Next Article in Journal
Summer Drought Delays Leaf Senescence and Shifts Radial Growth Towards the Autumn in Corylus Taxa
Previous Article in Journal
Comparison of Canopy–Vegetation Parameters from Interior Parts to Edge of Multi-Story Grove Forest Patch and Meadow Field Within Rural Landscape for Soil Temperature and Moisture
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 16
Issue 6
10.3390/f16060906
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Seasonal and Edaphic Modulation Influences the Phenolic Contents and Antioxidant Activity in Cork Oak (Quercus suber L.): Evidence from the Algerian Mediterranean Forest

by
Melia Hoceini-Bentaha
1,
Saliha Kadi-Bennane
2,
Mohand Ouidir Boussoum
3,
El-Hafid Nabti
4,
Nassima Kadir
5,
Nadjet Mestar-Guechaoui
6,
Nasir A. Ibrahim
7,*,
Mohammed Saad Aleissa
7,
Nosiba S. Basher
7,
Malika Boudiaf
2,
Lamia Trabelsi
8 and
Karim Houali
6
1
Laboratory of Agro-Biotechnology and Nutrition in Semi-Arid Areas, Department of Nature and Life Sciences, Faculty of Natural and Life Sciences, Ibn Khaldoun University, Tiaret 14000, Algeria
2
Department of Agronomic Sciences, Faculty of Biological Sciences and Agronomical Sciences, Mouloud Mammeri University, Tizi-Ouzou 15000, Algeria
3
Laboratory of Biodiversity, Health, and Valorization of Biological Resources, Department of Natural and Life Sciences, Faculty of Natural and Life Sciences, Ibn Khaldoun University, Tiaret 14000, Algeria
4
Laboratoire de Maitrise Des Energies Renouvelables, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, Bejaia 06000, Algeria
5
Department of Biology, Faculty of Natural and Life Sciences, Saad Dahlab University—Blida 1, Ouled Yaich 9000, Algeria
6
Laboratory of Applied Biochemistry and Biotechnology (LABAB), Faculty of Biological Sciences and Agronomical Sciences, Mouloud Mammeri University, Tizi-Ouzou 15000, Algeria
7
Biology Department, College of Science, Imam Mohammad Ibn Saud Islamic University (IMSIU), Riyadh 11623, Saudi Arabia
8
Marine Biodiversity Laboratory, National Institute of Marine Sciences and Technology (INSTM), University of Carthage, Tunis 1054, Tunisia
*
Author to whom correspondence should be addressed.
Forests 2025, 16(6), 906; https://doi.org/10.3390/f16060906
Submission received: 24 April 2025 / Revised: 21 May 2025 / Accepted: 27 May 2025 / Published: 28 May 2025
(This article belongs to the Section Forest Ecophysiology and Biology)
Browse Figures
Versions Notes

Abstract

:
The cork oak (Quercus suber L.), an emblematic species of Mediterranean biodiversity, is the focus of this study, which aimed to characterize the relationships between abiotic factors and variations in its secondary metabolites. Rhizospheric soil samples (collected at two depths: 0–15 cm and 15–25 cm), roots, and leaves were gathered in Azouza forest (Kabylia, Algeria) during the winter and summer seasons of 2019. Analyses were conducted on total polyphenol (TPP), flavonoid (FLAV), and tannin (TT) contents, and their antioxidant activities were assessed using DPPH, FRAP, and TAC assays. The results reveal seasonal and soil-depth variability, with the highest concentrations observed in leaves (170.2 mg GAE/g DW for TPP, 14.15 mg TAE/g DW for TT, and 6.4 mg QE/g DW for FLAV). Antioxidant activity was also more pronounced in leaves, with IC50 values of 130.90 µg/mL (DPPH) and 61.22 µg/mL (FRAP). Roots from the deeper layer (15–25 cm) exhibited higher phenolic compound levels and greater antioxidant activity compared to those from the superficial layer (0–15 cm). Principal component analysis showed that 93% of the variance was explained by seasonal factors and sampling depth, confirming their key role in secondary metabolite synthesis and biological activity. The cork oak’s biochemical adaptability to environmental changes reveals climate adaptation strategies, highlighting soil–plant influences on its metabolic responses in Mediterranean ecosystems.

1. Introduction

The Mediterranean region is recognized as one of the world’s 36 biodiversity hotspots [1]. However, intensifying climate change in recent decades has posed significant threats to the tree species native to this region [2]. These species have developed various adaptive mechanisms, including the production of secondary metabolites, which play a crucial role in their response to environmental stress [3]. The accumulation of phenolic compounds in plant tissues represents an adaptive strategy that enhances ecological resilience [4]. Secondary metabolites are economically important as they serve various functions, including use as medicines, flavors, fragrances, dyes, pigments, pesticides, and food additives. The commercial significance of these compounds is of great interest to both the pharmaceutical and food industries [5].
Studying the plant metabolome provides an excellent biochemical profiling tool for understanding how plants respond to changing environmental conditions [6]. In the context of ecosystem dynamics, long-lived trees produce a diverse array of secondary metabolites through different biosynthetic pathways [7]. These metabolites serve multiple functions, and different plant species may exhibit distinct natural product profiles that reflect phenotypic plasticity in response to environmental pressures [8]. Furthermore, plant growth and development are largely mediated by the endogenous levels of these secondary metabolites, which accumulate in response to various signaling molecules. Environmental factors significantly influence the synthesis and subsequent accumulation of secondary metabolites, and any change in these factors can lead to perturbations in the biosynthesis of plant secondary metabolites [9].
The cork oak (Quercus suber L.), a member of the Fagaceae family, is one of the most important forest species in the Mediterranean Basin. Native to the western Mediterranean region, it is primarily found in southwestern Europe and northwestern Africa [10]. Cork production grants it significant biological, ecological, and socioeconomic value, while also contributing substantially to soil conservation and carbon sequestration [11]. Although Q. suber is a long-lived species that regularly undergoes bark harvesting, cork—its most highly valued forest product—also serves as an important carbon sink, consuming minimal water [12]. This sclerophyllous evergreen tree species is well-adapted to endure numerous stresses that frequently occur concurrently in the Mediterranean region [13]. The plasticity of Q. suber has been identified as a trait that enhances its tolerance to drought, cold, and shade [14].
However, the severe decline in cork oak forests observed in recent decades has led to detrimental consequences at multiple ecosystem scales. Although cork oak woodlands have decreased by nearly half, they still represent about one-third of the total forested area [15]. This decline is attributed to inadequate forest management practices and the growing impacts of climate change. Cork oak faces numerous biotic (diseases, pests) and abiotic (thermal fluctuations, water stress) pressures [16]. Environmental factors significantly affect plant growth and the biosynthesis of secondary metabolites. Numerous studies have highlighted the remarkable richness of phenolic compounds in cork oak, particularly in low-molecular-weight secondary metabolites [17,18,19]. Plant growth and productivity are negatively affected by temperature extremes, salinity, and drought stress [9].
Recent studies have emphasized the urgent need to establish conservation and sustainable management strategies to preserve these ecosystems, particularly in light of climate projections predicting worsening environmental conditions [20,21,22]. Algeria contributes approximately 5% of global cork production, with around 220,000 hectares of cork oak forests [23]. However, an alarming degradation of cork oak stands has been observed in recent years [24].
This study aimed to assess the phenolic composition of cork oak in relation to various abiotic factors, including drought, cold, and soil physicochemical properties. We analyzed seasonal variations in phenolic compounds in leaves, roots, and rhizospheric soil during summer and winter. Additionally, we evaluated the antioxidant potential of plant extracts under hydric and thermal stress conditions. Correlations between biochemical parameters and environmental factors were established using principal component analysis (PCA).

2. Materials and Methods

2.1. Study Site

The study was conducted on samples collected from Ait Hammad station, located in northern Algeria within the Azouza State Forest (Zekri municipality), approximately 75 km from the provincial capital of Tizi-Ouzou. The site is bounded by Tigrin Forest in the North, Beni Zekki in the South, Azazga in the West, and Sidi Aissa in the East (Figure 1).
The geographical coordinates and climatic data are presented in Table 1 and Table 2.

2.2. Sampling

The sampling procedure targeted 10 even-aged high forest trees at the study site. Leaves were sampled from the mid- and inner-canopy positions of the trees, covering all four cardinal directions. Root systems and associated rhizospheric soil (RS) samples were obtained at two distinct depth intervals: 0–15 cm (D1) and 15–25 cm (D2). Soil collection followed a standardized protocol using a 625 cm3 quadrat, with sampling conducted at four cardinal points beneath each tree’s canopy [25].
All plant specimens (leaves and roots) were preserved in paper sampling bags, while soil samples were immediately sealed in polyethylene bags to maintain integrity. Each sample was properly labeled before transport to the laboratory for subsequent analysis.
The plant material was air-dried, ground to powder using an electric mill, and subsequently stored in glass containers. The soil was processed separately: following air-drying, it was sieved through a 2 mm mesh screen.

2.3. Soil Analysis

2.3.1. Physicochemical Characterization of Rhizospheric Soil

Soil samples underwent standardized physicochemical analysis [26]. The particle size distribution was determined using the Robinson pipette method following sodium hexametaphosphate dispersion, in accordance with ISO 11277:2020 [27,28]. Clay and fine silt fractions were isolated using the Aubert settling method [29], a validated technique for soil characterization [30]. The soil pH and electrical conductivity (EC) of saturated extracts were measured using digital pH and conductivity meters (HI-9811, Hanna Instruments, Woonsocket, RI, USA) at soil/water ratios of 1:2.5 and 1:5, respectively. Available phosphorus (P) was quantified via Olsen’s spectrophotometric method [31]. Carbon content was determined using the loss on ignition (LOI) method [32]. The Kjeldahl method quantifies total nitrogen by converting organic and inorganic nitrogen into ammonium sulfate through acid digestion. The resulting ammonium is then released as ammonia via alkaline distillation and captured in a receiving solution. Finally, the amount of ammonia is determined by titration, allowing for the calculation of the total nitrogen content in the sample [33]. Soil moisture was measured using a hygrometric probe (Hanna Instruments), allowing for an in situ assessment of the volumetric water content.

