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Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species

  • Shengfeng Chai , Haidu Jiang , Yishan Yang , Xinfeng Pan , Rong Zou , Jianmin Tang , Zongyou Chen , Danjuan Zeng EMAIL logo and Xiao Wei EMAIL logo
Published/Copyright: March 9, 2024

Abstract

We grew three yellow Camellia species (the calcifuge C. nitidissima and C. tunghinensis, and the calcicole C. pubipetala) in acidic and calcareous soils for 7 months and assessed their photosynthetic physiological characteristics, growth performance, and element concentrations in this developmental context. The calcifuge C. nitidissima and C. tunghinensis species exhibited poor growth with leaf chlorosis, growth stagnation, and root disintegration in calcareous soils, and with their P n, G s, T r, F v/F m, ΦPSII, ETR, qP, leaf Chla, Chlb, and Chl(a + b) concentrations, and root, stem, leaf, and total biomass being significantly lower when grown in calcareous soils relative to in acidic soils. In contrast, the calcicole C. pubipetala grew well in both acidic and calcareous soils, with few differences in the above parameters between these two soil substrates. The absorption and/or transportation of nutrient elements such as N, K, Ca, Mg, and Fe by the two calcifuge Camellia species plants grown in calcareous soils were restrained. Soil type plays a major role in the failure of the two calcifuge Camellia species to establish themselves in calcareous soils, whereas other factors such as competition and human activity are likely more important limiting factors in the reverse case. This study furthers our understanding of the factors influencing the distribution of these rare and endangered yellow Camellia species, allowing for improved management of these species in conservation projects and horticultural production.

1 Introduction

Edaphic properties are key environmental factors that affect species diversity, distribution, and plant nutrition [14]. Calcareous soils and acidic soils are both widely distributed at the global level and are associated with distinct soil properties that are linked to consequent differences in species diversity. Calcareous soils are rich in Ca and has a higher pH and HCO 3 levels; moreover, the availability of phosphorus (P), iron (Fe), manganese (Mn), and zinc (Zn) is very low due to higher pH in this soil type [57]. In contrast, acidic soils have lower Ca and pH levels and higher Al concentrations [8]. Ecologists have classified plant species into calcifuges, which grow in acidic soils with low Ca2+ concentrations, and calcicoles, which grow in calcareous substrates [9]. Calcicole plants can grow well in calcareous soils, and can acclimate to the high calcium environment through a series of morphological and/or physiological functional adjustments [10], such as the synthesis of calcium oxalate crystals and storage thereof in tissues and intercellular spaces [1113], the formation of calcified roots, depositing calcium [14], reducing root-mediated calcium absorption [15,16], increasing root organic acid secretion [17,18], or forming mycorrhizal associations that can promote the absorption of certain insoluble elements [1921]. In contrast, calcifuge plants are usually sensitive to high calcium environments, and they grow poorly in calcareous soils primarily because of Ca-associated toxicity [22,23] and/or element deficiencies [24,25]. Some studies of the adaptability and their mechanistic basis of calcicole and calcifuge plants to acidic and calcareous soils have been conducted, but these experiments have primarily focused on single species or on different families and genera, with few such studies of calcicole–calcifuge behaviors among different species in the same genus having been conducted [2628], especially for endangered plants.

Camellia, sect. Chrysantha Chang is an evergreen shrub or small tree in the Theaceae family that is renowned for its yellow camellia flowers, representing a rare ornamental plant group and germplasm resource of value for the breeding of new hybrid camellia varieties [29]. These plants primarily grow in Guangxi Province, South China and North Vietnam in tropical limestone evergreen broad-leaved forests, limestone mountain seasonal rainforests, and subtropical evergreen broad-leaved forests [30]. Plants in this group are most common in mountain valleys, alongside streams, and on limestone slopes from 120 to 350 m above sea level [31], and most have a narrow distribution and are listed in the list of rare and endangered plants in China. To date, 16 species that grow best in calcareous soils in limestone mountain regions have been described, while seven species that grow most readily in acidic soils in sandstone and shale mountains have been identified [32,33]. Under natural conditions, there have been no reports of the same species growing in both of these soil types [30]. Camellia, sect. Chrysantha Chang species can be separated into calcicole and calcifuge categories based upon their calcium dependence and whether they grow most readily in acidic or calcareous soils, respectively. These contrasting soil type preferences within the same genus are interesting but are not well understood.

Most calcicole yellow Camellia species can grow in acidic soils [34], but the adaptability of calcifuge Camellia species to calcareous soils remains unclear. The objectives of this study were to compare the performance of these three yellow Camellia species in these two soil types. We hypothesized that (1) the calcifuge yellow Camellia species would grow poorly and exhibit lower chlorophyll content and photosynthetic capacity in calcareous soils owing to an inability to acclimate to such soils owing to Ca-associated toxicity and/or element deficiencies and (2) the growth performance, chlorophyll content, and photosynthetic capacity of calcicole Camellia species in calcareous soils would be better or similar to those observed in acidic soils.

2 Materials and methods

2.1 Study site

The experiment was carried out in Guilin Botanical Garden, Yanshan District, Guilin City, Guangxi Province, China in 2018. This site is located at 25°11.2′N, 110°12.0′E at an altitude of 175 m in a subtropical monsoon climate zone with an average annual temperature of 19.2°C, average temperatures during the hottest and coldest months are 28.4 and 7.7°C, respectively, and with temperature extremes of 39 and –2°C. The average annual rainfall at this study site is 1854.8 mm, with most rain (73%) falling between April and August. On average, this site receives 1,680 h of sunshine per year, and the annual average relative humidity is 82%. Relative to the climate conditions experienced by the three species in their natural environments, the experimental site was to the north and the temperature was lower in the winter, but the three plants were still able to grow normally in acidic soil.

2.2 Treatments

Two calcifuge species (Camellia nitidissima and Camellia tunghinensis) and one calcicole species (Camellia pubipetala) were used in this experiment. The C. nitidissima plants used in this study were 1-year-old seedlings propagated from seeds collected from wild populations in Golden Camellia National Nature Reserve, Fangcheng, Guangxi (21°45.0′N, 108°5.9′E). This Reserve belongs to the north tropical monsoon climate, with an average annual temperature of 21.9°C, average temperature of the coldest month (January) is 12.6°C, extreme low temperature of −0.9°C, average temperature of the hottest month (July) is 28.3°C, and extreme high temperature of 39.1°C. The average sunshine hours per year is 1,525 h and the average annual rainfall is more than 2,500 mm. The C. tunghinensis plants used in this study were 2-year-old grafted seedlings propagated from the branches of wild plants in Golden Camellia National Nature Reserve. The C. pubipetala plants were 2-year-old grafted seedlings propagated from the branches of wild plants in Pingshan town, Long’an County, Guangxi (23°0.1′N, 107°34.8′E). This site has a subtropical monsoon climate, with hot summer and warm winter, abundant rainfall and comparatively high relative humidity. The average temperatures are 21.8°C as the annual mean, 13.2°C in January (the coldest month), and 33.2°C in July (the hottest month). Most of the rainfall is observed in the summer and autumn, with an annual mean of 1,500 mm. The original soils in which the two calcifuge species grown were acidic with low levels of calcium, while those of calcicole species were neutral or weakly alkaline with a high calcium content [35]. Before the experiment, the seedlings of these three species were planted in plastic bags containing loess and peat soil, with a volume ratio of 2:1, and all these seedlings are growing well.

