on mechanical properties of oyster mushrooms during growth. Biophys J 2014:1–6
Ferri M, Tassoni A (2011) Chitosan as elicitor of health beneficial secondary metabolites in in vitro plant cell cultures. In: Richard GM, Jennifer MT (eds) Handbook of chitosan research and application, pp 1–25
Formica-Oliveira AC, Martínez-Hernández GB, Díaz-López V, Artés F, Artés-Hernández F (2017) Effects of UV-B and UV-C combination on phenolic compounds biosynthesis in fresh-cut carrots. Postharvest Biol Technol 127:99–104
Fraga CG, Galleano M, Verstraeten SV, Oteiza PI (2010) Basic biochemical mechanisms behind the health benefits of polyphenols. Mol Asp Med 31(6):435–445
Ghimire BK, Seong ES, Yu CY, Kim SH, Chung IM (2017) Evaluation of phenolic compounds and antimicrobial activities in transgenic Codonopsis lanceolata plants via overexpression of the γ-tocopherol methyltransferase (γ-tmt) gene. S Afr J Bot 109:25–33
Giampieri F, Gasparrini M, Forbes-Hernandez TY, Mazzoni L, Capocasa F, Sabbadini S, Alvarez-Suarez JM, Afrin S, Rosati C, Pandolfini T, Molesini B, Sánchez-Sevilla JF, Amaya I, Mezzetti B, Battino M (2018) Overexpression of the Anthocyanidin synthase gene in strawberry enhances antioxidant capacity and cytotoxic effects on human hepatic cancer cells. J Agric Food Chem 66(3):581–592
González-Villagra J, Cohen JD, Reyes-Díaz MM (2018) Abscisic acid is involved in phenolic compounds biosynthesis, mainly anthocyanins, in leaves of Aristotelia chilensis plants (Mol.) subjected to drought stress. Physiol Plant 165(4):855–866
Grzeszczuk M, Salachna P, Meller E (2018) Changes in photosynthetic pigments, total phenolic content, and antioxidant activity of Salvia coccinea Buc’hoz ex Etl. induced by exogenous salicylic acid and soil salinity. Molecules 23(6):1296–1307
Guina T, Deiana M, Calfapietra S, Cabboi B, Maina M, Tuberoso CI, Leonarduzzi G, Gamba P, Gargiulo S, Testa GJF, Poli G, Biasi F (2015) The role of p38 MAPK in the induction of intestinal inflammation by dietary oxysterols: modulation by wine phenolics. Food Funct 6(4):1218–1228
Hajihashemi S, Noedoost F, Geuns JM, Djalovic I, Siddique KH (2018) Effect of cold stress on photosynthetic traits, carbohydrates, morphology, and anatomy in nine cultivars of Stevia rebaudiana. Front Plant Sci 9:1–12
Hejazi MM, Shariatmadari H, Khoshgoftarmanesh A, Dehghani F (2012) Copper effects on growth, lipid peroxidation, and total phenolic content of rosemary leaves under salinity stress. J Agric Sci Technol 14:205–212
Heredia JB, Cisneros-Zevallos L (2009) The effects of exogenous ethylene and methyl jasmonate on the accumulation of phenolic antioxidants in selected whole and wounded fresh produce. Food Chem 115(4):1500–1508
Ho TT, Lee JD, Ahn MS, Kim SW, Park SY (2018a) Enhanced production of phenolic compounds in hairy root cultures of Polygonum multiflorum and its metabolite discrimination using HPLC and FT-IR methods. Appl Microbiol Biotechnol 102(22):9563–9575
Ho TT, Lee JD, Jeong CS, Paek KY, Park SY (2018b) Improvement of biosynthesis and accumulation of bioactive compounds by elicitation in adventitious root cultures of Polygonum multiflorum. Appl Microbiol Biotechnol 102(1):199–209
Hruby A, Hu FB (2015) The epidemiology of obesity: a big picture. PharmacoEconomics 33(7):673–689
Hugo W (1978) Phenols: a review of their history and development as antimicrobial agents. Microbios 23(92):83–85
Ichim MC (2019) The Romanian experience and perspective on the commercial cultivation of genetically modified crops in Europe. Transgenic Res 28(1):1–7
Jacobo-Velázquez DA, Cisneros-Zevallos L (2012) An alternative use of horticultural crops: stressed plants as biofactories of bioactive phenolic compounds. Agriculture 2(3):259–271
Jacobo-Velázquez DA, Martínez-Hernández GB, del C. Rodríguez S, Cao CM, Cisneros-Zevallos L (2011) Plants as biofactories: physiological role of reactive oxygen species on the accumulation of phenolic antioxidants in carrot tissue under wounding and hyperoxia stress. J Agric Food Chem 59(12):6583–6593
Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11(1):100–105
Jamalian S, Gholami M, Esna-Ashari M (2013) Abscisic acid-mediated leaf phenolic compounds, plant growth and yield is strawberry under different salt stress regimes. Theor Exp Plant Phys 25(4):291–299
Johkan M, Shoji K, Goto F, Hashida S-N, Yoshihara T (2010) Blue light-emitting diode light irradiation of seedlings improves seedling quality and growth after transplanting in red leaf lettuce. HortScience 45(12):1809–1814
Jorge TF, Rodrigues JA, Caldana C, Schmidt R, van Dongen JT, Thomas-Oates J, António C (2016) Mass spectrometry-based plant metabolomics: metabolite responses to abiotic stress. Mass Spectrom Rev 35(5):620–649
Marchese JA, Ferreira JFS, Rehder VLG, Rodrigues O (2010) Water deficit effect on the accumulation of biomass and artemisinin in annual wormwood(Artemisia annua L., Asteraceae). Braz J Plant Physiol 22(1):1–9
Kang KS, Yamabe N, Wen Y, Fukui M, Zhu BT (2013) Beneficial effects of natural phenolics on levodopa methylation and oxidative neurodegeneration. Brain Res 1497:1–14
Kang SN, Lee J, Park JH, Cho JH, Park JH, Cho KK, Lee OH, Kim IS (2014) In vitro anti-osteoporosis properties of diverse Korean Drynariae rhizoma phenolic extracts. Nutrients 6(4):1737–1751
Karakas FP, Yidirim AB, Bayram R, Yavuz MZ, Gepdiremen A, Turker AU (2015) Antiproliferative activity of some medicinal plants on human breast and hepatocellular carcinoma cell lines and their phenolic contents. Trop J Pharm Res 14(10):1787–1795
Karr S (2017) Epidemiology and management of hyperlipidemia. Am J Manag Care 23(9):139–148
Khan T, Khan T, Hano C, Abbasi BH (2019) Effects of chitosan and salicylic acid on the production of pharmacologically attractive secondary metabolites in callus cultures of Fagonia indica. Ind Cop Prod 129:525–535
Kiani BH, Ullah N, Haq I, Mirza B (2015) Transgenic Artemisia dubia WALL showed altered phytochemistry and pharmacology. Arab J Chem 2:1–11
Kim EY, Park SA, Park BJ, Lee Y, Oh MM (2014) Growth and antioxidant phenolic compounds in cherry tomato seedlings grown under monochromatic light-emitting diodes. Hortic Environ Biotechnol 55(6):506–513
Kısa D, Elmastaş M, Öztürk L, Kayır Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59(6):813–820
Kováčik J, Klejdus B, Bačkor M, Repčák M (2007) Phenylalanine ammonia-lyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes. Plant Sci 172(2):393–399
Kováčik J, Klejdus B, Hedbavny J, Štork F, Bačkor M (2009) Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant Soil 320(1–2):231
Król A, Amarowicz R, Weidner S (2014) Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiol Plant 36(6):1491–1499
Król A, Amarowicz R, Weidner S (2015) The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves. J Plant Physiol 189:97–104
Kutchan TM, Gershenzon J, Møller BL, Gang DR (2015) Natural products. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry & molecular biology of plants. American Society of Plants, Rockville, pp 1250–1318
Lee MJ, Son JE, Oh M-M (2013) Growth and phenolic content of sowthistle grown in a closed-type plant production system with a UV-A or UV-B lamp. Hortic Environ Biotechnol 54(6):492–500
Li P, Linhardt RJ, Cao Z (2016) Structural characterization of Oligochitosan elicitor from Fusarium sambucinum and its elicitation of defensive responses in Zanthoxylum bungeanum. Int J Mol Sci 17(12):2076
Li X, Li M, Han C, Jin P, Zheng Y (2017) Increased temperature elicits higher phenolic accumulation in fresh-cut pitaya fruit. Postharvest Biol Technol 129:90–96
Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem 135(3):1065–1070
Lin KH, Chao PY, Yang CM, Cheng WC, Lo HF, Chang TR (2006) The effects of flooding and drought stresses on the antioxidant constituents in sweet potato leaves. Bot Stud 47(4):417–426
Liu H, Chen Y, Hu T, Zhang S, Zhang Y, Zhao T, Yu H, Kang Y (2016) The influence of light-emitting diodes on the phenolic compounds and antioxidant activities in pea sprouts. J Funct Foods 25:459–465