2.3.2. Total Polyphenol Content (TPC) Determination

Total soil polyphenol content was determined using a modified Dallali protocol [34]. Briefly, 2 g of dried soil was mixed with 20 mL methanol/water (70:30 v/v), shaken for 30 min at 25 °C, then centrifuged (5000× g, 10 min, 3×) The evaporated extract was stored at 4 °C.
TPC was measured following the protocol of Blum et al. (1991) [35]; 0.5 mL soil extract was mixed with 4.5 mL distilled water, 0.75 mL 1.9 M Na2CO3, and 0.25 mL Folin–Ciocalteu reagent (Sigma, Darmstadt, Germany). After 1 h of dark incubation at room temperature, absorbance was measured at 750 nm [36]. Gallic acid served as calibration standard [37].

2.4. Plant Material Analysis

2.4.1. Plant Extract Preparation

Powdered plant material (roots/leaves, 2.5 g) was extracted with 25 mL 70% methanol, shaken (30 min), then macerated (24 h). After triple centrifugation (5000× g, 10 min), the supernatant was evaporated and stored at 4 °C [38,39].

2.4.2. Quantitative Analyses

Total Polyphenol Content

TPC was determined using Folin–Ciocalteu assay with a gallic acid standard. A 200 μL extract was mixed with 1 mL diluted Folin–Ciocalteu reagent, followed by 800 μL 75% Na2CO3 after 4 min. After 2 h of dark incubation, absorbance was measured at 765 nm [40,41]. The results are expressed as mg gallic acid equivalents per g dry weight (mg GAE/g DW).

Total Tannin Content

Tannins were quantified via protein precipitation [42]. A 500 μL extract was incubated (4 °C, 24 h) with 1 mL bovine serum albumin (BSA) and then centrifuged (950× g, 15 min). The precipitate was dissolved in 2 mL SDS-TEA solution with 500 μL FeCl3, incubated (15 min dark), and read at 510 nm [43]. Tannic acid standard curve (400–2000 μg/mL) was used, with results expressed as mg tannic acid equivalents/g DW (mg TAE/g DW).

Total Flavonoid Content

Flavonoids were measured following Fattahi et al. (2014) [44]. A 0.5 mL extract was mixed with 1.5 mL methanol, 0.1 mL 10% AlCl3, 0.1 mL 1M CH3COOK, and 2.8 mL water. After 30 min of incubation, absorbance was read at 415 nm using quercetin standard (10–100 μg/mL). The results are expressed as mg quercetin equivalents/g DW (mg QE/g DW).

2.5. Antioxidant Properties

2.5.1. DPPH Radical Scavenging Assay

DPPH scavenging was measured following Smith et al. (2020) [45]. Extract concentrations (10–450 μg/mL) were mixed with 1 mL 0.1 mM DPPH, incubated (30 min dark), and read at 517 nm. Vitamin C (10–140 μg/mL) served as a control. Inhibition percentage was calculated: I% = [(Ac − Ae)/Ac] × 100 [46]. IC50 values (μg/mL) represent concentrations scavenging 50% DPPH radicals.

2.5.2. Ferric Reducing Antioxidant Power (FRAP)

FRAP was assessed via Fe3⁺ reduction; extract dilutions (5–100 μL/mL) were mixed with phosphate buffer and potassium ferricyanide, incubated (50 °C, 20 min), and then reacted with FeCl3 [47]. Absorbance was read at 700 nm against an ascorbic acid standard (5–60 μg/mL).

2.5.3. Total Antioxidant Capacity (TAC)

TAC was determined using phosphomolybdenum assay; extract concentrations (50–500 μg/mL; winter leaves 50–700 μg/mL) were mixed with molybdate reagent, incubated (95 °C, 90 min), and read at 695 nm [48]. Vitamin C (50–300 μg/mL) served as a reference.

2.6. Statistical Analysis

Data were analyzed by one-way ANOVA (p < 0.05) with Tukey’s post hoc test using R Commander (v3.1). Principal component analysis (PCA) was performed with Statbox AGRI software to evaluate Q. suber responses to edapho-climatic parameters and phytochemical composition.

3. Results

3.1. Rhizospheric Soil Analysis

Table 3 presents the physicochemical characteristics of the soil. Soil moisture (SM) was measured when the soil profile was opened in summer, for both depths (D1 and D2). SMD1% = 50.87%, SMD2% = 81.85%.
An analysis of the physical parameters of the rhizospheric soil at the two studied depths revealed a sandy–loamy texture with a low clay content. The chemical properties indicated acidic soil, with pH values ranging between 4.93 and 5.36. A significant variation in pH (p = 0.043) was observed between the D1 (0–15 cm) and D2 (15–25 cm) horizons, with higher values in the D2 horizon during winter.
Electrical conductivity (EC) showed a significant variation (p = 0.0001) between horizons, with mean values of 0.92 and 2.58 dS/m for D1 and D2, respectively. Carbon and total nitrogen contents exhibited highly significant variation between soil depths across both seasons (p < 0.0001). Mean carbon concentrations ranged from 2.59% to 12.87%, while total nitrogen levels varied from 0.17% to 0.53%.
The carbon-to-nitrogen ratio (C/N) exhibited significant differences (p = 0.0001) between horizons in summer, as well as between D1 and D2 in winter. The high C/N ratio (33.88 ± 15.89) in the D1 horizon during winter suggests slow organic matter decomposition. The cork oak forest soil had a low available phosphorus content with significant seasonal differences (p = 0.0001): 1.73 × 10−4 ± 0.14 g/Kg in summer compared to only 0.44 × 10−4 ± 0.035 g/Kg in winter.
The total polyphenol content in the rhizospheric soil was negatively influenced by the winter season and depth. Significant differences (p = 0.00001) were observed between rhizospheric soil at a 0–15 cm depth (D1RS) in summer (0.808 mg GAE/g) and D1RS in winter (0.210 mg GAE/g) compared to rhizospheric soil at a 15–25 cm depth (D2RS) in summer (0.028 mg GAE/g) and D2RS in winter (0.154 mg GAE/g soil) (Figure 2).

3.2. Plant Material Analysis

3.2.1. Chemical Composition

Roots

The quantification of secondary metabolites revealed the presence of three main classes of compounds in the roots: polyphenols, flavonoids, and tannins. Significant variations (p = 0.001) were observed in total polyphenols, total tannins, and flavonoid contents, modulated by season and depth. However, no significant differences were found in polyphenol and flavonoid concentrations between Root D1 and Root D2 roots in summer, nor between Root D1 in winter and Root D2 in summer (Figure 3).
A phytochemical analysis revealed distinct seasonal patterns in secondary metabolite accumulation within root systems. Total polyphenol and tannin concentrations were consistently elevated during the winter months at both soil depths examined (D1 and D2) (Figure 3). However, flavonoid accumulation exhibited a contrasting pattern at the D2 depth level, with significantly higher concentrations observed during summer compared to winter (Figure 3).
Roots collected at 15–25 cm depth (RD2) showed significantly higher (p = 0.0001) concentrations of total polyphenols, total tannins, and flavonoids compared to those from 0–15 cm (RD1). However, flavonoid content was greater in RD1 samples than in RD2 during winter.
Total polyphenol concentrations in RD2 roots exhibited a strong seasonal variation: 158.16 ± 4.2 mg GAE/g DW in summer versus 62.29 ± 0.94 mg GAE/g DW in winter, representing a 60.6% decrease; RD1 roots showed 95.47 ± 0.78 mg GAE/g DW in summer and 52.11 ± 7.69 mg GAE/g DW in winter (45.4% reduction), suggesting a significant environmental influence on their biosynthesis (Figure 3). Cork oak roots contained tannins ranging significantly from 21.28 ± 0.12 to 42.84 ± 0.36 mg TAE/g DW (Figure 3), with particularly high winter concentrations: 27.43 ± 0.1 mg TAE/g DW for RD1 and 42.84 ± 0.36 mg TAE/g DW for RD2. Flavonoids were also detected in the root extracts; although their concentrations were modest relative to TPP and tannins, they displayed significant seasonal fluctuations. RD2 roots displayed notable summer increases (15.97 ± 0.4 mg QE/g DW), threefold higher than winter levels (4.9 ± 0.4 mg QE/g DW. p = 0.0001), while RD1 maintained relatively stable concentrations (~12 mg QE/g DW) regardless of season (Figure 3).

Leaves

The quantitative analysis reveals highly significant seasonal fluctuations (p < 0.001, ANOVA) in foliar secondary metabolite accumulation in Q. suber (Figure 4). Notably, we observed a distinct seasonal partitioning of phenolic compounds: flavonoid (FLV) and total polyphenol (TPP) concentrations were significantly elevated during summer (FLV: 3.07 ± 0.5 mg QE/g DW, +52.46%; TPP: 170.21 ± 8.1 mg GAE/g DW, +37%; p < 0.001, Tukey’s), contrasting with a marked winter accumulation of condensed tannins (TT: 14.15 ± 1.2 mg TAE/g DW, +17.45% versus summer levels; p < 0.001) (Figure 4).
In each season, a significant difference between roots D1, D2, and Leave (p < 0.05) was observed, except for TPP in summer, where the difference was only significant between roots (D1 and D2) with Leave (p < 0.05) (Figure 5). The results show a highly significant differential distribution (p < 0.001, Tukey test) of phenolic compounds between aerial and underground tissues. An analysis revealed that roots at the D2 stage had significantly higher concentrations of total polyphenols (TPP: 158.16 ± 4.9 mg GAE/g DW) and condensed tannins (TT: 42.84 ± 0.36 mg TAE/g DW) compared to D1 roots (TPP: 95.47 ± 0.78 mg GAE/g DW; TT: 27.43 ± 0.1 mg TAE/g DW) and foliar tissues (TPP: 107.21 ± 0.13 mg TAE/g DW; TT: 14.15 ± 0.09 mg TAE/g WD). Notably, we observed an inverse accumulation pattern for flavonoids, which were preferentially concentrated in D1 roots (12.14 ± 0.14 mg QE/g DW), showing a significant 45.7% reduction in D2 root (4.9 ± 0.4 mg QE/g DW) (Figure 5).

3.2.2. Antioxidant Activity

A comparative analysis of seasonal antioxidant activity in Q. suber tissues revealed a significantly (p = 0.001) elevated free radical scavenging capacity during summer months relative to winter periods (p < 0.001). Both foliar and root tissues exhibited consistent seasonal patterns across all three assay systems. However, all three phytochemical assays (polyphenols, flavonoids, and tannins) revealed pronounced seasonal variations in antioxidant capacity. Quantitative evaluation using half-maximal inhibitory concentration (IC50) measurements demonstrated moderate antioxidant efficacy when compared to standard references such as vitamin C. These findings confirm the presence of bioactive compounds throughout the plant while highlighting their dynamic nature across seasons.