Acidic and calcareous soils were used for this study. Acidic soils were collected from Guilin Botanical Garden. These were acidic, sticky, yellow soils with low levels of organic matter that were formed via the weathering of sandy shale, and were collected at a depth of 0–20 cm. The calcareous soils were collected from the crevices of karst hills in Gongcheng County, Guilin City, Guangxi Province at a collection depth of 0–20 cm. Plant residues and stones were removed after collection, and large pieces of soils were crushed and screened prior to use. Relative to the acidic soils, the calcareous soils exhibited a nearly neutral pH, higher levels of organic matter, total N, available Ca, and available Mg, and lower levels of available P (Table 1).

Table 1

Nutrient status of the soils used in this study

Soil type pH value Organic matter (%) Total N (g/kg) Total P (g/kg) Total K (g/kg) Available Ca (cmol(1/2Ca2+)/kg) Available Mg (cmol(1/2Mg2+)/kg)
Acidic soils 5.34 1.26 1.53 1.09 14.11 2.05 0.18
Calcareous soils 7.07 14.29 14.63 2.05 11.12 21.60 2.34

In early April 2018, healthy plants with comparable levels of growth were selected to conduct pot-based experiments using acidic and calcareous soils as substrates. The roots of members of these three yellow Camellia species were washed and planted in plastic pots with an inner diameter of 30 cm and a depth of 25 cm. One plant was planted per pot, with 20 plants per experimental treatment. These three yellow Camellia species are shade-adapted plants, C. nitidissima and C. pubipetala grow best under 10% sunlight (among 10, 30, 50, and 100% of full sunlight) [36,37], and the light transmittance under forest canopy in the original habitat of these three species are less than 25% [38]. Therefore, in this experiment, we placed the potted plants in a shade shed with a relative light intensity of 10%. Regular weeding and pest control were conducted, but no fertilizer was applied during the experimental period to compare the effects of different soil types on seedling growth.

2.3 Sample collection and analysis

In early November 2018, the third to fifth mature functional leaves from the top of experimental plants were assessed to measure gas exchange parameters, chlorophyll fluorescence, and photosynthetic pigments. The biomass of the plants and the root and leaf nutrient concentrations therein were also measured.

2.3.1 Determination of gas exchange parameters

The net photosynthetic rate (P n, μmol m−2 s−1), transpiration rate (T r, mol m−2 s−1), stomatal conductance (G s, mmol m−2 s−1), and intercellular CO2 concentration (C i, μmol mol−1) were assessed with a Li-6400 portable photosynthesis analyzer system (LI-COR, NE, USA). Measurements were made from 9:00 to 11:00 on sunny days. The photosynthetically active radiation was set at 300 μmol m−2 s−1. The maximum photon flux density experienced on a sunny day is about 2,000–2,500 μmol m−2 s−1 at the experimental site and it shall not exceed 300 μmol m−2 s−1 in the shade net. These three yellow Camellia species are shade-adapted plants, and the light saturation point of them are all less than 500 μmol m−2 s−1 [38,39]. Therefore, we chose 300 μmol m−2 s−1 as the measured light intensity for this study. The temperature of the control chamber was (28 ± 1)°C, the CO2 concentration in the sample chamber was (400 ± 5) mmol mol−1, the mean relative humidity was 53 ± 2%, and the flow rate was set at 500 µmol s–1.

2.3.2 Chlorophyll fluorescence analyses

Chlorophyll fluorescence parameters of leaves were assessed with a Mini-Imaging-PAM modulation chlorophyll fluorescence imaging system (Walz Company, Germany) after 20 min of dark adaptation in the morning. The initial fluorescence (F o) was analyzed using a measuring light (0.1 μmol m−2 s−1), and then the maximum fluorescence (F m) was generated via excitation with a saturated 6,000 μmol m−2 s−1 light pulse (pulse time: 0.8 s). The minimum fluorescence ( F o ), maximum fluorescence ( F m ), and stable fluorescence (F s) of leaves under light adaptation were measured using a fluorescence kinetic curve induced by actinic light (55 μmol m−2 s−1), and the maximum photochemical efficiency (F v/F m), actual photochemical efficiency (ΦPSII), photosynthetic electron transfer rate (ETR), photochemical quenching (qP), and non-photochemical quenching (NPQ) were calculated with the Wincontrol-3 software [40].

2.3.3 Determination of photosynthetic pigments

Leaf chlorophyll (Chl) and carotenoid (Car) contents were determined as per the methods of Lichtenthaler [41]. These pigments were extracted with 95% ethanol, and the absorbance of extracted liquids was recorded with a spectrophotometer (TU1901, Beijing Purkinje General Instrument Co., Ltd, China) at 665 and 649 nm for Chl, and at 470 nm for Car. The following formulae were then used to calculate pigment concentrations: Chla = 13.95 A 665−6.88 A 649, Chlb = 24.96 A 649−7.32 A 665, Car = (1,000 A 470−2.05 Chla−114.8 Chlb)/245, as well as the ratios of Chla/b and Car/Chl.

2.3.4 Biomass measurement

After 7 months of in-pot growth during the experimental period, whole plants were harvested and taken back to the laboratory for washing and drying. Plants were dried at 80°C to a constant weight in an oven, after which the stem, root, and leaf weights were determined with an electronic balance, and the biomass of each of these tissue types was calculated, as was total biomass.

2.3.5 Nutrient element measurement

After biomass measurements were completed, root and leaf samples were ground and homogenized. The N, P, K, Ca, Mg, Fe, and Mn concentrations in these roots and leaves were then quantified. N concentrations were measured using the Kjeldahl method, with samples being digested using K2SO4:CuSO4·5H2O:Se (10:1:0.1) and H2SO4 [42]. Other nutrient (P, K, Ca, Mg, Fe, and Mn) levels were assessed by digesting samples using concentrated HNO3 [43], and were then analyzed using an inductively coupled plasma emission spectrum (iCAP Qc, Thermo Fisher Scientific, Bremen, Germany).

2.3.6 Data processing

For the same species grown in different substrates, t-tests were used to assess the effects of soil type on gas exchange parameters, chlorophyll fluorescence, photosynthetic pigment content, biomass, and leaf/root nutrient element concentrations. SPSS 20.0 (SPSS Inc., IL, USA) was used for all statistical testing. Sigmaplot 12.5 was used to plot the resultant data (Systat Software, CA, USA).