Liu Q, Liu Y, Xu Y, Yao L, Liu Z, Cheng H, Ma M, Wu J, Wang W, Ning W (2018) Overexpression of and RNA interference with hydroxycinnamoyl-CoA quinate hydroxycinnamoyl transferase affect the chlorogenic acid metabolic pathway and enhance salt tolerance in Taraxacum antungense Kitag. Phytochem Lett 28:116–123
Løvdal T, Lillo C (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 387(2):238–242
Lucas L, Russell A, Keast R (2011) Molecular mechanisms of inflammation. Anti-inflammatory benefits of virgin olive oil and the phenolic compound oleocanthal. Curr Pharm Des 17(8):754–768
Lv J, Huang H, Yu L, Whent M, Niu Y, Shi H, Wang TT, Luthria D, Charles D, Yu LLJFC (2012) Phenolic composition and nutraceutical properties of organic and conventional cinnamon and peppermint. Food Chem 132(3):1442–1450
Malčovská SM, Dučaiová Z, Maslaňáková I, Bačkor M (2014) Effect of silicon on growth, photosynthesis, oxidative status and phenolic compounds of maize (Zea mays L.) grown in cadmium excess. Water Air Soil Pollut 225(8):2056
Márquez-García B, Fernández-Recamales M, Córdoba F (2012) Effects of cadmium on phenolic composition and antioxidant activities of Erica andevalensis. J Bot 2012:1–6
Marrelli M, Tudisco R, Mastellone V, Conforti F (2013) A comparative study of phytochemical composition of genetically and non-genetically modified soybean (Glycine max L.) and evaluation of antitumor activity. Nat Prod Res 27(6):574–578
Mele L, Bidault G, Mena P, Crozier A, Brighenti F, Vidal-Puig A, Del Rio D (2017) Dietary (poly) phenols, brown adipose tissue activation, and energy expenditure: a narrative review. Adv Nutr 8(5):694–704
Estados Unidos Mexicanos (2005) Ley de bioseguridad de organismos genéticamente modificados. Diario Oficial de la Federción
Minh L, Khang D, Ha PTT, Tuyen PT, Minh TN, Quan NV, Xuan TD (2016) Effects of salinity stress on growth and phenolics of rice (Oryza sativa L.). Int Lett Nat Sci 57:1–10
Moreira-Rodríguez M, Nair V, Benavides J, Cisneros-Zevallos L, Jacobo-Velázquez D (2017) UVA, UVB light doses and harvesting time differentially tailor glucosinolate and phenolic profiles in broccoli sprouts. Molecules 22(7):1065
Morkunas I, Woźniak A, Mai V, Rucińska-Sobkowiak R, Jeandet P (2018) The role of heavy metals in plant response to biotic stress. Molecules 23(9):2320
Neagu M, Constantin C, Caruntu C, Dumitru C, Surcel M, Zurac S (2018) Inflammation: a key process in skin tumorigenesis. Oncol Lett 17:4068–4084
Olas B (2017) The multifunctionality of berries toward blood platelets and the role of berry phenolics in cardiovascular disorders. Platelets 28(6):540–549
Oliveira LL, Carvalho MV, Melo L (2014) Health promoting and sensory properties of phenolic compounds in food. Revista Ceres 61:764–779
Ortega-García F, Blanco S, Peinado MÁ, Peragón J (2008) Polyphenol oxidase and its relationship with oleuropein concentration in fruits and leaves of olive (Olea europaea) cv.‘Picual’ trees during fruit ripening. Tree Physiol 28(1):45–54
Ozcan T, Akpinar-Bayizit A, Yilmaz-Ersan L, Delikanli B (2014) Phenolics in human health. Int J Chem Eng Appl 5(5):393–396
Panche A, Diwan A, Chandra S (2016) Flavonoids: an overview. J Nutr Sci 5:1–15
Pandey A, Misra P, Trivedi PK (2015) Constitutive expression of Arabidopsis MYB transcription factor, AtMYB11, in tobacco modulates flavonoid biosynthesis in favor of flavonol accumulation. Plant Cell Rep 34(9):1515–1528
Pansuksan K, Mii M, Supaibulwatana K (2014) Phytochemical alteration and new occurring compounds in hairy root cultures of Mitracarpus hirtus L. induced by phenylurea cytokinin (CPPU). Plant Cell Tissue Organ Cult 119(3):523–532
Papoutsis K, Vuong Q, Pristijono P, Golding J, Bowyer M, Scarlett C, Stathopoulos C (2016) Enhancing the total phenolic content and antioxidants of lemon pomace aqueous extracts by applying UV-C irradiation to the dried powder. Foods 5(3):55
Pareek A, Khurana A, Sharma AK, Kumar R (2017) An overview of signaling regulons during cold stress tolerance in plants. Curr Genomics 18(6):498–511
Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgórska M, Deckert J (2011) Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. effects of cadmium and lead on phenylalanine ammonia-lyase gene expression, enzyme activity and lignin content. Acta Biochim Pol 58(2):211–216
Petridis A, Therios I, Samouris G (2012a) Genotypic variation of total phenol and Oleuropein concentration and antioxidant activity of 11 Greek olive cultivars (Olea europaea L.). HortScience 47(3):339–342
Petridis A, Therios I, Samouris G, Koundouras S, Giannakoula A (2012b) Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olive (Olea europaea L.) cultivars. Plant Physiol Biochem 60:1–11
Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M (2016) Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev 74(10):624–634
Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ, Valko M (2017) Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci 38(7):592–607
Posmyk M, Kontek R, Janas K (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72(2):596–602
Puente-Garza CA, Meza-Miranda C, Ochoa-Martínez D, García-Lara S (2017) Effect of in vitro drought stress on phenolic acids, flavonols, saponins, and antioxidant activity in Agave salmiana. Plant Physiol Biochem 115:400–407
Qian H, Liu T, Deng M, Miao H, Cai C, Shen W, Wang Q (2016) Effects of light quality on main health-promoting compounds and antioxidant capacity of Chinese kale sprouts. Food Chem 196:1232–1238
Quideau S, Deffieux D, Douat-Casassus C, Pouységu L (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem 50(3):586–621
Rakei A, Maali-Amiri R, Zeinali H, Ranjbar M (2016) DNA methylation and physio-biochemical analysis of chickpea in response to cold stress. Protoplasma 253(1):61–76
Rodríguez-Calzada T, Qian M, Strid Å, Neugart S, Schreiner M, Torres-Pacheco I, Guevara-González RG (2019) Effect of UV-B radiation on morphology, phenolic compound production, gene expression, and subsequent drought stress responses in chili pepper (Capsicum annuum L.). Plant Physiol Biochem 134:94–102
Rodriguez-Morato J, Xicota L, Fito M, Farre M, Dierssen M, de la Torre R (2015) Potential role of olive oil phenolic compounds in the prevention of neurodegenerative diseases. Molecules 20(3):4655–4680
Rostoks N, Grantiņa-Ieviņa L, Ieviņa B, Evelone V, Valciņa O, Aleksejeva I (2019) Genetically modified seeds and plant propagating material in Europe: potential routes of entrance and current status. Heliyon 5(2):1–21
Saito K (2013) Phytochemical genomics – a new trend. Curr Opin Plant Biol 16(3):373–380
Santana-Gálvez J, Jacobo-Velázquez DA (2018) Classification of phenolic compounds. In: Nollet LM, Gutierrez-Uribe JA (eds) Phenolic compounds in food: characterization and analysis, vol 1, 1st edn. CRC Press, Boca Raton, pp 3–20
Sarega N, Imam MU, Ooi D-J, Chan KW, Md Esa N, Zawawi N, Ismail M (2016) Phenolic rich extract from Clinacanthus nutans attenuates hyperlipidemia-associated oxidative stress in rats. Oxid Med Cell Longev 2016:1–17
Sarker U, Oba S (2018) Response of nutrients, minerals, antioxidant leaf pigments, vitamins, polyphenol, flavonoid and antioxidant activity in selected vegetable amaranth under four soil water content. Food Chem 252:72–83
Seo JM, Arasu MV, Kim YB, Park SU, Kim SJ (2015) Phenylalanine and LED lights enhance phenolic compound production in Tartary buckwheat sprouts. Food Chem 177:204–213
Simic SG, Tusevski O, Maury S, Hano C, Delaunay A, Chabbert B, Lamblin F, Lainé E, Joseph C, Hagège D (2015) Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures. Plant Cell Tissue Organ Cult 122(1):213–226
Singh S (2016) Enhancing phytochemical levels, enzymatic and antioxidant activity of spinach leaves by chitosan treatment and an insight into the metabolic pathway using DART-MS technique. Food Chem 199:176–184
Soengas P, Rodríguez VM, Velasco P, Cartea ME (2018) Effect of temperature stress on antioxidant defenses in Brassica oleracea. ACS Omega 3(5):5237–5243