Roots

During both seasons, deep root extracts (RD2) exhibited superior antioxidant activity compared to surface roots (RD1) (Figure 6).
The DPPH (2,2-diphényl 1-picrylhydrazyle) assay revealed significant (p = 0.0001) depth- and season-dependent variations in radical scavenging capacity. Summer extracts exhibited higher antioxidant potency, with IC50 values of 131.58 ± 3.22 μg/mL (Root D2) and 146.88 ± 0.77 μg/mL (Root D1), whereas winter extracts showed a marked reduction in activity, requiring significantly higher concentrations (173.11 ± 2.64 μg/mL for Root D2 and 215.06 ± 12.44 μg/mL for Root D1, p < 0.0001), indicating a pronounced seasonal decline in free radical scavenging capacity (Figure 6).
The FRAP (Ferric Reducing Antioxidant Power) assay showed significant (p = 0.0001) differences between Root D2 and Root D1 extracts. Summer samples displayed IC50 values of 40.23 ± 0.26 μg/mL (Root D1) and 46 ± 0.75 μg/mL (Root D2), whereas winter samples exhibited a reversal in antioxidant efficacy, with IC50 values increasing to 92.07 ± 2.41 μg/mL (Root D1) and 50.88 ± 0.44 μg/mL (Root D1) in winter (Figure 6).
TAC (Total Antioxidant Capacity) analysis revealed highly significant (p < 0.0001) seasonal and depth-dependent variations. During summer, the IC₅₀ values for molybdenum reduction were 266.88 μg/mL in RD1 and 239.95 μg/mL in RD2, whereas in winter, these values increased to 413.20 μg/mL (RD1) and 306.15 μg/mL (RD2), indicating a seasonal decline in antioxidant capacity (Figure 6).

Leaves

Q. suber leaf extracts exhibited seasonally variable antioxidant activity, with summer IC50 130.90 ± 1.48 μg/mL versus winter 146.17 ± 1.87 μg/mL (Figure 7), indicating a mild winter efficacy reduction.
The antioxidant analysis of variance revealed significant seasonal variations (p = 0.0001) across all assays. The DPPH radical-scavenging activity showed markedly lower IC50 values during summer 130.90 ± 1.48 µg/mL versus 146.17 ± 1.87 µg/mL in winter, indicating a stronger antioxidant potential in warmer months. This variability showed a positive correlation with total polyphenol content, which was higher in summer months.
The FRAP assay revealed significantly greater activity in summer (IC50 = 61.22 ± 0.42 μg/mL) than in winter (63.74 ± 0.74 μg/mL; p = 0.0001).
The winter antioxidant activity (IC50 = 258.05 ± 3.25 µg/mL) while in summer exhibited significantly greater potency (IC50 = 196.86 ± 1.47 µg/mL), as demonstrated by TAC assay.

3.3. Statistical Analysis

The principal component analysis (PCA) reveals a clear structuring of the data along two main axes (F1: 70%; F2: 23%), collectively explaining 93% of the total variance (Figure 8).
F1 Axis Interpretation: The F1 axis strongly discriminates between harvest seasons, reflecting the predominant impact of seasonal climatic stresses. F2 Axis Interpretation: Simultaneously, the F2 axis organizes variables according to soil depth, highlighting the interaction between climatic and edaphic factors on the one hand and their combined role in modulating metabolic profiles on the other hand.
Therefore, the high explained variance (93%) demonstrates the predominant importance of seasonal variations and the role of pedological characteristics in regulating the metabolic pathways of Q. suber. This analysis establishes PCA as a relevant tool for deciphering the complex relationships between environmental variables, and the physiological responses in Q. suber.
The investigation of Q. suber in Azouza forest reveals a significant soil-mediated control of secondary metabolism. The profiles of secondary metabolism and antioxidant activity in both leaves and roots appear to be modulated by a complex interplay of edaphic and climatic factors. Principal component analysis (PCA) revealed a well-structured distribution of the data, with two principal axes explaining 93% of the total variance (F1: 70%; F2: 23%) (Figure 8).
Seasonal differentiation was clearly observed along the F1 axis, delineating two distinct clusters. The winter profile was characterized by elevated levels of total root polyphenols (TRP), total root tannins (TRT), and root FRAP activity (RFRAP), which were positively correlated with clay content (CL) (R = 0.90–0.99). Additionally, root total antioxidant capacity (RTAC) and root DPPH activity (RDPPH) were positively associated with other soil parameters, including silt content (SI), C/N ratio, and electrical conductivity (EC). Furthermore, a significant positive correlation was observed between low winter temperatures and increased antioxidant activity (DPPH, FRAP, TAC) in both leaf and root tissues, which coincided with an enhanced accumulation of root polyphenols (TRP) and tannins (TLT, TRT). In contrast, the summer cluster was defined by environmental conditions associated with water stress. Under these conditions, strong positive correlations (R = 1) were observed between reduced precipitation and phosphorus deficiency, and the enhanced biosynthesis of leaf polyphenols and flavonoids. Root flavonoid levels also increased, although the correlation was more moderate (R = 0.65).

4. Discussion

4.1. Sol Analysis

A pedological analysis of the forest soils revealed acidic conditions across both sampled depths (D1, D2), consistent with the preferred edaphic range for Q. suber, a well-adapted calcifuge species [49]. These findings align with previous reports from Algerian cork oak forests where pH ranged from 4.45 to 6.60 [50].
According to the classification by Mathieu and Pieltain (2003) [32], the D1 (0–15 cm) and D2 (15–25 cm) soil layers at the Erudite site are categorized as slightly saline during summer and winter, respectively. This salinity is attributed to a higher influx of saline water compared to drainage capacity, leading to salt accumulation in the soil profile, as also noted by Kalev and Toor (2018) [51]. Humus decomposition patterns showed distinct stratification with surface layers (D1) exhibiting higher C/N ratios characteristic of Mor-type humus and slower organic matter mineralization, while subsurface layers (D2) demonstrated significantly lower C/N ratios (p < 0.05), indicating more advanced humification, consistent with patterns reported by Berg et al. (2014) [52]. This pattern likely results from seasonal fluctuations in temperature and precipitation. The decrease in the C/N ratio with depth suggests more advanced humus degradation and stabilization in deeper layers [53]. The turnover process is effectively slowed down, indicating that the cork oak soil studied has a low assimilable phosphorus content. This low availability can be attributed to the soil’s acidity, which limits the mobility of phosphate ions (optimal at a pH of 6.5–7) [54].
The analysis demonstrates a significant decrease in soil phenolic content with depth (p < 0.001), consistent with previous findings in grassland ecosystems where total polyphenol (TPP) concentrations declined between 10–20 cm and 20–30 cm soil layers [55]. This vertical gradient, which is likely due to the limited leaching of phenolic compounds into deeper layers, further demonstrated that the release of secondary metabolites into the soil intensifies during drought periods [56,57]. TPP levels are also influenced by the input of above- and belowground plant residues [58,59], as well as by soil physicochemical properties such as pH, temperature, texture, and nutrient availability, which affect root exudation rates [60,61].

