Effect of environmental factors in the production and biochemical compounds in
Abstract
Agronomic practices and climatic factors affect the content and profile of phytochemicals. The effects of the environment, such as salinity, climate, and other abiotic factors, promote biochemical responses, inducing changes in the quantity and quality of polyphenol compounds, carotenoids, vitamins, glucosinolates, and polyamines, which are bioactive compounds. In plants, among the various functions, some phytochemicals can protect against biotic factors. Brassica vegetables are a source of several primary and secondary metabolism compounds, and they might be responsible for disease prevention. In addition, the increase of bioactive compounds in plant-based foods is important to the diet and consequently for the improvement of public health. In this chapter, we will point out the abiotic factors that affect the productive performance, quality, and chemical composition of different Brassica species and cultivars. We will also discuss its implications on plant protection and human health.
Keywords
- environmental factors
- cultivation conditions
- polyphenol
- carotenoids
- glucosinolates
1. Introduction
The
The species of the
Variations in the agronomic conditions (e.g., vegetal species, cultivars, development stage, plants organs, fertilization, and soil pH) and climatic factors (e.g., light intensity and water availability) are known for significantly affecting the phytochemical content and profile. The understanding of the effects of climatic and agronomic factors is necessary for increasing the predictability of the desired compounds, increasing the benefits related to the human health and to the plants’ protection (plague control) [6]. Although there is little information on the real influence of cultivation on the contents of glucosinolates and other important phytochemicals in
2. Agronomic factors and production
The photosynthetic activity is the base for the production of reserves in the plant, which will constitute the biomass, a factor that can determine the vegetal development limits. The production depends on the interaction between the productive potential and the environmental factors. The edaphoclimatic factors are directly related to productive responses that influence the flowering, hydric balance, respiration, and absorption of minerals. Latitude, altitude, rainfall, topography, and soil physics act indirectly on the production and other factors, such as solar radiation, temperature, water, and chemical elements of the soil act directly on the photosynthesis. The environmental factors, such as water, temperature, quality, and quantity of light hours, will determine the plants’ growth rate.
The temperature is a climatic factor that can limit the production of determined species in tropical and equatorial regions. Besides determining the growth and development, it establishes the end of the vegetative stage and the beginning of the productive stage in the biennial species, such as broccoli, cauliflower, Brussels sprout, among other species. The broccoli has a better productive development under average temperatures between 60 and 65°F, with a maximum of 75°F [7]. Prolonged periods of temperature above 77°C can retard the formation of inflorescence in plants that are in phase of vegetative growth, reducing the size and causing the development of leaves and bracts in the floral peduncles [8].
The temperature strongly influences the plants’ metabolic activity, and the stress caused by high and low temperatures can induce effects in the primary and secondary metabolism (Table 1). The heat or cold can affect the membrane fluidity, metabolism, and cytoskeleton rearrangement, consequently affecting the vegetative and reproductive tissues [9]. Abrupt increases of temperature can provoke excessively fast growth of the inflorescence and elongating the peduncle in certain cultivars [10]. Cultivations in conditions of high temperatures, where there are only few days with ideal temperatures for vernalization, the plants can continue to vegetate or to not produce commercial inflorescences, which means uneven bunches, the presence of bracts, and low compactness of the head and yellow coloration. Temperatures below the ideal level can prolong the cycle of provoke premature flowering in some species, as in the case of summer cauliflowers submitted to low temperatures [11]. Among the
Stress factor | Productive and/or biochemical response | Citations | |
---|---|---|---|
Temperature | Heat | Affects the glucosinolates content Higher glucosinolates production |
[59] [13] |
Cold | Higher glucosinolates production Higher glucosinolates production in broccoli under low temperatures |
[13] [60] |
|
Thermal amplitude | Higher glucosinolates production in broccoli plants under temperatures between 53.6 and 89.6°F, compared to plants under temperature 71.6F | [61] | |
Luminosity | Competition (population density and consortium) | Reduced levels of trypsin inhibitors in Reduced levels of glucosinolates in the leaves and roots in |
[6] |
Excess | Photoinhibition, thermal stress, and stomatal closing, leading to a reduction of net photosynthesis in |
[62] | |
Protected cultivation (light diffusion and shading) | Mustard plants |
[63] | |