3 Results

3.1 Gas exchange parameters

Relative to plants grown in acidic soils, the P n, G s, and T r of the two calcifuge Camellia species grown in calcareous soils were significantly decreased (P < 0.01), while C i was significantly increased (P < 0.05). The P n, G s, and T r of C. nitidissima plants grown in calcareous soils were 9.51, 26.47, and 23.40% of those for plants grown in acidic soils, respectively, while for C. tunghinensis these respective values were 7.76, 9.84, and 8.70% (Table 2). The C i of these two plants was 1.46 and 1.24 times higher, respectively, relative to corresponding plants grown in acidic soils. The P n of calcicole C. pubipetala in calcareous soils was significantly higher than that in acidic soils (P < 0.05), while there was no significant difference in G s, T r, or C i between the plants grown in these two soil types (P > 0.05) (Table 2).

Table 2

Photosynthetic gas exchange parameters of three yellow Camellia species grown in different soil types

Species Soil type P n (μmol m−2 s−1) G s (mol m−2 s−1) T r (mmol m−2 s−1) C i (μmol mol−1)
C. nitidissima Acidic soils 2.84 ± 0.61 0.034 ± 0.011 0.94 ± 0.24 245.08 ± 20.27
Calcareous soils 0.27 ± 0.12 0.009 ± 0.001 0.22 ± 0.02 356.96 ± 17.22
** ** ** *
C. tunghinensis Acidic soils 4.64 ± 0.49 0.061 ± 0.011 1.61 ± 0.31 259.33 ± 10.28
Calcareous soils 0.36 ± 0.29 0.006 ± 0.002 0.14 ± 0.06 321.40 ± 36.30
** ** ** *
C. pubipetala Acidic soils 3.09 ± 0.45 0.054 ± 0.011 1.01 ± 0.357 297.39 ± 7.37
Calcareous soils 3.66 ± 0.47 0.055 ± 0.010 0.95 ± 0.20 281.04 ± 18.19
* ns ns ns

Data are mean ± SD (n = 6). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant.

3.2 Chlorophyll fluorescence

Relative to those of plants grown in acidic soils, the F v/F m, ΦPSII, ETR, and qP of the two calcifuge Camellia species grown in calcareous soils were significantly decreased (P < 0.05), while NPQ were significantly increased (P < 0.01) (Table 3). The chlorophyll fluorescence parameters of the calcicole C. pubipetala did not exhibit any significant differences between acidic and calcareous soils (P > 0.05).

Table 3

Chlorophyll fluorescence parameters for three yellow Camellia species grown in different soil substrates

Species Soil type F v/F m ΦPSII ETR qP NPQ
C. nitidissima Acidic soils 0.79 ± 0.01 0.63 ± 0.04 14.53 ± 0.88 0.88 ± 0.04 0.52 ± 0.13
Calcareous soils 0.72 ± 0.03 0.39 ± 0.08 8.50 ± 1.71 0.75 ± 0.14 2.21 ± 0.45
* * * * **
C. tunghinensis Acidic soils 0.79 ± 0.01 0.65 ± 0.03 15.06 ± 0.80 0.91 ± 0.02 0.47 ± 0.16
Calcareous soils 0.69 ± 0.03 0.42 ± 0.05 9.78 ± 1.12 0.87 ± 0.01 1.54 ± 0.25
* * * * **
C. pubipetala Acidic soils 0.79 ± 0.01 0.60 ± 0.02 13.86 ± 0.53 0.86 ± 0.03 0.62 ± 0.10
Calcareous soils 0.80 ± 0.01 0.59 ± 0.06 15.85 ± 4.11 0.83 ± 0.06 0.63 ± 0.19
ns ns ns ns ns

Data are mean ± SD (n = 6). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant.

3.3 Photosynthetic pigment contents and ratios

The Chla, Chlb, Chl(a + b), and Car contents of the two calcifuge Camellia species grown in calcareous soils were significantly lower than those of plants grown in acidic soils (P < 0.05 or 0.01), while the Chla/b and Car/Chl values were significantly higher than those in acidic soils (P < 0.05) (Table 4). There was no significant difference in these parameters when comparing calcicole C. pubipetala plants grown in acidic and calcareous soils (P > 0.05).

Table 4

Photosynthetic pigment contents and ratios in the leaves of three yellow Camellia species grown in different soil substrates

Species Soil type Chla (mg g−1 FW) Chlb (mg g−1 FW) Chl(a + b) (mg g−1 FW) Car (mg g−1 FW) Cha/b Car/Chl
C. nitidissima Acidic soils 1.66 ± 0.08 0.66 ± 0.03 2.32 ± 0.10 0.26 ± 0.05 2.50 ± 0.14 0.11 ± 0.02
Calcareous soils 0.87 ± 0.09 0.39 ± 0.05 1.26 ± 0.10 0.22 ± 0.03 3.27 ± 0.31 0.18 ± 0.02
** ** ** * * *
C. tunghinensis Acidic soils 2.09 ± 0.25 0.53 ± 0.06 2.62 ± 0.35 0.55 ± 0.08 3.92 ± 0.13 0.21 ± 0.01
Calcareous soils 1.17 ± 0.08 0.25 ± 0.03 1.42 ± 0.10 0.36 ± 0.02 4.67 ± 0.51 0.25 ± 0.03
** ** ** * * *
C. pubipetala Acidic soils 1.92 ± 0.11 0.81 ± 0.05 2.83 ± 0.16 0.33 ± 0.02 2.38 ± 0.02 0.12 ± 0.01
Calcareous soils 1.85 ± 0.10 0.78 ± 0.05 2.63 ± 0.15 0.30 ± 0.01 2.39 ± 0.03 0.11 ± 0.01
ns ns ns ns ns ns

Data are mean ± SD (n = 4). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant.

3.4 Plant appearance and biomass

Almost no growth was observed for either of these two calcifuge Camellia species in calcareous soils, and they exhibited leaf chlorosis, some of the leaves wilting and loss, root disintegration. The calcicole C. pubipetala plants grew well in both soils (Figure 1). The root biomass, stem biomass, leaf biomass, and total biomass of the two calcifuge Camellia species grown in calcareous soils were significantly lower than those of plants grown in acidic soils (P < 0.01) (Table 5). The root, stem, leaf and total biomass of C. nitidissima grown in calcareous soils were 40.85, 51.81, 33.23, and 40.10% of those grown in acidic soils, respectively, while for C. tunghinensis these respective values were 38.79, 55.65, 36.84, and 43.61% (Table 5). The root and stem biomass of the calcicole C. pubipetala grown in calcareous soils were similar to those of plants grown in acidic soils, and the leaf biomass and total biomass of these plants were higher than those grown in acidic soils, although the difference was not significant (P > 0.05).