4.2. Chemical Composition and Antioxidant Activities of Vegatal Material

The quantification of total polyphenol in Q. suber roots revealed lower summer concentrations compared to values reported for Quercus ilex root by Meziti et al. (2019) [62] (490.81 mg GAE/g DW). Meanwhile, winter levels reflect intermediate adaptation between Portuguese (211.8 mg GAE/g DW) and other Mediterranean populations (10.6 mg GAE/g DW) as reported by Singh and Bisht (2018) [60] in Quercus oblongata from India, possibly reflecting distinct metabolic adaptations to seasonal stresses.
Notably, condensed tannin concentrations surpass the value reported for Q. ilex root by Solla et al. (2016) [63] (19 mg TAE/g DW in May, Madrid, Spain), corroborating Endo et al.’s (2021) [64] findings regarding Q. suber’s unique metabolic specialization. The preferential accumulation of tannins in root hypodermal layers immediately beneath the suberized exodermis supports their hypothesized dual function: physical–chemical barrier against pathogen ingress and reactive oxygen species scavenging during soil hypoxia events [51]. According to Tattini et al. (2006) [65], tannins are synthesized in very high concentrations in Mediterranean species. The contribution of root turnover to soil tannin enrichment further underscores their ecological importance in biogeochemical cycles and plant–soil interactions [66].
The quantification of summer flavonoid content in Q. suber revealed significantly higher concentrations than those reported for Q. ilex root by Meziti et al. (2019) [62] (3.11 mg QE/g DW), yet substantially lower than winter values documented in Calotropis procera by Mbinda and Musangi, 2021 [67] (43.09 mg QE/g DW). This differential accumulation, particularly pronounced in summer, corroborates observations on flavonoid induction by water stress, suggesting their protective role against drought [68].
The foliar polyphenol content of Q. suber from Azouzza forest exhibited significant climatic sensitivity, surpassing those reported for Q. cerris in Hungary (65.89 mg GAE/g DW) [69]. This divergence between the two species may be the result of specific genotypic adaptations and regional climatic gradients [70]. Winter leaf polyphenols (107.21 mg GAE/g DW) fell between extreme values reported by Custódio et al. (2015) [17] in Portugal (211.8 mg GAE/g DW) and by Lavado et al. (2021) [71] in autumn (10.6 mg GAE/g DW). These variations confirm the determining role of abiotic factors (temperature, water availability) in modulating secondary metabolism in Q. suber from Azouza forest, as observed in other Mediterranean taxa [70].
The tannin concentrations observed in this study were significantly lower than those reported for Iranian oak species (Q. persica: 73 mg TAE/g DW; Q. infectoria: 109 mg TAE/g DW; Q. libani: 100 mg TAE/g DW) [72] yet substantially exceeded values for Q. coccifera in Turkey (0.4 mg TAE/g DW), confirming interspecific heterogeneity in tannin profiles and geographical influences on their biosynthesis [73].
The accumulation of flavonoids observed in summer exceeded the values reported for Q. cerris in Hungary (3.76 mg QE/g DW) by Tálos-Nebehaj et al. (2017) [69], while their winter persistence suggests a role in protection against cold-related photo-oxidative damage. However, observed levels remained below those documented for Q. suber in other Mediterranean regions, highlighting the impact of local climatic gradients on their production [17,71,74]. These results corroborate conclusions about flavonoid sensitivity to environmental conditions and harvest timing, reflecting their plasticity as physiological markers of seasonal stresses [75].
The observed antioxidant activity aligns with previous Mediterranean studies that reported Q. suber’s phytochemical content [17,62,71] while demonstrating significant seasonal variability that reflects that the species from Azouzza forest have an adaptive response to abiotic stressors, particularly photosynthetically active radiation temperature extremes, and drought intensity. The moderate efficacy compared to vitamin C indicates that while the individuals studied (Q. suber) contained valuable antioxidants, their potency may be context-dependent on environmental conditions.
The study revealed that Q. suber roots exhibit seasonally modulated antioxidant activity, with summer DPPH inhibition (IC50) significantly surpassing values reported for Q. ilex root bark by bark Meziti et al. (2019) [62] (5.67 ± 0.09 μg/mL). This interspecific variation likely stems from three key factors. Genetic divergence in phenylpropanoid pathway regulation, particularly RAV1 gene expression patterns identified by Magalhães et al. (2016) [76] as drought-responsive in Q. suber, or methodological differences in solvent extraction efficiency and ecological adaptation gradients across Mediterranean biomes [69,71]. Compared to Q. oblongata roots (IC50 3.48 μg/mL) reported by Singh and Bisht (2018) [60], Q. suber roots maintain notable DPPH scavenging capacity even in winter. These contrast with [49] findings for Q. ilex roots (IC50 8.55 ± 1.52 μg/mL).
The FRAP assay results contrast with those reported by Meziti et al. (2019) [62] for Quercus ilex roots, which exhibited a significantly lower IC50 value of 8.55 ± 1.52 μg/mL.
The molybdenum reduction capacity of root extracts from both soil depths was lower than that reported by Toori et al. (2014) [77] for Q. robur bark, which exhibited an IC₅₀ value of 5.13 ± 1 µg/mL.
Cork oak leaves from the Aït Hammad site exhibited notable free radical scavenging capacity. Comparative analysis showed that the IC₅₀ values recorded in summer were lower than those reported for Q. cerris and Q. petraea [69]. In contrast, the winter radical scavenging activity exceeded that reported for Mediterranean Q. suber (IC₅₀ = 54.5 μg/mL) [71], as well as for Q. ilex (IC50 = 9.39–11.31 μg/mL) [78].
The notably high radical-scavenging capacity observed in our study suggests that leaves from this population may exhibit a distinctive phenolic profile, potentially involving synergistic or antagonistic interactions among bioactive compounds. This variability showed positive correlation with total polyphenol content, which was higher during summer months, confirming the predominant role of phenolic compounds in antioxidant activity—consistent with findings in Sorghum bicolor [79].
The iron-reducing capacity of cork oak leaves from the Aït Hammad site during summer was higher than that reported for Q. robur leaf extracts from Portuguese populations (IC50 = 153.8 ± 26.3 μg/mL), suggesting a comparatively stronger antioxidant potential in this population [80]. However, in winter, the IC50 value exceeded that reported by Lavado et al. (2021) [71] for ethanolic extracts of Q. suber leaves in Spain (IC50 = 54.5 µg/mL). Such differences can be expected between phylogenetically distant species, as evolutionary divergence influences the synthesis of secondary metabolites [81].
TAC analysis revealed striking contrasts with previously reported values, such as 13.82 µg/mL for Q. suber leaves [74] and 418.26 µg/mL for Q. ilex acorns [82]. These findings highlight a pronounced seasonal modulation of antioxidant metabolism, alongside notable geographic variability in phenolic expression. The data also suggest that Q. suber populations from Azouzza forest exhibit distinct metabolic responses to prevailing climatic conditions.

4.3. Correlation Studies

The differential accumulation of phenolic compounds and antioxidant activity between the season and the roots of two deep cork oaks from Azouza forest may reflect the behavior of these trees with respect to the abiotic stress studied (drought, cold, and soil properties).
These findings reveal a pronounced seasonal modulation of antioxidant metabolism in Q. suber with geographic variability in phenolic expression and distinct species-specific responses to climatic conditions. The significant metabolic diversity observed suggests this species employs markedly different antioxidant strategies across tissues and seasons. A comparative analysis of leaf versus root tissues demonstrates organ-specific adaptation mechanisms, reflecting differential ecological roles in stress response. The antioxidant system of Q. suber emerges as an integrated stress-adaptation framework, where soil–climate interactions dynamically regulate phenolic biosynthesis pathways. The notable metabolic diversity in Q. suber is reflected in its distinctly different antioxidant profiles, as well as in its tissue-specific responses. Comparisons between leaf and root tissues reveal organ-dependent adaptation strategies.
Mediterranean summers characterized by intense heat waves inducing simultaneous water and thermal stress, contrasting cool to cold winter conditions [76,83]. These results corroborate the known mechanisms of secondary metabolite induction by abiotic stress [84] and confirm the significant differences detected by ANOVA, seasonal and edaphic dynamics of phenolic compounds in individuals from the AIT HAMMAD site, and adaptive strategies in Mediterranean environments consistent with the observations of [71], confirming the adaptive mechanisms described by [85].
Edaphic parameters appear to have an effect on the vertical stratification of secondary metabolites. Deeper horizons are characterized by greater hydric and thermal stability [86]. These findings align with the work of [87] on phenolic pathway modulation by nutrient availability at different depths and [88] on antioxidant strategy optimization along soil profiles.
The clay fraction of the soil appears to influence metabolite biosynthesis through a dual mechanism. First, it exerts a direct stress effect by limiting water availability and restricting nutrient diffusion in clay-rich substrates [89]. Second, it indirectly modulates plant metabolic responses by altering the composition and functionality of the rhizosphere microbial community, likely through the formation of organo-mineral complexes that affect the bioavailability of key elements [90,91]. Interestingly, soils with a lower clay content tend to promote mycorrhizal associations, which, in turn, can stimulate the production of flavonoids involved in root signaling and symbiotic interactions [92,93]. These complex interactions between the mineral matrix, microbiota, and plant metabolism [94] underscore the key role of pedogenesis in shaping adaptive strategies of Mediterranean plants.
The limited phosphorus availability in the soil and water stress surrounding the studied oak trees appear to influence their adaptive responses, notably through the enhanced accumulation of flavonoids in the leaves and roots. This response is likely multifaceted. On the one hand, flavonoids may serve a photoprotective function, mitigating the adverse effects of reduced photosynthetic efficiency under nutrient stress [95]. On the other hand, the root-specific exudation of flavonoids (e.g., daidzein) and isoflavonoids may promote beneficial mycorrhizal associations and contribute to the mobilization of otherwise unavailable phosphorus and iron forms [96,97]. In line with this, previous studies have shown that the plant defense system against abiotic stress—such as water deficit—is closely linked to the bioactivity of phenolic compounds in leaves. These processes are particularly active in summer, where combined water stress and mineral deficiency enhance phenolic biosynthesis. Observations in Medicago truncatula [98] and Cucumis melo [99] confirm flavonoids as chemical mediators in the rhizosphere, preferentially accumulating in root caps and exudation zones. This metabolic strategy, though carbon-costly, optimizes nutrient acquisition in phosphorus-poor Mediterranean soils [100].
Summer drought and reduced precipitation intensify water stress, leading to elevated production of reactive oxygen species (ROS) within the thylakoid membranes, which contributes to the degradation of photosynthetic pigments [101]. In response, polyphenolic compounds contribute to photoprotection and oxidative stress mitigation through several complementary mechanisms. They act as optical screens, limiting excess light absorption by chlorophyll molecules, dissipate surplus light energy via blue fluorescence emission, and neutralize ROS, thereby preserving cellular integrity [101,102]. These protective mechanisms are accompanied by a redistribution of secondary metabolites toward exposed aerial organs, where they play a critical role in plant defense under drought conditions, primarily through their antioxidant activity [84].
The weaker correlation observed in roots (R = 0.68) suggests a preferential allocation of carbon resources to aerial organs under conditions of acute summer water stress, while maintaining a basal level of flavonoid production to sustain rhizospheric interactions [103]. This pattern indicates that the accumulation of flavonoids in the leaves of the studied oaks may represent a convergent adaptive response to both phosphorus limitation and drought stress, highlighting the multifunctional role of secondary metabolites in plant stress physiology.
The plant response to low temperatures involves a coordinated set of physiological mechanisms. The cold-induced disruption of photosynthetic processes leads to an increase in reactive oxygen species (ROS) production [104]. This is accompanied by the activation of phenolic biosynthetic pathways, particularly through the induction of phenylalanine ammonia-lyase (PAL), a key enzyme in the phenylpropanoid pathway [105]. In parallel, low temperatures promote structural remodeling of chloroplast membranes, enhancing the accumulation of accessory pigments such as xanthophylls and the synthesis of secondary metabolites [106]. In Mediterranean woody species such as Q. ilex, this response is further characterized by a reorganization of carbon allocation toward the production of defensive compounds [107]. Additionally, winter-induced soil anaerobiosis appears to potentiate root-based adaptive responses. Together, these complex metabolic adjustments underscore the pivotal role of polyphenols in acclimation to seasonal thermal stress [108].
A correlation analysis revealed complex interactions between phenolic compound pools and their associated biological functions. Root polyphenols (TRP) exhibit strong synergistic relationships with tannins, likely reflecting their role in defense against soil-borne pathogens and in mitigating oxidative stress in the rhizosphere [109]. The observed negative correlation between total leaf phenolics (TLP) and TRP suggests a strategic partitioning of carbon resources, whereby plants allocate phenolic precursors between aerial and belowground organs according to physiological demands, as previously reported in Q. robur [110]. This trade-off highlights the essential role of phenolics in leaf oxidative stress protection [111].
The underlying structure–activity relationships are driven by two key factors: the ability of phenolic hydroxyl groups to chelate redox-active metals (e.g., Fe3⁺, Mo⁶⁺) and scavenge free radicals, and tissue-specific specialization, with leaves prioritizing photoprotection while roots enhance chemical defenses in the rhizosphere [112].

5. Conclusions

This research highlights the seasonal and edaphic dynamics of phenolic compounds and antioxidant activity in Quercus suber from Azouza forest in the Algerian Mediterranean region. The findings demonstrate significant metabolic adaptations to abiotic stresses, marked by a differential accumulation of polyphenols, tannins, and flavonoids across seasons and soil depths. Seasonal variation accounted for 70% of the observed phytochemical variability, emphasizing the interplay between climatic and soil factors.
These results underscore the necessity of integrating climatic and soil parameters into sustainable management strategies for cork oak forests. Additionally, the study paves the way for exploring cork oak bioactive compounds in pharmaceutical and agri-food applications. Future research should focus on the molecular mechanisms behind these adaptations and the role of plant–microbiota interactions in secondary metabolite production. Overall, this work enhances our understanding of Mediterranean ecosystems and highlights the urgent need to protect these habitats amid increasing environmental pressures.