Photoperiod | Affects the glucosinolates content Spring broccoli growth in intermediate temperatures, high luminous intensity, longer days, and dry conditions have the highest total GLS content Glucosinolates levels in kale are not influenced by the photoperiod |
[59] [6] [61] |
|
Water | Hydric restriction | Growth reduction, lower yield of cabbage heads, and an increase of dry mass Kale: growth reduction, biomass reduction, increase of sorbitol, sucrose, verbascose and kestose levels, and a decrease of manitol An increase in the sugar content in the phloem sap of broccoli submitted at hydric stress Lower glucosinolate content in broccoli in hydric restriction Biomass reduction, an increase of nitrogen in the leaf, and a darker green leaf in Chinese cabbage |
[64] [65] [66] [67] |
Salinity | Growth reduction, Na or Cl accumulation, and lower productivity A decrease of fresh matter in the aerial part of broccoli An increase in GLS content and phenolic compounds A drastic decrease in the vitamin C content in old broccoli leaves A significant decrease in the vitamin C content in young broccoli leaves; Loss of flavonoids in old broccoli leaves; Loss of turgor Accumulation of glucosinolates in Reduction in the nitrate content Increase or no effect in the nitrate content |
[68] [69] [70] [71] [72] |
|
Fertilization | Nitrogen (N) Sulfur (S) |
Nitrogen fertilization influences the GLS metabolism in broccoli High level of sulfur provided an increase of polyphenol contents (flavonoids and phenolic acids) in An increase of the total glucosinolates with the increase of fertilization with sulfur Higher quantities of sulfur and nitrogen combined did not provide higher contents of glucosinolates |
[73] [74] [75] [60] |
The plants can be modified to some degree, tolerating light stresses from either low or high temperatures when slowly submitted to the stress, leading to acclimatization. By contrast, plants that survive the exposition to conditions above the ideal temperature can produce chaperones, molecules that are related to the antioxidant activity, and solutes accumulation [9]. Low temperatures cause reduction in the enzymatic activity, rigidity of membranes, destabilization of protein complexes, compromise of photosynthesis, and rupture of the membranes. Cellular alterations associated to the tolerance to cold and/or freezing include the accumulation of sugar or compatible solutes, changes in the membrane composition, and synthesis of dehydrin-like proteins [9].
The stress by temperature can cause changes in the plants’ chemical constitution. Broccoli sprouts present increased glucosinolate contents when cultivated under high (84.2 or 89.6°F) or low temperatures (51.8 or 60.8°F), comparing the cultivated sprouts under ideal temperature (70.7°F) [13]. Similar to the sprouts, the broccoli leaves showed the highest glucosinolate level when cultivated under 53.6 or 89.6°F. This effect was also observed in younger cabbage plants. Under low temperatures, there is an increase of the glucosinolate levels in broccoli and watercress (Table 1). The combination of temperature and precipitation influences the glucosinolate content in
The light is a factor that influences the
3. Brassicas’ phytochemical composition
Many epidemiologic studies do not differ among the types of cruciferous vegetables, but the most common studies in the entire world include the broccoli, cauliflower, cabbages, bok choy, kale, watercress, turnip, and rocket [21]. Besides human health aspects, these metabolites play a fundamental role in the plants’ defense against microorganisms; thus, there is an increasing interest in raising the content of these secondary compounds as a strategy of increasing the protection to cultures and reducing the use of agrochemicals.
Even though there is little information on the real influence of the cultivation in the levels of glucosinolates and other important phytochemicals in
3.1. Glucosinolates
The glucosinolates profile and its modifications, together with specific products of hydrolyzation, are being discussed as a plant defense mechanism to deal with various abiotic and biotic stresses. Recent studies showed that glucosinolates, for example, breakdown products of 1-methoxy-indol-3-ylmethyl glucosinolate and 5-phenylpentyl isothiocyanate, exert mutagenic or genotoxic effects in mammalian and bacterial cell studies [22]. Studies indicate that broccoli sprouts are sources of GLS (varying from 679.01 to 554.90 mg/100 g FW), and the predominant GLS is the glucosinolate glucoraphanin (GRA) (33% of the total GLS) [23].
Glucosinolates and isothiocyanates (products of glucosinolate hydrolysis) are produced by some plants in response to biotic stress. They are important as protective agents of the plants, due to their toxic or repelling effects against potential plagues (herbivores, bacteria, and fungi) [24]. Even though these compounds can be used as protection agents in plants, with a great importance in agriculture and horticulture, they are significantly important to human nutrition, due to the preventive effects on human health [24, 25]. These compounds are known for protecting against cancer in humans [26] and, in plants, these secondary metabolites and/or their breakdown products have different biological functions, like fungicidal, bactericidal, nematocidal, and allelopathic properties [27].