Figure 1 
                  Growth performance of three yellow Camellia species grown in different soil substrates: (a, d) C. nitidissima, (b, e) C. tunghinensis, (c, f) C. pubipetala. The plants grown in acidic and calcareous soils are shown on the left and right, respectively.
Figure 1

Growth performance of three yellow Camellia species grown in different soil substrates: (a, d) C. nitidissima, (b, e) C. tunghinensis, (c, f) C. pubipetala. The plants grown in acidic and calcareous soils are shown on the left and right, respectively.

Table 5

Biomass of three yellow Camellia species grown in different soil substrates

Species Soil type Root biomass (g) Stem biomass (g) Leaf biomass (g) Total biomass(g)
C. nitidissima Acidic soils 1.42 ± 0.15 1.66 ± 0.17 3.19 ± 0.36 6.26 ± 0.34
Calcareous soils 0.58 ± 0.10 0.86 ± 0.18 1.06 ± 0.17 2.51 ± 0.28
** ** ** **
C. tunghinensis Acidic soils 2.32 ± 0.28 2.39 ± 0.29 2.66 ± 0.20 7.36 ± 0.38
Calcareous soils 0.90 ± 0.18 1.33 ± 0.14 0.98 ± 0.10 3.21 ± 0.28
** ** ** **
C. pubipetala Acidic soils 2.61 ± 0.44 2.31 ± 0.09 2.15 ± 0.30 7.07 ± 0.62
Calcareous soils 2.78 ± 0.34 2.32 ± 0.18 2.63 ± 0.25 7.74 ± 0.70
ns ns ns ns

Data are mean ± SD (n = 4). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant.

3.5 Element concentrations

The leaf N concentrations of the two calcifuge Camellia species grown in calcareous soils were significantly lower than those of plants grown in acidic soils (P < 0.05), while the root N concentrations were significantly higher than those of plants grown in acidic soils (P < 0.01). The leaf and root N concentrations of the calcicole C. pubipetala plants grown in calcareous soils were higher than those of plants grown in acidic soils (Figure 2a) (P < 0.05 or 0.01). Aside from the root P concentrations in C. nitidissima, which were significantly higher for plants grown in calcareous soils relative to plants grown in acidic soils, there were no significant differences in leaf or root P concentrations for these three yellow Camellias species grown in different soil substrates (Figure 2b) (P > 0.05). Leaf and root K concentrations for three yellow Camellia species grown in calcareous soils were lower than those of plants grown in acidic soils (Figure 2c).

Figure 2 
                  Leaf and root nutrient concentrations of three yellow Camellia species grown in different soil substrates. Data are mean ± SD (n = 3). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant. ▲ denotes calcifuge species, ● denotes calcicole species.
Figure 2

Leaf and root nutrient concentrations of three yellow Camellia species grown in different soil substrates. Data are mean ± SD (n = 3). Significance (t-test): *P < 0.05, **P < 0.01; ns: not significant. ▲ denotes calcifuge species, ● denotes calcicole species.

The leaf Ca concentrations of the calcifuge Camellia plants grown in calcareous soils were significantly lower than those of plants grown in acidic soils (P < 0.05), while root Ca concentrations were significantly higher relative to those in acidic soils (P < 0.05 or 0.01) (Figure 2d). The leaf Ca concentrations of the calcicole C. pubipetala were significantly higher in calcareous soils relative to acidic soils, whereas the opposite was true for root Ca concentrations (P < 0.05).

Leaf Mg concentrations were significantly lower in calcifuge Camellia plants grown in calcareous soils relative to plants grown in acidic soils (P < 0.05), whereas there were no significant differences in root Mg concentrations between these two soil types (P > 0.05) (Figure 2e). The root and leaf Mg concentrations of the calcicole C. pubipetala in calcareous soils were significantly higher than those in acidic soils (P < 0.05 or 0.01).

Leaf Fe concentrations of the calcifuge C. nitidissima were significantly higher following growth in calcareous soils relative to acidic soils (P < 0.05), whereas no such differences were observed for calcifuge C. tunghinensis plants (P > 0.05) (Figure 2f). Root Fe concentrations in these two calcifuge Camellia species were significantly lower following growth in calcareous soils relative to acidic soils (P < 0.05). Leaf Fe concentrations in calcicole C. pubipetala plants were significantly lower following growth in calcareous soils relative to acidic soils, whereas the opposite was observed in the roots of these plants (P < 0.05).

With the exception of C. nitidissima, which exhibited no difference in leaf Mn concentrations when grown in these two soil types, the leaf and root Mn concentrations in these three yellow Camellia species were significantly lower following growth in calcareous soils relative to acidic soils (P < 0.05) (Figure S1).

4 Discussion

Calcifuge plants usually grow poorly in calcareous soils due to Ca-associated toxicity and/or element deficiencies, which primarily manifest in the form of leaf chlorosis or necrosis, decreased chlorophyll content, and reductions in photosynthetic capacity and biomass [27,28,44,45]. In contrast, calcicole plants are usually insensitive to soil calcium content, and most grow normally in both acidic and calcareous soils [44,46]. This study was the first to focus on the calcicole–calcifuge behaviors of Camellia species, and attempts to elucidate the endangered mechanism of yellow Camellia species from the perspective of soil factors. In this study, when grown in calcareous soils the two calcifuge Camellia species showed reduced photosynthetic capacity, growth stagnation, root disintegration, nutrient deficiency, and negative impacts on physiology, while the calcicole C. pubipetala plants can grow well, and allocate more Ca to their leaves compared with calcifuges. The results of this study are partly similar to those of previous studies, but can also provide some new insight into the mechanism driving these patterns of growth.

In this experiment, the P n, G s, and T r of the two calcifuge Camellia species were significantly lower when grown in calcareous soils relative to acidic soils, and their P n values were less than 10% of the values observed following growth in acidic soils. This indicates that these two calcifuge Camellia species were under severe stress in calcareous soils, consistent with their leaf chlorosis and growth stagnation. The decrease in P n was accompanied by an increase in C i, indicating that the former was mainly caused by non-stomatal factors [47], such as impaired carboxylation ability or decreased chlorophyll content in mesophyll cells [48]. This was consistent with the significant decrease of chlorophyll fluorescence parameters ETR, ΦPSII, qP, and chlorophyll content of the calcifuge Camellia species grown in calcareous soils, and these manifestations may be related to element deficiencies and Ca-associated toxicity. There was little difference in photosynthetic capacity, chlorophyll fluorescence parameters, and chlorophyll content of the calcicole C. pubipetala plants when grown in these two soil types, suggesting that C. pubipetala was readily able to acclimate to both of these soil substrates.

Under normal physiological conditions, the F v/F m values of the vast majority of C3 plants are in the 0.8–0.84 range [49]. If this value is greatly reduced, it indicates that the plant is subject to environmental stress [50]. In this experiment, the F v/F m values of the two calcifuge Camellia species grown in calcareous soils were 0.72 and 0.69, respectively, which may be attribute to the down regulation of photosynthetic function, although the damage of photosynthetic structure cannot be ruled out. Changes in the Chla/b ratio are related to the balance of light absorption capacity of photosystems [51]. The Car/Chl ratio reflects the relationship between light absorption and protection against light damage protection in plants [52]. In this experiment, the higher Chla/b and Car/Chl ratios of the two calcifuge Camellia species grown in calcareous soils were able to reduce the absorption of light energy by increasing heat dissipation, and this may represent a protective mechanism whereby plants can cope with stress conditions.