Author Contributions

Writing—original draft, M.H.-B.; conceptualization, M.H.-B., S.K.-B. and M.O.B.; methodology, M.H.-B., S.K.-B. and M.O.B.; data curation N.M.-G., N.A.I., N.S.B., M.B. and K.H.; formal analysis, E.-H.N. and N.K.; validation, M.S.A., M.H.-B., E.-H.N. and K.H.; investigation, N.M.-G.; visualization, M.H.-B., S.K.-B., L.T. and K.H.; supervision and validation, E.-H.N., M.B., L.T. and K.H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported and funded by the Deanship of Scientific Research at Imam Mohammad Ibn Saud Islamic University (IMSIU) (grant number, IMSIU-DDRSP2502).

Institutional Review Board Statement

The experimental protocol was approved by the ethics committee of our university (N°Ethi/UMMTO/26-MAR-2024).

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets used during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Acknowledgments

We deeply regret the loss of our dear colleague and friend, Malika Boudiaf, whose inspiration and dedication laid the foundations for this research. Her passion, wisdom, and contributions were invaluable, and her absence leaves a deep void in our hearts and in our work. Although she is no longer with us, her legacy lives on through the knowledge she helped create and the lives she touched. We will always be grateful for her guidance and commitment. Rest in peace, Malika. We will always remember you.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

pH-H2O: hydrogen potential of water/EC: Electrical Conductivity/C/N: Carbon/Nitrogen/P: Phosphorus/Clay: CL/Sand: S/Silt: SI/TPP SR: Total Polyphenols in Rhizospheric Soil/Total Root Polyphenols: TRP/Total Leaf Polyphenols: TLP/Total Leaf Tannins: TLT/Leaf Flavonoids: LF/Total Root Tannins: TRT/Root Flavonoids: RF/Leaf FRAP: L FRAP/Leaf DPPH: L DPPH/Leaf TAC: L TAC/Root FRAP: R FRAP/Root DPPH: R DPPH/Root TAC: R TAC/Temperature: T/Precipitation: PR.