Thus, factors influencing phytochemical content and profile in the production of
The quality and quantity of GLS differ among the plants species, among the different plant organs (tubercle or leaves), and in function of the ontogeny. The profile of these compounds is not only determined by the plant genetic constitution but also influenced by the environmental conditions [31]. Generally, high levels of GLS occur in response to temperature [32], exposition to different wavelengths [33], nutrients availability [34], and signaling molecules as the salicylic acid (SA) [25], jasmonic acid (JA), and methyl jasmonate (MeJA) [31, 35]. Exogenous applications of SA and its analogous acids, damage by herbivory or treatment with JA, induce increases of indole GLS in
Saline stress (150 mM NaCl) can reduce the total GLS levels, due to the decrease of both aliphatic GLP, as indole (GBS and MBGS), in broccoli sprouts [23]. This decrease is attributed to cell damages induced by Na accumulation [39]. However, studies with broccoli sprouts determined that the decrease in the GLS level in response to excessive contents of NaCl (44% in comparison to the control—0 mM NaCl) can be decreased by the application of MeJA, applied daily from the third day of growth of 10-day-old broccoli sprouts [23].
The thermal treatment causes denaturation of enzymes that catalyze the degradation of nutrients and some metabolites. When
3.2. Polyphenols
The phenolic compounds are a group of secondary metabolites present in the vegetal kingdom. The most disseminated and diversified groups of polyphenols are the flavonoids, which have C6-C3-C6 flavone skeleton. The flavonoids are important phenolic phytochemicals containing a basic structure of two aromatic benzene rings separated by a heterocyclic-oxygenated ring [43]. The flavonoids and the hydroxycinnamic acids are widely distributed in plants and are important bioactive compounds in the human diet. The dietetic flavonoids have antiviral, anti-inflammatory, antihistaminic, and antioxidant properties. Flavonoids and phenolic acids are the most characterized groups of phenolic compounds in
Generally, the phenolic compounds are produced through the phenylpropanoid pathway. Biotic or abiotic stresses, such as elicitors, were reported for inducing alterations in the phenolic compounds contents, as described in broccoli sprouts [23, 46]. In addition, the quality and quantity of the phenols differ among the plant species and among the plant organs. For example, broccoli sprouts have higher phenolic levels (1133.85 mg/100 g FW), when compared with mature broccoli inflorescences (63.4 mg/100 g FW) [45]. Most of the phenolic compounds present in broccoli sprouts are the hydroxycinnamic acids (sinapic acid derivatives), approximately 98% of the total phenolics found [23].
In saline-stress conditions, there is a possibility for a decrease to occur up to 30% in the phenolic compounds’ content in
The culinary process is a source of several alterations, both physical and biochemical, modifying the phytochemical constituents present in the vegetables, resulting in changes in the nutritional values [48] of
3.3. Carotenoids
Carotenoids are a class of phytonutrients that are responsible for the colors red, orange, and light yellow in many vegetables and fruits. Most of the
In order for the carotenoid absorption to occur by gut enterocytes, the mechanical and/or enzymatic disruption of the food matrix is necessary. In addition, due to the hydrophobic character of these chemical molecules, the formation of micelles before its absorption is also necessary [54]. Since the carotenoids in fruits and vegetables are present in the chromoplasts, their substructure and the cell wall are the main barriers to the bioavailability of these compounds [55]. Thus, thermal processing as the boiling or the steaming can have positive effects in bioavailability, collaborating to the food matrix disruption, even though negative effects caused by the carotenoids degradation were also reported [56].
The processing methods used in
4. Conclusion
Many studies show that stress can lead to the accumulation of bioactive compounds in plants, generating the production of foods with more benefits to the human health. In contrast, the growth and development are affected, because there is a reallocation of primary metabolites for the formation of secondary metabolites. This reflects in the biomass production and, certainly, in the species production. However, these metabolites, such as GLS, phenolic compounds, and carotenoids, play a fundamental role in the plants’ defense against microorganisms, possibly leading to a better adaptation of the plants to the environment and, consequently, to the reduction in the use of agrochemicals. The current knowledge of the climatic factors that affect the content and profile of these phytochemicals in
Acknowledgments
The authors gratefully acknowledge the support by São Paulo Research Foundation (FAPESP—Brazil), process 2016/22665-2 and 2016/00972-0, São Paulo State University, and Conselho Nacional de Pesquisa (CNPq e Brazil), process 305177/2015-0.
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