Plant biomass accumulation is an indicator of net carbon gain. Calcifuge species generally grow poorly and exhibit lower biomass in calcareous soils relative to acidic soils, while calcicole species present with lower biomass in acidic soils than in calcareous soils [28], or with no significant difference between these two soil types [44,53]. In this experiment, the root biomass, stem biomass, leaf biomass, and total biomass of calcifuge plants grown in calcareous soils were significantly less than those of plants grown in acidic soils, especially for roots, calcifuge plants grown in calcareous soils had almost no fibrous roots. In contrast, no significant difference in biomass was observed when calcicole C. pubipetala plants were grown in acidic or calcareous soils. This suggests that soil type plays a major role in the failure of the two calcifuge Camellia species to establish themselves in calcareous soils, whereas other factors such as competition and human activity are likely more important limiting factors in the reverse case [44,54]. The low fruit and seed set of C. pubipetala cultivated in acidic soils (personal data) should make it weak in community competition, which may be an important factor for limiting the distribution of this species in acidic soils. Although there are soil hills in acidic soils near the native population sites of C. pubipetala, the habitat suitable for the growth of this species has been destroyed by human activities, which may be another reason for excluding this species from acidic soils.

In calcareous soils, phosphate availability in plants is reduced owing to the fact that high pH values and Ca2+ concentrations can result in Ca phosphate precipitation and apatite formation [55]. P deficiency is known to impair calcifuge plant growth in calcareous soils [5658], and such impairment is believed to be related to the reduced ability of these plants to solubilize phosphate relative to calcicole species [14,59,60]. In this experiment, there were no significant differences in leaf P concentrations between the two calcifuge Camellia species grown in different soil substrates, and the root P concentration of C. nitidissima in calcareous soils was even higher than that in acidic soils, this result is not consistent with the significant decrease of P concentrations in leaves of some calcifuge plants grown in calcareous soils [57], indicating that P deficiency may not be the reason for the inability of these two calcifuge Camellia species to grow in calcareous soils.

High pH values and HCO 3 concentrations cause Fe deficiency chlorosis in plants grown in calcareous soils [61], both by reducing soil Fe solubility and by inhibiting Fe uptake, metabolism, and translocation [6264]. Therefore, synthetic and natural chelators are widely used in cropping systems to improve iron and other micro-nutrients in plants [65]. Although the leaf Fe concentrations in the two calcifuge plants were not significantly lower when grown in calcareous soils than when grown in acidic soils, the change of biologically available Fe concentration in leaves was not clear, so whether there was Fe deficiency in calcifuge Camellia plants grown in calcareous soils still needs further verification.

Calcium toxicity is one of the major causes of calcifuge plant sensitivity to calcareous soils [6668]. High Ca levels may disturb the lamellar structure of chloroplasts and consequently decrease net photosynthetic rates, and high Ca availability in the rhizosphere can also reduce cell wall extensibility, leaf expansion rate, and root elongation [6971]. Excessive Ca may precipitate with P as Ca3(PO4)2 in plant tissues, thereby rendering both Ca and P unavailable [7274]. In this experiment, the significantly elevated root Ca concentrations and decreased leaf Ca concentrations of the two calcifuge Camellia species grown in calcareous soils relative to acidic soils, combined with significantly reduced root biomass and root disintegration, indicating that the roots, rather than the leaves, of these two calcifuge Camellia species grown in calcareous soils may suffer toxic effects of exposure to high calcium levels. This was partially confirmed by another experiment. Under high calcium treatment, the photosynthetic capacity, chlorophyll fluorescence parameters ΦPSII, ETR, and chlorophyll content of the two calcifuge Camellia species decreased significantly [75]. This result is in contrast to findings in some calcifuge plants grown in high calcium environments, which exhibit higher root and leaf calcium concentrations [27,28,67]. Calcicole species tend to exhibit tight control over Ca uptake and/or translocation from roots to leaves, or to achieve better Ca compartmentation at the cellular level [73], these abilities likely play an important role in the tolerance of some calcicole species to calcareous soils [7678]. The leaf Ca concentrations of calcicole C. pubipetala plants grown in calcareous soils were significantly higher than those of plants grown in acidic soils, and they were also much higher than those of the calcifuge species grown in calcareous soils, indicating that this species exhibits a strong leaf Ca absorption and storage capacity when grown in high calcium environment [79]. This high Ca tolerance is most likely achieved through the biomineralization of excess Ca, leading to the formation of Ca-based minerals (presumably Ca oxalate), thereby avoiding any Ca2+ interference with cell functioning or with the availability/allocation of other nutrients [80,81]. The results indicated that the calcicole C. pubipetala is a high-Ca species [82].

The leaf N, Mg, and K concentrations of the two calcifuge Camellia species in calcareous soils were significantly lower than those in acidic soils, which may be attributable to the metabolic imbalance caused by the damage root.

5 Conclusions

The calcifuge C. nitidissima and C. tunghinensis plants exhibited poor growth in calcareous soils with leaf chlorosis, growth stagnation, and root disintegration. The P n, G s, T r, F v/F m, ΦPSII, ETR, qP, leaf Chl a, Chl b, and Chl(a + b) concentrations, as well as the root, stem, leaf, and total biomass of these two calcifuge Camellia species were significantly reduced when grown in calcareous soils relative to when grown in acidic soils. The absorption and/or transportation of the nutrient elements such as N, K, Ca, Mg, and Fe by the two calcifuge Camellia species plants grown in calcareous soils were restrained probably attributable to the damaged root. In contrast, the calcicole C. pubipetala grew well in both acidic and calcareous soils, with few differences in the photosynthetic parameters and growth performance between these two soil substrates. Soil type plays a major role in the failure of the two calcifuge Camellia species to establish themselves in calcareous soils, whereas other factors such as competition and human activity are likely more important limiting factors in the reverse case. This is the first study to demonstrate how calcareous soils impact yellow Camellia species, thus helping to explain why some yellow Camellia species are excluded from calcareous habitats. This study furthers our understanding of the factors influencing the distribution of these rare and endangered yellow Camellia species, allowing for improved management of these species in conservation projects and horticultural production.

  1. Funding information: This work was supported by the National Natural Science Foundation of China (32060248, 32160091), the key research and development program of Guangxi (GuikeAB21196018), the key research and development project of Guangxi (GuikeAB22080097).

  2. Author contributions: D.J.Z. and X.W. designed the study, S.F.C. performed the experiment and drafted the manuscript, H.D.J., Y.S.Y., X.Y.P., R.Z., J.M.T., and Z.Y.C. helped in conducting the experiment. All authors have read and approved the final manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

[1] Vélez-Bermúdez IC, Schmidt W. Plant strategies to mine iron from alkaline substrates. Plant Soil. 2022;483:1–25.10.1007/s11104-022-05746-1Search in Google Scholar

[2] Poschenrieder C, Gunsé B, Corrales I, Barceló J. A glance into aluminum toxicity and resistance in plants. Sci Total Environ. 2008;400(1–3):356–68.10.1016/j.scitotenv.2008.06.003Search in Google Scholar PubMed

[3] Guilherme Pereira C, Clode PL, Oliveira RS, Lambers H. Eudicots from severely phosphorus-impoverished environments preferentially allocate phosphorus to their mesophyll. N Phytol. 2018;218(3):959–73.10.1111/nph.15043Search in Google Scholar PubMed

[4] Cross AT, Lambers H. Calcicole–calcifuge plant strategies limit restoration potential in a regional semi-arid flora. Ecol Evol. 2021;11(11):6941–61.10.1002/ece3.7544Search in Google Scholar PubMed PubMed Central

[5] Tyler G. Some ecophysiological and historical approaches to species richness and calcicole/calcifuge behavior–contribution to a debate. Folia Geobot. 2003;38:419–28.10.1007/BF02803249Search in Google Scholar

[6] Souri MK, Hatamian M. Aminochelates in plant nutrition; a review. J Plant Nutr. 2019;42(1):67–78.10.1080/01904167.2018.1549671Search in Google Scholar

[7] Souri MK, Naiji M, Aslani M. Effect of Fe-glycine aminochelate on pod quality and iron concentrations of bean (Phaseolus vulgaris L.) under lime soil conditions. Commun Soil Sci Plan. 2018;49(2):215–24.10.1080/00103624.2017.1421655Search in Google Scholar

[8] Kochian LV, Piñeros MA, Liu J, Magalhaes JV. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol. 2015;66:571–98.10.1146/annurev-arplant-043014-114822Search in Google Scholar PubMed

[9] White PJ, Broadley MR. Calcium in plants. Ann Bot. 2003;92:487–511.10.1093/aob/mcg164Search in Google Scholar PubMed PubMed Central

[10] Lux A, Kohanová J, White PJ. The secrets of calcicole species revealed. J Exp Bot. 2021;72:968–70.10.1093/jxb/eraa555Search in Google Scholar PubMed PubMed Central

[11] Webb MA. Cell-mediated crystallization of calcium oxalate in plants. Plant Cell. 1999;11(4):751–60.10.2307/3870897Search in Google Scholar

[12] Franceschi VR, Nakat PA. Calcium oxalate in plants: formation and function. Annu Rev Plant Biol. 2005;56:41–71.10.1146/annurev.arplant.56.032604.144106Search in Google Scholar PubMed

[13] Gao J, Wang F, Ranathunge K, Arruda AJ, Cawthray GR, Clode PL, et al. Edaphic niche characterization of four Proteaceae reveals unique calcicole physiology linked to hyper-endemism of Grevillea thelemanniana. N Phytol. 2020;228(3):869–83.10.1111/nph.16833Search in Google Scholar PubMed

[14] Musetti R, Favalim A. Cytochemical localization of calcium and X-ray microanalysis of Catharanthus roseus L. infected with phytoplasmas. Micron. 2003;34(8):387–93.10.1016/S0968-4328(03)00082-9Search in Google Scholar PubMed

[15] Mcconnaughey TA, Whelan JF. Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev. 1997;42(1–2):95–117.10.1016/S0012-8252(96)00036-0Search in Google Scholar

[16] Kotula L, Clode PL, Ranathunge K, Lambers H. Role of roots in adaptation of soil-indifferent Proteaceae to calcareous soils in south-western Australia. J Exp Bot. 2021;72(4):1490–505.10.1093/jxb/eraa515Search in Google Scholar PubMed

[17] Tyler G, Ström L. Differing organic acid exudation pattern explains calcifuge and acidifuge behaviour of plants. Ann Bot. 1995;75(1):75–8.10.1016/S0305-7364(05)80011-3Search in Google Scholar PubMed PubMed Central

[18] Ohta T, Hiura T. Root exudation of low-molecular-mass-organic acids by six tree species alters the dynamics of calcium and magnesium in soil. Can J Soil Sci. 2016;96(2):199–206.10.1139/cjss-2015-0063Search in Google Scholar

[19] Olsson PA, Tyler G. Occurrence of non-mycorrhizal plant species in south Swedish rocky habitats is related to exchangeable soil phosphate. J Ecol. 2004;92(5):808–15.10.1111/j.0022-0477.2004.00912.xSearch in Google Scholar

[20] Hayes PE, Nge FJ, Cramer MD, Hayes PE, Nge FJ, Cramer MD, et al. Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus impoverished landscapes. Plant Soil. 2021;462:6–88.10.1007/s11104-021-04886-0Search in Google Scholar

[21] Wala M, Kołodziejek J, Mazur J. The diversity of iron acquisition strategies of calcifuge plant species from dry acidic grasslands. J Plant Physiol. 2023;280:153898.10.1016/j.jplph.2022.153898Search in Google Scholar PubMed

[22] De Silva DLR, Ruiz LP, Atkinson CJ, Mansfield TA. Physiological disturbances caused by high rhizospheric calcium in the calcifuge Lupinus Luteus. J Exp Bot. 1994;45(5):585–90.10.1093/jxb/45.5.585Search in Google Scholar

[23] Vicherová E, Hájek M, Hájek T. Calcium intolerance of fen mosses: physiological evidence, effects of nutrient availability and successional drivers. Perspect. Plant Ecol. 2015;17(5):347–59.10.1016/j.ppees.2015.06.005Search in Google Scholar

[24] Tyler D. Mineral nutrient limitations of calcifuge plants in phosphate sufficient limestone soil. Ann Bot. 1996;77(6):649–56.10.1006/anbo.1996.0081Search in Google Scholar

[25] Zohlen A, Tyler G. Immobilization of tissue iron on calcareous soil: differences between calcicole and calcifuge plants. Oikos. 2000;89(1):95–106.10.1034/j.1600-0706.2000.890110.xSearch in Google Scholar

[26] Li W, Xu F, Chen S, Zhang Z, Zhao Y, Jin Y, et al. A comparative study on Ca content and distribution in two Gesneriaceae species reveals distinctive mechanisms to cope with high rhizospheric soluble calcium. Front Plant Sci. 2014;5:647.10.3389/fpls.2014.00647Search in Google Scholar PubMed PubMed Central

[27] Ding W, Clode PL, Clements JC, Lambers H. Sensitivity of different Lupinus species to calcium under a low phosphorus supply. Plant Cell Environ. 2018;41(7):1512–23.10.1111/pce.13179Search in Google Scholar PubMed

[28] Liao J, Liang D, Jiang Q, Mo L, Pu G, Zhang D. Growth performance and element concentrations reveal the calcicolecalcifuge behavior of three Adiantum species. BMC Plant Biol. 2020;20(1):1–8.10.1186/s12870-020-02538-6Search in Google Scholar PubMed PubMed Central

[29] Wei X, Jiang S, Jian Y, Tang H, Cao H. Research progress of Camellia nitidissima, a rare and endangered plant. J Fujian Sci Technol. 2006;33:169–74.Search in Google Scholar

[30] Su Z, Mo X. Geographic distribution of Camellia section Chrysantha form China. Guihaia. 1988;8(1):75–81.Search in Google Scholar

[31] Liang S. Classification of Camellia section Chrysantha and their ecological geographical distribution characteristics. Guangxi Sci. 1989;1:1–3.Search in Google Scholar

[32] Zhang H, Ren S. Flora of China, the third fascicle in forty-ninth volume. Beijing: Science Press; 1998.Search in Google Scholar

[33] Li G, Jiang C, Hang X, Qi Y, Li Z, Luo X, et al. Yellow camellia illustrated handbook. Nanning: Guangxi Science and Technology Press; 2021.Search in Google Scholar

[34] Ge Y, Zou L, Tang G, Zhou T, Huang S. Phenological characteristics of 7 species of Sect. Chrysantha Chang in Guilin Botany Garden. Acta Agric Jiangxi. 2009;21(4):59–60.Search in Google Scholar

[35] Zhu X, Tang J, Qin H, Bai K, Chen Z, Zou R, et al. Contrasting adaptation mechanisms of golden Camellia species to different soil habitats revealed by nutrient characteristics. Agron J. 2022;12(7):1511.10.3390/agronomy12071511Search in Google Scholar

[36] Chai S, Tang J, Mallik A, Shi Y, Zou R, Li J, et al. Eco-physiological basis of shade adaptation of Camellia nitidissima, a rare and endangered forest understory plant of Southeast Asia. BMC Ecol. 2018;18:1–10.10.1186/s12898-018-0159-ySearch in Google Scholar PubMed PubMed Central

[37] Chai S, Zhuang X, Wei X, Wang M, Tang J, Chen Z. Effects of light intensity on photosynthesis and physiological characteristics in seedlings of Camellia pubipetala. Acta BotBoreali-Occident Sin. 2013;33(3):547–54.Search in Google Scholar

[38] Wei X, Chai S, Chen Z, Wang ML, Jiang Y, Tang H, et al. Conservation biology of the rare and endangered golden Camellia species. Nanning: Guangxi Science and Technology Press; 2015.Search in Google Scholar

[39] Wei X, Jiang YS, Jiang SY, Qi XX, Xiong ZC, Ye WH, et al. Photosynthetic characteristics of an endangered species Camellia nitidissima and its widespread congener Camellia sinensis. Photosynthetica. 2008;46(2):312–4.10.1007/s11099-008-0057-1Search in Google Scholar

[40] Baker NR. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol. 2008;59:89–113.10.1146/annurev.arplant.59.032607.092759Search in Google Scholar PubMed

[41] Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol. 1987;148:350–82.10.1016/0076-6879(87)48036-1Search in Google Scholar

[42] Bremner JM. Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci. 1960;55(1):11–33.10.1017/S0021859600021572Search in Google Scholar

[43] Zarcinas BA, Cartwright B, Spouncer LR. Nitric acid and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal. 1987;18(1):131–46.10.1080/00103628709367806Search in Google Scholar

[44] Newton IP, Cowling RM, Lewis OAM. Growth of calcicole and calcifuge Agulhas Plain Proteaceae on contrasting soil types, under glasshouse conditions. S Afr J Bot. 1991;57(6):319–24.10.1016/S0254-6299(16)30909-7Search in Google Scholar

[45] Cross AT, Stevens JC, Sadler R, Moreira-Grez B, Ivanov D, Zhong H, et al. Compromised root development constrains the establishment potential of native plants in unamended alkaline post-mining substrates. Plant Soil. 2018;461:163–79.10.1007/s11104-018-3876-2Search in Google Scholar

[46] Pedersen J, Fransson AM, Olsson PA. Performance of Anisantha (Bromus) tectorum and Rumex acetosella in sandy calcareous soil. Flora. 2011;206(3):276–81.10.1016/j.flora.2010.07.002Search in Google Scholar

[47] Farquhar GD, Sharkey TD. Stomatal conductance and photosynthesis. Ann Rev Plant Physiol. 1982;3(1):317–45.10.1146/annurev.pp.33.060182.001533Search in Google Scholar

[48] Candana N, Tarhanb L. Effects of calcium, stress on contents of chlorophyll and carotenoid, LPO levels, and antioxidant enzyme activities in Mentha. J Plant Nutr. 2005;28(1):127–39.10.1081/PLN-200042192Search in Google Scholar

[49] Zhou R, Yu X, Kjær KH, Rosenqvist E, Ottosen CO, Wu Z. Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ Exp Bot. 2015;118:1–11.10.1016/j.envexpbot.2015.05.006Search in Google Scholar

[50] Dai Y, Shao M, Hannaway D, Wang L, Liang J, Hu L, et al. Effect of Thrips tabaci on anatomical features, photosynthetic characteristics and chlorophyll fluorescence of Hypericum sampsonii leaves. Crop Prot. 2009;28(4):327–32.10.1016/j.cropro.2008.11.012Search in Google Scholar

[51] Kitajima K, Hogan KP. Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ. 2003;26(6):857–65.10.1046/j.1365-3040.2003.01017.xSearch in Google Scholar PubMed

[52] Björkman O, Demmig-Adams B. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. Ecophysiology of photosynthesis. Berlin, Heidelberg: Springer Berlin Heidelberg; 1995. p. 17–47.10.1007/978-3-642-79354-7_2Search in Google Scholar

[53] Shi J, Strack D, Albornoz FE, Shi J, Strack D, Albornoz FE, et al. Differences in investment and functioning of cluster roots account for different distributions of Banksia attenuata and B. sessilis, with contrasting life history. Plant Soil. 2020;447:85–98.10.1007/s11104-019-03982-6Search in Google Scholar

[54] Snaydon RW. The growth and competitive ability of contrasting natural populations of Trifoliun repens L. on calcareous and acid soils. J Ecol. 1962;50:439–47.10.2307/2257454Search in Google Scholar

[55] Lindsay WL, Vlek PLG, Chien SH. Phosphate minerals. In: Dixon JB, Weed SB, editors. Minerals in soil environment. 2nd edn. Madison: Soil Science Society of America; 1989. p. 1089–130.10.2136/sssabookser1.2ed.c22Search in Google Scholar

[56] Tyler G. Inability to solubilize phosphate in limestone soils – key factor controlling calcifuge habit of plants. Plant Soil. 1992;145:65–70.10.1007/BF00009542Search in Google Scholar

[57] Tyler G. A new approach to understanding the calcifuge habit of plants. Ann Bot-London. 1994;73(3):327–30.10.1006/anbo.1994.1038Search in Google Scholar

[58] Zohlen A, Tyler G. Soluble inorganic tissue phosphorus and calcicole-calcifuge behaviour of plants. Ann Bot. 2004;94(3):427–32.10.1093/aob/mch162Search in Google Scholar PubMed PubMed Central

[59] Ström L, Olsson T, Tyler G. Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic acids. Plant Soil. 1994;167:239–45.10.1007/BF00007950Search in Google Scholar

[60] Ström L. Root exudation of organic acids: importance to nutrient availability and the calcifuge and calcicole behaviour of plants. Oikos. 1997;80:459–66.10.2307/3546618Search in Google Scholar

[61] Mengel K. Iron availability in plant tissues—iron chlorosis on calcareous soils. Plant Soil. 1994;165:275–83.10.1007/BF00008070Search in Google Scholar

[62] Susin S, Abadia A, Gonzales-Reyes JA, Lucena JJ, Abadia J. The pH requirement for in vivo activity of the iron deficiency-induced “turbo” ferric chelate reductase. Plant Physiol. 1996;110(1):111–23.10.1104/pp.110.1.111Search in Google Scholar PubMed PubMed Central

[63] Kosegarten HU, Hoffmann B, Mengel K. Apoplastic pH and Fe3+ reduction in intact sunflower leaves. Plant Physiol. 1999;121(4):1069–79.10.1104/pp.121.4.1069Search in Google Scholar PubMed PubMed Central

[64] Cawthray GR, Denton MD, Grusak MA, Shane MW, Veneklaas EJ, Lambers H. No evidence of regulation in root-mediated iron reduction in two Strategy I cluster-rooted Banksia species (Proteaceae). Plant Soil. 2021;461:203–18.10.1007/s11104-021-04849-5Search in Google Scholar

[65] Zargar Shooshtari F, Souri MK, Hasandokht MR, Kalate Jari S. Glycine mitigates fertilizer requirements of agricultural crops: case study with cucumber as a high fertilizer demanding crop. Chem Biol Technol Agric. 2020;7(1):1–10.10.1186/s40538-020-00185-5Search in Google Scholar

[66] De Silva DLR, Mansfield TA. The stomatal physiology of calcicoles in relation to calcium delivered in the xylem sap. Proc R Soc Lond Ser B Biol Sci. 1994;257(1348):81–5.10.1098/rspb.1994.0097Search in Google Scholar

[67] Jessop RS, Roth G, Sale P. Effects of increased levels of soil CaCO3 on lupin (Lupinus angustifolius) growth and nutrition. Soil Res. 1990;28(6):955–62.10.1071/SR9900955Search in Google Scholar

[68] Kerley SJ, Huyghe C. Comparison of acid and alkaline soil and liquid culture growth systems for studies of shoot and root characteristics of white lupin (Lupinus albus L.) genotypes. Plant Soil. 2001;236:275–86.10.1023/A:1012724821957Search in Google Scholar

[69] Kerley SJ, Huyghe C. Stress-induced changes in the root architecture of white lupin (Lupinus albus) in response to pH, bicarbonate, and calcium in liquid culture. Ann Appl Biol. 2002;141(2):171–81.10.1111/j.1744-7348.2002.tb00210.xSearch in Google Scholar

[70] Virk SS, Cleland RE. The role of wall calcium in the extension of cell walls of soybean hypocotyls. Planta. 1990;182(4):559–64.10.1007/BF02341032Search in Google Scholar PubMed

[71] Yu Q, Tang C. Lupin and pea differ in root cell wall buffering capacity and fractionation of apoplastic calcium. J Plant Nutr. 2000;23(4):529–39.10.1080/01904160009382037Search in Google Scholar

[72] McLaughlin SB, Wimmer R. Tansley review No. 104 calcium physiology and terrestrial ecosystem processes. N Phytol. 1999;142(3):373–417.10.1046/j.1469-8137.1999.00420.xSearch in Google Scholar

[73] Ding W, Clode PL, Clements JC, Lambers H. Effects of calcium and its interaction with phosphorus on the nutrient status and growth of three Lupinus species. Physiol Plant. 2018;163(3):386–98.10.1111/ppl.12732Search in Google Scholar PubMed

[74] Takagi D, Miyagi A, Tazoe Y, Takagi D, Miyagi A, Tazoe Y, et al. Phosphorus toxicity disrupts Rubisco activation and reactive oxygen species defence systems by phytic acid accumulation in leaves. Plant Cell Environ. 2020;43:2033–53.10.1111/pce.13772Search in Google Scholar PubMed

[75] Chai S, Fu R, Zou R, Tang J, Shi Y, Wei J. Effects of different calcium concentrations on photosynthetic and physiological indexes of calcicole- and calcifuge-type golden Camellia. Guihaia 41(2):167–76.Search in Google Scholar

[76] Raza S, Abdel-Wahab A, Jørnsgård B, Christiansen JL. Calcium tolerance and ion uptake of Egyptian lupin landraces on calcareous soils. Afr Crop Sci J. 2000;9(2):393–400.10.4314/acsj.v9i2.27610Search in Google Scholar

[77] Valentinuzzi F, Mimmo T, Cesco S, Al M, Santner J, Hoefer C, et al. The effect of lime on the rhizosphere processes and elemental uptake of white lupin. Environ Exp Bot. 2015;118:85–94.10.1016/j.envexpbot.2015.06.010Search in Google Scholar

[78] Wu G, Li M, Zhong F, Fu C, Sun J, Yu L. Lonicera confuse has an anatomical mechanism to respond to calcium-rich environment. Plant Soil. 2011;338:343–53.10.1007/s11104-010-0549-1Search in Google Scholar

[79] Hayes PE, Clode PL, Guilherme PC, Lambers H. Calcium modulates leaf cell-specific phosphorus allocation in Proteaceae from South-Western Australia. J Exp Bot. 2019;70(15):3995–4009.10.1093/jxb/erz156Search in Google Scholar PubMed PubMed Central

[80] White PJ, Holland JE. Calcium in plant physiology and its availability from the soil. In: White PJ, Holland JE. Proceedings of the International Fertiliser Society 827: Calcium in Plant Physiology and its Availability from the Soil. UK: International Fertiliser Society; 2018.Search in Google Scholar

[81] Zhu X, Tang J, Tao Y, Qin H, Liu K, Xei X, et al. Difference in calcium speciation of leaves of golden Camellia species from calcareous soil and acidic soil habitats. Guihaia. 2023;43(3):442–51.Search in Google Scholar

[82] Wang CY, Wang SJ, Rong L, Luo XQ Analyzing about characteristics of calcium content and mechanisms of high calcium adaptation of common Pteridophyte in Maolan karst area of China. China J Plant Ecol. 2011; 35(10):1061–9.Search in Google Scholar

Received: 2023-05-28
Revised: 2023-11-30
Accepted: 2024-01-17
Published Online: 2024-03-09

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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