References

  1. Albassatneh, M.; Escudero, M.; Monnet, A.; Arroyo, J.; Bacchetta, G.; Bagnoli, F.; Dimopoulos, P.; Hampe, A.; Leriche, A.; Médail, F.; et al. Spatial patterns of genus-level phylogenetic endemism in the tree flora of Mediterranean Europe. Divers. Distrib. 2021, 27, 913–928. [Google Scholar] [CrossRef]
  2. Moreno, M.; Simioni, G.; Cailleret, M.; Ruffault, J.; Badel, É.; Carrière, S.; Davi, H.; Gavinet, J.; Huc, R.; Limousin, J.; et al. Consistently lower sap velocity and growth over nine years of rainfall exclusion in a Mediterranean mixed pine-oak forest. Agric. For. Meteorol. 2021, 308, 108472. [Google Scholar] [CrossRef]
  3. Almeida, T.; Pinto, G.; Correia, B.; Gonçalves, S.; Meijón, M.; Escandón, M. In-depth analysis of the Quercus suber metabolome under drought stress and recovery reveals potential key metabolic players. Plant Sci. 2020, 299, 110606. [Google Scholar] [CrossRef]
  4. Li, T.; Tiiva, P.; Rinnan, Å.; Julkunen-Tiitto, R.; Michelsen, A.; Rinnan, R. Long-term effects of elevated CO2, nighttime warming and drought on plant secondary metabolites in a temperate heath ecosystem. Ann. Bot. 2020, 125, 1065–1075. [Google Scholar] [CrossRef]
  5. Hussain, M.S.; Fareed, S.; Ansari, S.; Rahman, M.A.; Ahmad, I.Z.; Saeed, M. Current approaches toward production of secondary plant metabolites. J. Pharm. Bioallied Sci. 2012, 4, 10–20. [Google Scholar] [CrossRef]
  6. Wink, M. Modes of action of herbal medicines and plant secondary metabolites. Medicines 2015, 2, 251–286. [Google Scholar] [CrossRef]
  7. Beran, F.; Köllner, T.G.; Gershenzon, J.; Tholl, D. Chemical convergence between plants and insects: Biosynthetic origins and functions of common secondary metabolites. New Phytol. 2018, 223, 52–67. [Google Scholar] [CrossRef]
  8. Yang, L.; Wen, K.S.; Ruan, X.; Zhao, Y.X.; Wei, F.; Wang, Q. Response of plant secondary metabolites to environmental factors. Molecules 2018, 23, 762. [Google Scholar] [CrossRef]
  9. Ashraf, M.A.; Iqbal, M.; Rasheed, R.; Hussain, I.; Riaz, M.; Arif, M.S. Environmental Stress and Secondary Metabolites in Plants: Chapter 8—An Overview. In Plant Metabolites and Regulation Under Environmental Stress; Academic Press: Cambridge, MA, USA, 2018. [Google Scholar]
  10. Touhami, I.; Chirino, E.; Aouinti, H.; Khorchani, E.; Elaieb, M.; Khaldi, A.; Nasr, Z. Decline and dieback of cork oak (Quercus suber L.) forests in the Mediterranean basin: A case study of Kroumirie, Northwest Tunisia. J. For. Res. 2020, 31, 1461–1477. [Google Scholar] [CrossRef]
  11. Von Essen, M.; Rosário, I.; Santos-Reis, M.; Nicholas, K. Valuing and mapping cork and carbon across land use scenarios in a Portuguese montado landscape. PLoS ONE 2019, 14, e0212174. [Google Scholar] [CrossRef]
  12. Zhao, M.; Running, S.W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 2010, 329, 940–943. [Google Scholar] [CrossRef] [PubMed]
  13. Natali, L.; Vangelisti, A.; Guidi, L.; Remorini, D.; Cotrozzi, L.; Lorenzini, G.; Nali, C.; Pellegrini, C.; Trivellini, C.; Vernieri, P.; et al. How Quercus ilex L. saplings face combined salt and ozone stress: A transcriptome analysis. BMC Genom. 2018, 19, 87. [Google Scholar] [CrossRef] [PubMed]
  14. Thyroff, E.; Burney, O.; Mickelbart, M.; Jacobs, D. Unraveling shade tolerance and plasticity of semi-evergreen oaks: Insights from maritime forest live oak restoration. Front. Plant Sci. 2019, 10, 1526. [Google Scholar] [CrossRef] [PubMed]
  15. Puyo, J.Y. Grandeurs et vicissitudes de l’aménagement des suberaies algériennes durant la période coloniale française (1830–1962). Forêt Méditerranéenne 2013, 34, 129–142. [Google Scholar]
  16. Gentilesca, T.; Camarero, J.J.; Colangelo, M.; Nolã, A.; Ripullone, F.; Nole, A. Drought-induced oak decline in the western Mediterranean region: An overview on current evidences, mechanisms and management options to improve forest resilience. iForest 2017, 10, 796–806. [Google Scholar] [CrossRef]
  17. Custódio, A.L.; Madeira, J.F.A. GLODS: Global and Local Optimization using Direct Search. J. Glob. Optim. 2015, 62, 1–28. [Google Scholar] [CrossRef]
  18. Santos, S.A.; Pinto, P.C.; Silvestre, A.J.; Neto, C.P. Chemical composition and antioxidant activity of phenolic extracts of cork from Quercus suber L. Ind. Crops Prod. 2010, 31, 521–526. [Google Scholar] [CrossRef]
  19. Touati, R.; Santos, S.A.; Rocha, S.M.; Belhamel, K.; Silvestre, A.J. The potential of cork from Quercus suber L. grown in Algeria as a source of bioactive lipophilic and phenolic compounds. Ind. Crops Prod. 2015, 76, 936–945. [Google Scholar] [CrossRef]
  20. Aronson, J. Current state of knowledge of wind energy impacts on bats in South Africa. Acta Chiropterologica 2022, 24, 221–238. [Google Scholar] [CrossRef]
  21. IPCC. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; Masson-Delmotte, V., Zhai, P., Pirani, A., Connors, S.L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Gomis, M.I., et al., Eds.; Cambridge University Press: Cambridge, UK, 2021. [Google Scholar]
  22. UNDP. United Nations Development Programme Annual Report 2023; UNDP: New York, NY, USA, 2023. [Google Scholar]
  23. Ghefar, M.; Dehane, B. Etude des paramètres réglant la production du liège dans la subéraie de M’Sila (Oran, Algérie). Agric. For. J. 2018, 2, 48–58. [Google Scholar]
  24. Bouzid, A.; Bouzid, K.; Benabdeli, K. Contribution the Failure Mode Analysis and Criticality Evaluation Method to the Rehabilitation of Cork Oak (Quercus suber) Forests in Forest Massif of Tlemcen (Algeria). J. Manaj. Hutan Trop. 2022, 28, 191. [Google Scholar] [CrossRef]
  25. Orgeas, J.; Ourcival, J.M.; Bonin, G. Seasonal and spatial patterns of foliar nutrients in cork oak (Quercus suber L.) growing on siliceous soils in Provence (France). Plant Ecol. 2003, 164, 201–211. [Google Scholar] [CrossRef]
  26. Soil Science Society of America. Soil Analysis: A Comprehensive Guide; SSSA: Madison, WI, USA, 2020. [Google Scholar]
  27. Gee, G.; Bauder, J.W. Particule-size analysis. In Methods of Soil Analysis, Part 1: Physical and Mineralogical Methods; Klute, A., Ed.; American Society of Agronomy: Madison, WI, USA, 1986; pp. 383–411. [Google Scholar]
  28. ISO 11277:2020; Soil Quality—Determination of Particle Size Distribution in Mineral Soil Material—Method by Sieving and Sedimentation. ISO: Geneva, Switzerland, 2020.
  29. Aubert, M.; Yéne’ Atangana, Q. Self-potential method in hydrogeological exploration of volcanic areas. Ground Water 1996, 34, 1010–1016. [Google Scholar] [CrossRef]
  30. Deng, J.; Camenen, B.; Legoût, C.; Nord, G. Estimation of fine sediment stocks in gravel bed rivers including the sand fraction. Sedimentology 2023, 71, 152–172. [Google Scholar] [CrossRef]
  31. Olsen, S.R.; Cole, C.V.; Watanabe, F.S. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate; USDA Circular No. 939; US Government Printing Office: Washington, DC, USA, 1954. [Google Scholar]
  32. Mathieu, C.; Pieltain, F.; Jeanroy, E. Analyse Chimique des Sols: Méthodes Choisies; Tec & Doc: Paris, France, 2003; pp. 33–48. [Google Scholar]
  33. Bremner, J.M. Determination of nitrogen in soil by the Kjeldahl method. J. Agric. Sci. 1960, 55, 11–33. [Google Scholar] [CrossRef]
  34. Dallali, S.; Rouz, S.; Aichi, H.; Hassine, H.B. Phenolic content and allelopathic potential of leaves and rhizosphere soil aqueous extracts of white horehound (Marrubium vulgare L.). J. New Sci. 2017, 39, 2106–2120. [Google Scholar]
  35. Blum, K.; Noble, E.P.; Sheridan, P.J.; Finley, O.; Montgomery, A.; Ritchie, T.; Ozkaragoz, T.; Fitch, R.J.; Sadlack, F.; Sheffield, D. Association of the A1 allele of the D2 dopamine receptor gene with severe alcoholism. Alcohol 1991, 8, 409–416. [Google Scholar] [CrossRef]
  36. Box, J.D. Investigation of the Folin-Ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res. 1983, 17, 511–525. [Google Scholar] [CrossRef]
  37. Miftode, A.M.; Stefanache, A.; Şpac, A.F.; Miftode, R.S.; Miron, A.; Dorneanu, V. In vitro measurement of total antioxidant capacity of Crataegus macracantha Lodd leaves. Rev. Med.-Chir. Soc. Med. Nat. Iași 2016, 120, 2. [Google Scholar]
  38. Bourgou, S.; Beji, R.S.; Medini, F.; Ksouri, R. Effet du solvant et de la méthode d’extraction sur la teneur en composés phénoliques et les potentialités antioxydantes d’Euphorbia helioscopia. J. New Sci. 2016, 28, 1649–1655. [Google Scholar]
  39. Ouzid, Y.; Smail-Saadoun, N.; Houali, K. Comparative study of in vitro antioxidant activity of foliar endophytic fungi and leaves extracts of Peganum harmala of Dayateaiat (Laghouat, Algeria). J. Fundam. Appl. Sci. 2018, 10, 147–157. [Google Scholar] [CrossRef]
  40. Li, H.B.; Cheng, K.W.; Wong, C.C.; Fan, K.W.; Chen, F.; Jiang, Y. Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem. 2007, 102, 771–776. [Google Scholar] [CrossRef]
  41. Górnaś, P.; Rudzińska, M. Seeds recovered from industry by-products of nine fruit species with a high potential utility as a source of unconventional oil for food and non-food purposes. Food Chem. 2016, 213, 133–142. [Google Scholar]
  42. Naczk, M.; Oickle, D.; Pink, D.; Shahidi, F. Protein precipitating capacity of crude canola tannins: Effect of pH, tannin, and protein concentrations. J. Agric. Food Chem. 1996, 44, 2144–2148. [Google Scholar] [CrossRef]
  43. Hagerman, A.E.; Butler, L.G. Determination of protein in tannin-protein precipitates. J. Agric. Food Chem. 1980, 28, 944–947. [Google Scholar] [CrossRef]
  44. Fattahi, S.; Zabihi, E.; Abedian, Z.; Pourbagher, R.; Motevalizadeh Ardekani, A.; Mostafazadeh, A.; Akhavan-Niaki, H. Total phenolic and flavonoid contents of aqueous extract of stinging nettle and in vitro antiproliferative effect on Hela and BT-474 cell lines. Int. J. Mol. Cell. Med. 2014, 3, 102–107. [Google Scholar]
  45. Smith, J.; Johnson, L.; Wang, R. Updated methods for measuring DPPH radical scavenging activity. J. Food Sci. 2020, 85, 1234–1240. [Google Scholar]
  46. Dupont, A. Vitamin C as a control in antioxidant assays. Food Chem. 2021, 345, 128–135. [Google Scholar]
  47. Fejes, S.; Blázovics, A.; Lugasi, A.; Lemberkovics, É.; Petri, G.; Kéry, Á. In vitro antioxidant activity of Anthriscus cerefolium L. (Hoffm.) extracts. J. Ethnopharmacol. 2000, 69, 259–265. [Google Scholar] [CrossRef]
  48. Prieto, P.; Pineda, M.; Aguilar, M. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E. Anal. Biochem. 1999, 269, 337–341. [Google Scholar] [CrossRef]
  49. Mechergui, T.; Pardos, M.; Boussaidi, N.; Jacobs, D.F.; Catry, F.X. Problems and solutions to cork oak (Quercus suber L.) regeneration: A review. Inst. Cienc. For. (ICIFOR) 2023, 16, 10–22. [Google Scholar] [CrossRef]
  50. Kaci, M.B.N.; Ahmed, S.O.; Saad, L.; Halimi, R.; Khelfaoui, L.; Issaoun, D. Effect of fire recurrence on abundance and distribution of soil fauna under Quercus suber L. in Taksebt forest Zekri (Algeria). J. New Sci. 2018, 1, 3290–3298. [Google Scholar]
  51. Kalev, S.D.; Toor, G.S. The composition of soils and sediments. In Green Chemistry; Elsevier: Amsterdam, The Netherlands, 2018; pp. 339–357. [Google Scholar]
  52. Berg, B.; McClaugherty, C. Plant Litter: Decomposition, Humus Formation, Carbon Sequestration; Springer: Berlin, Germany, 2003. [Google Scholar]
  53. Batjes, N.H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 2014, 65, 10–21. [Google Scholar] [CrossRef]
  54. Penn, C.J.; Camberato, J.J. A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 2019, 9, 120. [Google Scholar] [CrossRef]
  55. Zeng, J.; Chen, H.; Bai, Y.; Dong, F.; Peng, C.; Yan, F.; Yang, G. Water table drawdown increases plant biodiversity and soil polyphenol in the Zoige Plateau. Ecol. Indic. 2021, 121, 107118. [Google Scholar] [CrossRef]
  56. Kainulainen, P.; Holopainen, J.K. Concentrations of secondary compounds in Scots pine needles at different stages of decomposition. Soil Biol. Biochem. 2002, 34, 37–42. [Google Scholar] [CrossRef]
  57. Ehlers, B.K.; Berg, M.P.; Staudt, M.; Holmstrup, M.; Glasius, M.; Ellers, J.; Peñuelas, J. Plant secondary compounds in soil and their role in belowground species interactions. Trends Ecol. Evol. 2020, 35, 716–730. [Google Scholar] [CrossRef]
  58. Preston, C.; Bhatti, J.; Flanagan, L.; Norris, C. Stocks, chemistry and sensitivity to climate change of dead organic matter along the Canadian boreal forest transect case study. Clim. Change 2006, 74, 223–251. [Google Scholar] [CrossRef]
  59. Kanerva, S.; Kitunen, V.; Loponen, J.; Smolander, A. Phenolic compounds and terpenes in soil organic horizon layers under silver birch, Norway spruce and Scots pine. Biol. Fertil. Soils 2008, 44, 547–556. [Google Scholar] [CrossRef]
  60. Singh, A.; Bisht, M. Evaluation of in-vitro antioxidant potential and in-vivo hepatoprotective activity of root extract of Quercus oblongata D. DON. J. Drug Deliv. Ther. 2018, 8, 152–161. [Google Scholar] [CrossRef]
  61. Gargallo-Garriga, A.; Preece, C.; Sardans, J.; Oravec, M.; Urban, O.; Peñuelas, J. Root exudate metabolomes change under drought and show limited capacity for recovery. Sci. Rep. 2018, 8, 12696. [Google Scholar] [CrossRef] [PubMed]
  62. Meziti, H.; Bouriche, H.; Kada, S.; Demirtas, I.; Kizil, M.; Senator, A.; Garrido, G. Phytochemical analysis, and antioxidant, anti-hemolytic and genoprotective effects of Quercus ilex L. and Pinus halepensis Mill. methanolic extracts. J. Pharm. Pharmacogn. Res. 2019, 7, 260–272. [Google Scholar] [CrossRef] [PubMed]
  63. Solla, A.; Milanović, S.; Gallardo, A.; Bueno, A.; Corcobado, T.; Cáceres, Y.; Pulido, F. Genetic determination of tannins and herbivore resistance in Quercus ilex. Tree Genet. Genomes 2016, 12, 117. [Google Scholar] [CrossRef]
  64. Endo, I.; Kobatake, M.; Tanikawa, N.; Nakaji, T.; Ohashi, M.; Makita, N. Anatomical patterns of condensed tannin in fine roots of tree species from a cool-temperate forest. Ann. Bot. 2021, 128, 59–71. [Google Scholar] [CrossRef]
  65. Tattini, M.; Remorini, D.; Pinelli, P.; Agati, G.; Saracini, E.; Traversi, M.L.; Massai, R. Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytol. 2006, 170, 779–794. [Google Scholar] [CrossRef]
  66. Peter Constabel, C.; Yoshida, K.; Walker, V. Diverse ecological roles of plant tannins: Plant defense and beyond. Recent Adv. Polyphen. Res. 2014, 4, 115–142. [Google Scholar]
  67. Yuan, Y.; Liu, Y.; Wu, C.; Chen, S.; Wang, Z.; Yang, Z.; Huang, L. Water deficit affected flavonoid accumulation by regulating hormone metabolism in Scutellaria baicalensis Georgi roots. PLoS ONE 2012, 7, e42907. [Google Scholar] [CrossRef]
  68. Mbinda, W.; Musangi, C. Antioxidant activity, total phenolic and total flavonoid. J. Phytopharm. 2019, 8, 161–166. [Google Scholar] [CrossRef]
  69. Tálos-Nebehaj, E.; Hofmann, T.; Albert, L. Seasonal changes of natural antioxidant content in the leaves of Hungarian forest trees. Ind. Crops Prod. 2017, 98, 53–59. [Google Scholar] [CrossRef]
  70. Ruiz-Rodríguez, B.M.; Morales, P.; Fernández-Ruiz, V.; Sánchez-Mata, M.C.; Cámara, M.; Díez-Marqués, C.; Tardío, J. Valorization of wild strawberry-tree fruits (Arbutus unedo L.) through nutritional assessment and natural production data. Food Res. Int. 2011, 44, 1244–1253. [Google Scholar] [CrossRef]
  71. Lavado, G.; Ladero, L.; Cava, R. Cork oak (Quercus suber L.) leaf extracts potential use as natural antioxidants in cooked meat. Ind. Crops Prod. 2021, 160, 113086. [Google Scholar] [CrossRef]
  72. Elahi, M.Y.; Rouzbehan, Y. Characterization of Quercus persica, Quercus infectoria and Quercus libani as ruminant feeds. Anim. Feed Sci. Technol. 2008, 140, 78–89. [Google Scholar] [CrossRef]