Son K-H, Oh M-M (2013) Leaf shape, growth, and antioxidant phenolic compounds of two lettuce cultivars grown under various combinations of blue and red light-emitting diodes. HortScience 48(8):988–995
Surjadinata BB, Cisneros-Zevallos L (2012) Biosynthesis of phenolic antioxidants in carrot tissue increases with wounding intensity. Food Chem 134(2):615–624
Surjadinata B, Jacobo-Velázquez D, Cisneros-Zevallos L (2017) UVA, UVB and UVC light enhances the biosynthesis of phenolic antioxidants in fresh-cut carrot through a synergistic effect with wounding. Molecules 22(4):668
Takshak S, Agrawal S (2019) Defense potential of secondary metabolites in medicinal plants under UV-B stress. J Photochem Photobiol B 193:51–88
Torres-Contreras AM, Nair V, Cisneros-Zevallos L, Jacobo-Velázquez DA (2014) Plants as biofactories: stress-induced production of chlorogenic acid isomers in potato tubers as affected by wounding intensity and storage time. Ind Crop Prod 62:61–66
Tsao R (2010) Chemistry and biochemistry of dietary polyphenols. Nutrients 2(12):1231–1246
Tuzcu Z, Orhan C, Sahin N, Juturu V, Sahin K (2017) Cinnamon polyphenol extract inhibits hyperlipidemia and inflammation by modulation of transcription factors in high-fat diet-fed rats. Oxid Med Cell Longev 2017
Tyunin AP, Kiselev KV (2016) Alternations in VaSTS gene cytosine methylation and t-resveratrol production in response to UV-C irradiation in Vitis amurensis Rupr. Cells. Plant Cell Tissue Organ 124(1):33–45
Valls-Pedret C, Sala-Vila A, Serra-Mir M, Corella D, De la Torre R, Martínez-González MÁ, Martínez-Lapiscina EH, Fitó M, Pérez-Heras A, Salas-Salvadó J (2015) Mediterranean diet and age-related cognitive decline: a randomized clinical trial. JAMA Intern Med 175(7):1094–1103
Vosoughi N, Gomarian M, Ghasemi Pirbalouti A, Khaghani S, Malekpoor F (2018) Essential oil composition and total phenolic, flavonoid contents, and antioxidant activity of sage (Salvia officinalis L.) extract under chitosan application and irrigation frequencies. Ind Crop Prod 117:366–374
Weichselbaum E, Buttriss J (2010) Polyphenols in the diet. Nutr Bull 35(2):157–164
Wong RS (2011) Apoptosis in cancer: from pathogenesis to treatment. J Exp Clin Cancer Res 30(1):87
Xuan TD, Khanh TD, Khang DT, Quan NT, Elzaawely AA (2016) Changes in chemical composition, total phenolics and antioxidant activity of Alpinia (Alpinia zerumbet) leaves exposed to UV. Int Lett Nat Sci 55:25–34
Younis MB, Hasaneen MNA-G, Abdel-Aziz HMM (2010) An enhancing effect of visible light and UV radiation on phenolic compounds and various antioxidants in broad bean seedlings. Plant Signal Behav 5(10):1197–1203
Zhao CY, Si JH, Feng Q, Deo RC, Yu TF, Du Li P (2017) Physiological response to salinity stress and tolerance mechanics of Populus euphratica. Environ Monit Assess 189(11):533
Zheleznichenko T, Banaev E, Asbaganov S, Voronkova M, Kukushkina T, Filippova E, Mazurkova N, Shishkina L, Novikova T (2018) Nitraria schoberi L. hairy root culture as a source of compounds with antiviral activity against influenza virus subtypes А(H5N1) and А(H3N2). 3Biotech 8(6):260
Zheng S, Deng S, Huang Y, Huang M, Zhao P, Ma X, Wen Y, Wang Q, Yang XJF (2018) Anti-diabetic activity of a polyphenol-rich extract from Phellinus igniarius in KK-Ay mice with spontaneous type 2 diabetes mellitus. Food Funct 9(1):614–623
Zhou Y, Zheng J, Li Y, Xu D-P, Li S, Chen Y-M, Li H-B (2016) Natural polyphenols for prevention and treatment of cancer. Nutrients 8(8):515
Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324
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Aviles-Gaxiola, S., Olivo-Vázquez, G., Cabanillas-Bojórquez, L.A., Gutiérrez-Grijalva, E.P., Heredia, J.B. (2020). Plants as Biofactories for Phenolic Compounds. In: Lone, R., Shuab, R., Kamili, A. (eds) Plant Phenolics in Sustainable Agriculture . Springer, Singapore. https://doi.org/10.1007/978-981-15-4890-1_20
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