  73. Ulusu, F.; Darıcı, C. The influence of tannins purified from Eastern Mediterranean Region plants (Pinus brutia Ten. and Quercus coccifera L.) on carbon mineralization: Antimicrobial and antimutagenic evaluation. Anatol. J. Bot. 2023, 7, 60–69. [Google Scholar] [CrossRef]
  74. Frouja, O.; Hammami, M.; Dakhlaoui, S.; Wannes, W.A.; Hessini, K.; Msaada, K.; Ahmed, H.B. Intra and interspecific variability of Quercus suber and Quercus canariensis, an intrinsic water-use efficiency approach for differentiation. Environ. Res. Commun. 2022, 4, 105002. [Google Scholar] [CrossRef]
  75. Yarnes, C.T.; Boecklen, W.J.; Tuominen, K.; Salminen, J.P. Defining phytochemical phenotypes: Size and shape analysis of phenolic compounds in oaks (Fagaceae, Quercus) of the Chihuahuan Desert. Botany 2006, 84, 1233–1248. [Google Scholar] [CrossRef]
  76. Magalhães, A.P.; Verde, N.; Reis, F.; Martins, I.; Costa, D.; Lino-Neto, T.; Azevedo, H. RNA-Seq and gene network analysis uncover activation of an ABA-dependent signalosome during the cork oak root response to drought. Front. Plant Sci. 2016, 7, 1195. [Google Scholar] [CrossRef]
  77. Toori, M.A.; Mirzaei, M.; Mirzaei, N.; Lamrood, P.; Mirzaei, A. Antioxidant and hepatoprotective effects of the internal layer of oak fruit (Jaft). J. Med. Plants Res. 2013, 7, 24–28. [Google Scholar]
  78. Hadidi, L.; Babou, L.; Zaidi, F.; Valentao, P.; Andrade, P.B.; Grosso, C. Quercus ilex L.: How season, plant organ and extraction procedure can influence chemistry and bioactivities. Chem. Biodivers. 2017, 14, e1600187. [Google Scholar] [CrossRef]
  79. Awika, J.M.; Rooney, L.W.; Wu, X.; Prior, R.L.; Cisneros-Zevallos, L. Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. J. Agric. Food Chem. 2003, 51, 6657–6662. [Google Scholar] [CrossRef]
  80. Almeida, I.F.; Amaral, M.H.; Costa, P.C.; Bahia, M.F.; Valentao, P.; Andrade, P.B.; Pereira, T.M. Oak leaf extract as topical antioxidant: Free radical scavenging and iron chelating activities and in vivo skin irritation potential. Biofactors 2008, 33, 267–279. [Google Scholar] [CrossRef]
  81. Nikolaos, G.; Alexandras, P.; Evangelia, L.; Vassiliki, T.; Maria-Nektaria, N. Effect of ripening stage on the total phenolics content, lycopene and antioxidant activity of tomato fruits grown to a geothermal greenhouse. Biol. Hortic. Food Prod. Process. Technol. Environ. Eng. 2018, 23, 115–120. [Google Scholar]
  82. Setti, L.; Passarini, F.; De Gennaro, G.; Barbieri, P.; Perrone, M.G.; Borelli, M.; Miani, A. SARS-CoV-2 RNA found on particulate matter of Bergamo in Northern Italy: First evidence. Environ. Res. 2020, 188, 109754. [Google Scholar] [CrossRef] [PubMed]
  83. Gil-Pelegrín, E.; Peguero-Pina, J.J.; Sancho-Knapik, D. Oaks and people: A long journey together. In Oaks Physiological Ecology: Exploring the Functional Diversity of Genus Quercus L.; Springer: Cham, Switzerland, 2017; pp. 1–11. [Google Scholar]
  84. Akula, R.; Ravishankar, G.A. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal. Behav. 2011, 6, 1720–1731. [Google Scholar] [CrossRef]
  85. Pérez-Girón, J.C.; Díaz-Varela, E.R.; Álvarez-Álvarez, P. Climate-driven variations in productivity reveal adaptive strategies in Iberian cork oak agroforestry systems. For. Ecosyst. 2022, 9, 100008. [Google Scholar] [CrossRef]
  86. Das, S.; Barman, S.; Teron, R.; Bhattacharya, S.S.; Kim, K.H. Secondary metabolites and anti-microbial/anti-oxidant profiles in Ocimum spp.: Role of soil physico-chemical characteristics as eliciting factors. Environ. Res. 2020, 188, 109749. [Google Scholar] [CrossRef]
  87. Duarte, A.R.; Santos, S.C.; Seraphin, J.C.; Ferri, P.H. Influence of spatial, edaphic and genetic factors on phenols and essential oils of Myrciaria cauliflora fruits. J. Braz. Chem. Soc. 2012, 23, 737–746. [Google Scholar] [CrossRef]
  88. Chludil, H.D.; Corbino, G.B.; Leicach, S.R. Soil quality effects on Chenopodium album flavonoid content and antioxidant potential. J. Agric. Food Chem. 2008, 56, 5050–5056. [Google Scholar] [CrossRef]
  89. Nait-Kaci, M.B.; Hedde, M.; Bourbia, S.M.; Derridj, A. Hierarchization of factors driving soil macrofauna in North Algeria groves. BASE Biotechnol. Agron. Soc. Environ. 2014, 18, 11–18. [Google Scholar]
  90. Xu, Z.; Zhang, T.; Wang, S.; Wang, Z. Soil pH and C/N ratio determines spatial variations in soil microbial communities and enzymatic activities of the agricultural ecosystems in Northeast China: Jilin Province case. Appl. Soil Ecol. 2020, 155, 103629. [Google Scholar] [CrossRef]
  91. Roca-Fernández, A.I.; Dillard, S.L.; Soder, K.J. Ruminal fermentation and enteric methane production of legumes containing condensed tannins fed in continuous culture. J. Dairy Sci. 2020, 103, 7028–7038. [Google Scholar] [CrossRef]
  92. AL-Ghamdi, A.A.; Jais, H.M. Interaction between soil textural components, flavonoids in the roots and mycorrhizal colonization in Juniperus procera in Saudi Arabia. Afr. J. Microbiol. Res. 2013, 7, 996–1001. [Google Scholar]
  93. Vierheilig, H.; Bago, B.; Lerat, S.; Piché, Y. Shoot-produced, light-dependent factors are partially involved in the expression of the arbuscular mycorrhizal (AM) status of AM host and non-host plants. J. Plant Nutr. Soil Sci. 2002, 165, 21–25. [Google Scholar]
  94. Castells, E.; Peñuelas, J. Is there a feedback between N availability in siliceous and calcareous soils and Cistus albidus leaf chemical composition? Oecologia 2003, 136, 183–192. [Google Scholar] [CrossRef]
  95. Oliveira, J.S.D.; Ramos, N.P.; Júnior, J.L.; Xavier, L.P.; Andrade, E.H.; Mello, A.H.; Da Silva, J.K.R. Secondary metabolism and plant growth of Piper divaricatum (Piperaceae) inoculated with arbuscular mycorrhizal fungi and phosphorus supplementation. Agronomy 2022, 12, 596. [Google Scholar] [CrossRef]
  96. Akiyama, K.; Matsuoka, H.; Hayashi, H. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol. Plant-Microbe Interact. 2002, 15, 334–340. [Google Scholar] [CrossRef]
  97. Tomasi, N.; Weisskopf, L.; Renella, G.; Landi, L.; Pinton, R.; Varanini, Z.; Cesco, S. Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol. Biochem. 2008, 40, 1971–1974. [Google Scholar] [CrossRef]
  98. Watson, B.S.; Bedair, M.F.; Urbanczyk-Wochniak, E.; Huhman, D.V.; Yang, D.S.; Allen, S.N.; Sumner, L.W. Integrated metabolomics and transcriptomics reveal enhanced specialized metabolism in Medicago truncatula root border cells. Plant Physiol. 2015, 167, 1699–1716. [Google Scholar] [CrossRef]
  99. Malusà, E.; Russo, M.A.; Mozzetti, C.; Belligno, A. Modification of secondary metabolism and flavonoid biosynthesis under phosphate deficiency in bean roots. J. Plant Nutr. 2006, 29, 245–258. [Google Scholar] [CrossRef]
  100. Hawes, M.C.; Brigham, L.A.; Wen, F.; Woo, H.H.; Zhu, Y. Function of root border cells in plant health: Pioneers in the rhizosphere. Annu. Rev. Phytopathol. 1998, 36, 311–327. [Google Scholar]
  101. Zahedi, S.M.; Karimi, M.; Venditti, A. Plants adapted to arid areas: Specialized metabolites. Nat. Prod. Res. 2021, 35, 3314–3331. [Google Scholar]
  102. Bettaieb, I.; Zakhama, N.; Wannes, W.A.; Kchouk, M.E.; Marzouk, B. Water deficit effects on Salvia officinalis fatty acids and essential oils composition. Sci. Hortic. 2009, 120, 271–275. [Google Scholar] [CrossRef]
  103. Gobbo-Neto, L.; Lopes, N.P. Plantas medicinais: Fatores de influência no conteúdo de metabólitos secundários. Química Nova 2007, 30, 374–381. [Google Scholar] [CrossRef]
  104. Urban, L.; Berti, L.; Bourgaud, F.; Gautier, H.; Léchaudel, M.; Joas, J.; Sallanon, H. The effect of environmental factors on biosynthesis of carotenoids and polyphenolics in fruits and vegetables: A review and prospects. In II International Symposium on Human Health Effects of Fruits and Vegetables: FAVHEALTH 2007; ISHS: Leuven, Belgium, 2007; pp. 339–344. [Google Scholar]
  105. Caretto, S.; Linsalata, V.; Colella, G.; Mita, G.; Lattanzio, V. Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress. Int. J. Mol. Sci. 2015, 16, 26378–26394. [Google Scholar] [CrossRef]
  106. Brüggemann, W.; Bergmann, M.; Nierbauer, K.U.; Pflug, E.; Schmidt, C.; Weber, D. Photosynthesis studies on European evergreen and deciduous oaks grown under Central European climate conditions: II. Photoinhibitory and light-independent violaxanthin deepoxidation and downregulation of photosystem II in evergreen, winter-acclimated European Quercus taxa. Trees 2009, 23, 1091–1100. [Google Scholar]
  107. Korn, M.; Peterek, S.; Mock, H.P.; Heyer, A.G.; Hincha, D.K. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ. 2008, 31, 813–827. [Google Scholar] [CrossRef]
  108. Insam, H.; Seewald, M.S. Volatile organic compounds (VOCs) in soils. Biol. Fertil. Soils 2010, 46, 199–213. [Google Scholar] [CrossRef]
  109. Zhang, Y.; Li, Y.; Ren, X.; Zhang, X.; Wu, Z.; Liu, L. The positive correlation of antioxidant activity and prebiotic effect about oat phenolic compounds. Food Chem. 2023, 402, 134231. [Google Scholar] [CrossRef]
  110. Masante, T.; Cafà, S.; Di Iorio, A. Total polyphenol content and antioxidant activity of leaves and fine roots as indicators of drought resistance in the native Quercus robur and alien Quercus rubra. Forests 2024, 15, 1531. [Google Scholar] [CrossRef]
  111. Rebaya, A.; Belghith, S.I.; Baghdikian, B.; Leddet, V.M.; Mabrouki, F.; Olivier, E.; Ayadi, M.T. Total phenolic, total flavonoid, tannin content, and antioxidant capacity of Halimium halimifolium (Cistaceae). J. Appl. Pharm. Sci. 2015, 5, 052–057. [Google Scholar]
  112. Chen, X.X.; Wu, X.B.; Chai, W.M.; Feng, H.L.; Shi, Y.; Zhou, H.T.; Chen, Q.X. Optimization of extraction of phenolics from leaves of Ficus virens. J. Zhejiang Univ. Sci. B 2013, 14, 903–915. [Google Scholar] [CrossRef]
Forests 16 00906 g001
Figure 1. Location map of the study area (QGIS 3.10.10).
Figure 1. Location map of the study area (QGIS 3.10.10).
Forests 16 00906 g001
Forests 16 00906 g002
Figure 2. Total polyphenol content in the rhizospheric soil of cork oak (Q. suber) (D1RS: rhizospheric soil at 0–15 cm depth; D2RS: rhizospheric soil at 15–25 cm depth).
Figure 2. Total polyphenol content in the rhizospheric soil of cork oak (Q. suber) (D1RS: rhizospheric soil at 0–15 cm depth; D2RS: rhizospheric soil at 15–25 cm depth).
Forests 16 00906 g002
Forests 16 00906 g003
Figure 3. Total polyphenol, flavonoid, and tannin contents in roots of Q. suber (D1: root of 0–15 cm depth/D2: root of 15–25 cm depth/FLV: flavonoid/TPP: total polyphenol/TT: tannin).
Figure 3. Total polyphenol, flavonoid, and tannin contents in roots of Q. suber (D1: root of 0–15 cm depth/D2: root of 15–25 cm depth/FLV: flavonoid/TPP: total polyphenol/TT: tannin).
Forests 16 00906 g003
Forests 16 00906 g004
Figure 4. Flavonoid, total polyphenol, and tannin contents in leaves of Q. suber.
Figure 4. Flavonoid, total polyphenol, and tannin contents in leaves of Q. suber.
Forests 16 00906 g004
Forests 16 00906 g005
Figure 5. Distribution of flavonoid (FLV), total polyphenol (TPP), and tannin (TT) contents for leaves and root tissues of Q. suber. (a): winter season, (b): summer season.
Figure 5. Distribution of flavonoid (FLV), total polyphenol (TPP), and tannin (TT) contents for leaves and root tissues of Q. suber. (a): winter season, (b): summer season.
Forests 16 00906 g005
Forests 16 00906 g006
Figure 6. IC50 values from three antioxidant assays (DPPH, FRAP. TAC) for Q. suber roots (D1: 0–15 cm depth, D2: 15–25 cm depth), compared with ascorbic acid as a reference standard.
Figure 6. IC50 values from three antioxidant assays (DPPH, FRAP. TAC) for Q. suber roots (D1: 0–15 cm depth, D2: 15–25 cm depth), compared with ascorbic acid as a reference standard.
Forests 16 00906 g006
Forests 16 00906 g007
Figure 7. IC50 values from three antioxidant assays (DPPH, FRAP, TAC) for Q. suber leaves compared with ascorbic acid.
Figure 7. IC50 values from three antioxidant assays (DPPH, FRAP, TAC) for Q. suber leaves compared with ascorbic acid.
Forests 16 00906 g007
Forests 16 00906 g008
Figure 8. Principal component analysis (PCA) results displayed on the F1 × F2 plane: (a) projection of all measured variables, including secondary metabolites, antioxidant activities, and edaphic characteristics; (b) analysis of studied variables with consideration of influencing factors such as season and soil depth. This figure illustrates the distribution and relationships of various parameters, highlighting their contributions to the observed variance in the dataset. The axes represent the principal components, with F1 accounting for 70% of the total variance and F2 accounting for 23%, together explaining 93% of the variability in the measured parameters.
Figure 8. Principal component analysis (PCA) results displayed on the F1 × F2 plane: (a) projection of all measured variables, including secondary metabolites, antioxidant activities, and edaphic characteristics; (b) analysis of studied variables with consideration of influencing factors such as season and soil depth. This figure illustrates the distribution and relationships of various parameters, highlighting their contributions to the observed variance in the dataset. The axes represent the principal components, with F1 accounting for 70% of the total variance and F2 accounting for 23%, together explaining 93% of the variability in the measured parameters.
Forests 16 00906 g008
Table 1. Geographical coordinates of the study site.
Table 1. Geographical coordinates of the study site.
Station NameAltitude (m)LatitudeLongitudeSlope (°)Orientation
Ait Hammad800N36°47′24.8”E004°32′40.1”0NE
Table 2. Climatic data of the study site.
Table 2. Climatic data of the study site.
Station NameMean Temperature (°C)Precipitation (mm)
Winter (January)Summer (July)Winter (January)Summer (July)
Ait Hammad8.3725.3267.9814.66
Table 3. Physicochemical analysis results of rhizospheric soil samples.
Table 3. Physicochemical analysis results of rhizospheric soil samples.
SummerWinterp Value Soil Depth
Soil depth D1D2D1D2
pH-water5.27± 0.43 ab4.93± 0.41 a5.36± 0.31 b5.25 ± 0.14 ab0.043 *
EC (ds/m)0.92 ± 0.34 b0.33 ± 0.07 a2.58± 0.78 c0.7 ± 0.31 ab0.000 ***
C %7.02 ± 1.832.59 ± 0.512.87 ± 2.493.39 ± 0.930.000 ***
N %0.43 ± 0.50.17 ± 0.090.38 ± 0.120.22 ± 0.110.000 ***
C/N16.33 ± 2.43 a15.22 ± 6.02 a33.88 ± 15.89 b15.39 ± 5.58 a0.000 ***
P (g/Kg)1.73 × 10−4 ± 0.14 b1.66 × 10−4 ± 0.167 b0.4 × 10−4 ± 0.033 a0.44 × 10−4 ± 0.035 a0.009 **
Si %47.97 ± 14.61 a44.51 ± 14.73 a54.11 ± 18.4 a47.09 ± 12.81 a0.553
S %51.91 ± 4.62 a55.37 ± 14.73 a45.76 ± 18.41 a52.77 ± 12.85 a0.553
CL %0.12 ± 0.04 a0.12 ± 0.04 a0.13 ± 0.05 a0.14 ± 0.05 a0.734
D1: rhizospheric soil at 0–15 cm depth/D2: rhizospheric soil at 15–25 cm depth/pH-H2O: hydrogen potential of water/EC: Electrical Conductivity/C: organic carbon, N: total nitrogen, C/N: Carbon/Nitrogen/P: Phosphorus/Clay: CL/Sand: S/Silt: SI/. * statistically significant; ** very statistically significant; *** highly statistically significant; a–c are the three different statical groups abtained after anlysis.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hoceini-Bentaha, M.; Kadi-Bennane, S.; Boussoum, M.O.; Nabti, E.-H.; Kadir, N.; Mestar-Guechaoui, N.; Ibrahim, N.A.; Aleissa, M.S.; Basher, N.S.; Boudiaf, M.; et al. Seasonal and Edaphic Modulation Influences the Phenolic Contents and Antioxidant Activity in Cork Oak (Quercus suber L.): Evidence from the Algerian Mediterranean Forest. Forests 2025, 16, 906. https://doi.org/10.3390/f16060906

AMA Style

Hoceini-Bentaha M, Kadi-Bennane S, Boussoum MO, Nabti E-H, Kadir N, Mestar-Guechaoui N, Ibrahim NA, Aleissa MS, Basher NS, Boudiaf M, et al. Seasonal and Edaphic Modulation Influences the Phenolic Contents and Antioxidant Activity in Cork Oak (Quercus suber L.): Evidence from the Algerian Mediterranean Forest. Forests. 2025; 16(6):906. https://doi.org/10.3390/f16060906

Chicago/Turabian Style

Hoceini-Bentaha, Melia, Saliha Kadi-Bennane, Mohand Ouidir Boussoum, El-Hafid Nabti, Nassima Kadir, Nadjet Mestar-Guechaoui, Nasir A. Ibrahim, Mohammed Saad Aleissa, Nosiba S. Basher, Malika Boudiaf, and et al. 2025. "Seasonal and Edaphic Modulation Influences the Phenolic Contents and Antioxidant Activity in Cork Oak (Quercus suber L.): Evidence from the Algerian Mediterranean Forest" Forests 16, no. 6: 906. https://doi.org/10.3390/f16060906

APA Style

Hoceini-Bentaha, M., Kadi-Bennane, S., Boussoum, M. O., Nabti, E.-H., Kadir, N., Mestar-Guechaoui, N., Ibrahim, N. A., Aleissa, M. S., Basher, N. S., Boudiaf, M., Trabelsi, L., & Houali, K. (2025). Seasonal and Edaphic Modulation Influences the Phenolic Contents and Antioxidant Activity in Cork Oak (Quercus suber L.): Evidence from the Algerian Mediterranean Forest. Forests, 16(6), 906. https://doi.org/10.3390/f16060906

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop