1. Introduction
Basil (Ocimum basilicum L.) is a popular annual or perennial herb cultivated in many tropical and temperate regions [1]. Ornamentally, it has a well-branched stem and aromatic tender leaves and can grow well in all types of growing systems [2]. Medically, it has therapeutic values for cough, worms, diarrhea, constipation, skin infections, kidney malfunctions, etc. [3]. The extracts and the essential oil can be exploited as antioxidants or flavoring in the food and cosmetics industry [1,4]. Nowadays, consumer demand is increasingly growing and oriented toward potent, high-quality basil and counterpart products [5]. Thus, the effective management of fertilization is highly important to minimize production risks and meet the basil sustainable intensification goals in agriculture.
The nutritional properties and medicinal values of basil are directly linked to the tissue nutrient compositions, such as nitrogen (N), phosphorus (P), potassium (K), carotenoids, etc. [6]. These minerals contained in basil have been shown to play a pivotal role in human health; also, carotenoids can reduce oxidative stress by scavenging ROS (reactive oxygen species) [7,8]. Meanwhile the plant nutrition status was determined by the amount taken up of chemical constituents present in the growing medium. It is accordingly evident that a sufficient nutrient supply is essential for high-quality basil yield.
Nutritional disorders, nutrient deficiency, in particular, can affect vegetative development and cause plant abnormalities and ultimately retard the crop production. It is noteworthy that the photosynthetic ability can be severely damaged by a specific nutrient deficiency. Specifically, for several macronutrients, the omission of N (predominated by ammonium and nitrate) leads to significant decreases in leaf area and photosynthesis intensity, as well as the loss of leaf green color [9]. Limited photosynthesis was found in P-deprivation plants because of the fact that P is largely required as a phosphorylated intermediate in the photosynthetic carbon reduction (PCR) cycle [10]. K-deficiency-inflicted stomatal closure has been well documented in many plants and was considered a major factor in diminishing net photosynthesis [11,12]. Similar to P and K, magnesium (Mg) is also critically referred to in the process of photosynthesis and long-distance photo-assimilates [13]. Sulfur (S) is a constituent of the essential compound chlorophyll, which is an integral part of the photosynthetic reaction [14]. Furthermore, for certain micronutrients, the photosynthetic electron transport requires bulks of iron (Fe) cofactors for regular biochemical reactions [15]. Manganese (Mn) is believed to contribute to redox behavior concerning the water-oxidizing complexes in photosystem II (PSII) [16]. Copper (Cu) also acts as a redox-active cofactor in the PSII-mediated electron transport [17]. Accordingly, apart from that, the varying extent of damage to photosynthetic capacity can be conferred by nutrient deficiency. Each element should additionally show specific roles in the plant physiology and morphology. Their starvation can affect the plants in distinct and/or similar manners.
Therefore, visual nutrient deficiency symptoms, plant growth determination, and photosynthesis assessment, along with the tissue nutritional status analysis, are highly warranted for diagnosing nutrient disorders and optimizing fertilization strategy in basils. However, on the one hand, previous studies regarding the basil nutrients or factors influencing basil were dominated by the following: the seedlings’ planting time [2,18], the tolerance and toxicity mitigation of boron (B) [2,19], and basil nutrients as affected by the supplemented daily light integral [2,20]. On the other hand, which makes that the nutrient deficiency study in basil remains incipient: visual macro- and micronutrient deficiency symptoms in green basil were not comprehensively reported [1,2]; either the tissue nutrients contents and the relations among the various nutrients in response to the starvation of a specific nutrient are still unknown. For instance, the availability and deficiency of Fe often interact with S because the former in the metabolically activated form will be bound to the latter in support of an Fe–S cluster [21]. Furthermore, the previous research conducted on basil failed to present clear nutrient deficiency images, and most of them focused on one specific nutrient omission, neglecting the integrated comparisons among the nutrient deficiencies and the internal nutrient status; also, which nutrient deficiencies delivered similar impacts were lacking.
Accordingly, the study undertaken herein aims to (1) firstly induce the visual deficiency symptoms by omissions of the specific macro- and micronutrients in juvenile basils cultivated in protected hydroponic systems; (2) determine the effect of specific nutrient deficiency on the basil growth attributes, photosynthetic capacity, and uptake pattern of nutrients; and (3) ascertain the relationships among the various nutrient elements under a specific nutrient deficiency condition.
2. Materials and Methods
2.1. Plant Materials and Growth Conditions
Basil ‘Sweet Basil’ seeds were ordered from Asia Seed Co., Ltd. (Songpa-gu, Seoul, Republic of Korea) and were seeded in single-seed dibble foams (OASIS, Smithers Oasis Company, Seoul, Republic of Korea) separated in 128-cell plug trays (25 April 2022). The seeds germinated under greenhouse conditions at Gyeongsang National University (35°91′ N, 128°03′ E, Jinju, Gyeongsangnam-do, Republic of Korea) in five days after sowing (5 DAS). The seedlings with similar morphology and turned two true leaves stages were screened and demounted out of the tray (14 DAS). Selected uniform seedlings were transplanted and cultivated in an alternating diurnal regime (14 h light at 240 μmol·m−2·s−1 PPFD supplied from top white LED and 10 h darkness) with a hydroponic cultivator (tiiun mini, LG Electronics Inc., Seoul, Republic of Korea). The planting density is 0.05 plants/cm2. The peak wavelength and the dominant wavelength of the white LED light are distributed at 454 and 593 nm, respectively (Figure 1). In order to provide a controlled temperature consistent with the alternating diurnal regime for the basil growth, the hydroponic cultivators were placed in a growth chamber with air-conditioned temperatures at 24 °C (light condition) and 18 °C (dark condition).
2.2. Treatment Solutions and Experimental Design
Subsequently, the treatment solutions were designated on the basis of a multipurpose nutrient solution (MNS) [22,23] without nutrient omission (complete solution—CS) and with the specific nutrient (-N, -P, -K, -Ca, -Mg, -NH4+, -NO3−, -S, -Fe, -Mn, -B, -Zn, -Mo, and -Cu) omitted for deprivation treatments. The detailed recipe and chemicals used are shown in Table 1. One liter of nutrient solution in each cultivator was applied and replenished daily and replaced weekly. The pH of the nutrient solutions was checked daily and maintained at 6.0 ± 0.2 using deionized water-prepared NaOH or HCl. The effect of additionally introduced Na+ or Cl− is negligible in this study because the fluctuation of monitored pH was minor in contrast to the CS. The EC of all the nutrient solutions was 1.5 ± 0.1 mS·cm−1, and this value was inherently caused by the used chemicals.
In total, 14 specific nutrient-omitted solutions and one complete solution were assessed in a completely randomized design with three biological replicates. Each experimental unit was implemented with an independent cultivator containing ten basil seedlings.
Afterward, the basils were harvested on 29 May 2022 (35 DAS) until the visual deficiency symptoms appeared.
2.3. Assessment of Photosynthetic Ability
The photosynthetic ability was determined herein in terms of certain critical parameters. Specifically, the photosynthesis involved pigments, including the total chlorophyll content (a + b), and carotenoids were quantified according to a procedure as reported by Sims and Gamon [24]. The Fv/Fm value and greenness index (GI) were detected on the leaf mid-lamina part after a 30 min active photoperiod using a FluorPen 100 (Photon Systems Instruments, Drásov, Czech Republic) and a PolyPen RP 410 (Photon Systems Instruments, Drásov, Czech Republic), respectively, following the batch manufacturer’s manual.
2.4. Determination of Plant Growth Parameters
The plant growth parameters were determined concomitantly during harvest after the root foams were carefully washed away. The whole plant weight in terms of fresh weight and dry mass was measured by an electronic balance. The leaf area data were collected by a leaf area scanning apparatus (LI-3000, Lincoln, NE, USA). The shoot length, tap root length, and leaf length and width were collected using a metal ruler. The shoot and tap root diameters were measured with a Vernier caliper (CD-20CPX, Mitutoyo Korea Co., Gunpo, Republic of Korea).
2.5. Destructive Sampling and Quantification of Nutrient Content in Leaves
Afterward, the juvenile basil plants were cut at the base to separate the roots and shoots. The plant leaves subjected to different treatments with various statuses and appearances were individually collected.
The quantifications of ions were performed by following a minor modified protocol as presented by Song et al. [25]. The collected fresh leaves were firstly stored at 70 °C in an air-forced oven for the constant dry weight. Accurately weighted 0.1 g dried samples were placed in a furnace (Lilienthal, Bremen, Germany) at 520 °C for 120 min. The ashed samples were subjected to mix with 5 mL 25% HCl and adjusted to 30 mL with deionized water. Then, the clear and impurity-free mixture solutions were acquired after paper filtering. Eventually, the ion contents in the solution specimens were quantified three times using the ICP (inductively coupled plasma) technique (Optima 4300 DV/5300 DV, Perkin Elmer, Rodgau, Germany).
2.6. Statistical Analysis and Graphing
All the displayed data are means ± SE of more than three independent replicates (n > 3). The SAS 8.0 program (SAS 8.2 Inst., Cary, NC, USA) was used for the statistical analysis following one-way ANOVA of Duncan’s multiple range test at p = 0.05. Bar graphs were generated with the GraphPad Prism 8.0 program. The heat maps and the PCA analysis were plotted with Origin 2022 software (Origin Lab Corp., Northampton, MA, USA) to show the correlations among ion contents and to visualize the interrelationships among the attributes investigated in this study, respectively.
3. Results
3.1. Basil Plant Growth Parameters and Nutrient Deficiency Symptoms
The basil seedlings with the complete MNS showed vigorous and healthy growth status and concomitantly formed green and normal shape foliage without any visual deficiency symptoms (Figure 2A(a–c)). But, the omission of specific nutrients in MNS instigated the appearance of unique visual nutrient deficiency symptoms. Meanwhile, the severity of the nutrient deficiency symptoms varies significantly (Figure 2).
3.1.1. N Deficiency, P Deficiency, and K Deficiency
The basil plants subjected to the N, P, and K omission treatments were found to be notably stunted (Figure 2A(d–l)). In specific, the N-deficiency basil plants developed chlorosis, inhibited growth, and even necrosis together with stunted roots (Figure 2A(d–f)). On the whole, the recorded growth parameters of the basil plants under nutrient omissions decreased as compared to those cultured with CS. The fresh weight, shoot length, and leaf area of plants in N omission solution were significantly reduced by 84.8%, 35.4%, and 87.1%, respectively, compared to that treated with CS (Table 2). In addition, the tap root length between the N-deficiency plants and the plants cultured in CS displayed no statistical differences (Table 2).
Similarly, the plants cultivated in the P omission of the nutrient solutions also developed prominent nutrient deficiency symptoms; the slender and smaller leaves with olive-green spots can be firstly observed, then the abscised leaves with certain marginal necrosis appeared (Figure 2A(g–i)). Consistent with that, the fresh weight, shoot diameter, and leaf area of P-deficiency plants markedly decreased by 86.1%, 50.2%, and 83.8%, respectively, compared with that grown in the CS regime (Table 2).
Unlike N deficiency and P deficiency, the K-deficiency basil plants did not develop conspicuous diminishments in plant size relative to that cultured with CS. However, the unhealthy appearances were also detected as characterized by the stunted leaves firstly, progressed by leaf yellowing and even scorching; freckles were observed in the central part of leaves during this period (Figure 2A(j–l)). Compared with the basil plants cultivated in CS, the fresh weight, shoot length, and leaf area of K-deficiency plants significantly declined by 49.4%, 36.8%, and 35.6%, respectively (Table 2).
3.1.2. Ca Deficiency, Mg Deficiency, and S Deficiency
Symptoms of Ca deficiency displayed are slightly stunting regarding the decreased growth parameters and irregular leaf shape. Specifically, the Ca omission caused the leaflets to narrow with lighter green coloration when compared to the CS-treated plants (Figure 2A(m–o)). The dry weight, shoot length, and tap root diameter of Ca omission plants significantly declined by 18.8%, 18.5%, and 30.8%, respectively, when compared with the plants grown in CS (Table 2). The Mg-deficiency plants possessed relatively small-sized leaves and further displayed chlorosis from the edge to the central portion of the old leaves advanced by the curling (Figure 2A(p–r)). The Mg omission presented the marked declines of the studied parameters with the exception of tap root length when compared to the plants grown in CS (Table 2). The primary symptoms of S deficiency were a slight overall loss of green coloration, resulting in fragile and yellowing foliage (Figure 2A(s–u)). The S-deficiency symptoms were further characterized by the restricted growth attributes. For instance, the whole fresh weight, dry weight, and leaf area of S-deficiency plants dramatically reduced 30.3%, 28.1%, and 29.8%, respectively, compared with that cultured in the CS regime (Table 2).
3.1.3. NH4+ Deficiency and NO3− Deficiency
The NH4+ deficiency plants manifested highly contrasting symptoms compared to those cultured with NO3− omission solutions (Figure 2A(v–aa)). The former basil plants showed similar morphology and appearances as compared to the plants grown in CS treatment, whereas the latter basil plants finally developed the NH4+ toxicity symptoms, as characterized by severe chlorosis and even dead fronds, necrosis, and stunted growth (Figure 2A(aa)). It could be demonstrated that the basil plants were highly sensitive to the NH4+ nutrition while they were tolerant to the NO3− nutrition. These findings were further evidenced by the recorded growth parameters. The fresh weight, shoot diameter, and leaf area of NH4+ deficiency plants were not significantly different (no statistical difference) from the NO3− deficiency plants (Table 2). However, all the recorded growth attributes of NO3− deficiency plants were conspicuously disturbed. Notably, the whole fresh weight, shoot length, leaf area, and tap root length of NO3− omission plants remarkedly decreased by 91.9%, 60.1%, 83.2%, and 78.8%, respectively, compared to the basil plants treated with CS (Table 2).
3.1.4. Fe Deficiency and Mo Deficiency
The growth was significantly inhibited when the basil plants were grown in the Fe omission solution. The notable symptomology of Fe deficiency was the overall foliage discoloration (netted chlorosis) with burned tips, together with the stunted roots (Figure 2B(a–c)). Consistently, the recorded growth parameters of Fe deficiency plants were all significantly curtailed. For example, the whole fresh weight, leaf area, and tap root length of Fe deficiency plants dramatically declined 84.2%, 87.1%, and 86.9%, respectively, in comparison with that treated with CS (Table 2). Furthermore, the basil growth was also significantly disturbed when grown under a Mo-deficient solution relative to that treated with CS (Table 2). And the major Mo deficiency symptoms were stunted roots and leaves accompanied by downward curling of margins (Figure 2B(m–o)).
3.1.5. Mn Deficiency, B Deficiency, Zn Deficiency, and Cu Deficiency
The consensus nutrient deficiency symptoms of Mn, B, Zn, and Cu in this study were slight chlorosis, irregular leaf shapes, and stunted roots (Figure 2B). However, with the exception of whole fresh weight, the other studied growth traits of Mn, B, Zn, and Cu deficiencies plants were all significantly decreased relative to the plants grown in CS (Table 2).
3.2. Photosynthetic Capacity
The photosynthesis of basil plants was greatly influenced when they were subjected to nutrient deficiencies. The photosynthetic capacity was estimated herein by the photosynthesis pigments, Fv/Fm, and greenness index.
On the whole of Figure 3, as compared to the basil plants grown in the CS regime, the photosynthetic capacity to varying degrees declined, regardless of the nutrient omission treatments, in particular of the plants that developed chlorosis, such as -N, -P, -S, -Fe, etc. Take the omission of S as an example. The chlorophyll a, b, and carotenoids of S-deficiency plants significantly decreased 51.7%, 52%, and 49.1%, respectively, when compared to the plants grown in CS (Figure 3A). The Fv/Fm value of -N, -P, -K, -Ca, -NO3−, -S, and -Fe remarkably diminished by 15%, 9.2%, 7.4%, 6.6%, 70.9%, 15.9%, and 32.2%, respectively (Figure 3B). Meanwhile, the greenness index of -N, -K, -Ca, -NO3−, -S, -Fe, and -Mo significantly reduced 21.2%, 12.4%, 14.6%, 45.3%, 21.2%, 32.1%, and 19.7%, respectively (Figure 3C).
3.3. Macronutrient Uptake
The macronutrient contents regarding P, K, Ca, Mg, and S were significantly influenced by the specific nutrient deprivation treatments. The omissions of specific macronutrients resulted in the reductions of corresponding internal macronutrient contents (Figure 4). Nutrient solutions omitted N, Mg, NO3−, and S notably reduced the accumulation of P, whereas the omissions of K and Zn significantly induced the P uptake in the basil plants (Figure 4A). It was noted that the K-deficiency plants distinctly increased the Ca uptake (Figure 4C); also, the Ca-deficiency plants significantly increased the K uptake (Figure 4B); concomitantly, either K or Ca omitted plants significantly increased the uptake of Mg (Figure 4D). Additionally, K-, Ca-, and Mg- deficiency plants dramatically decreased the uptake of S, while the omissions of N and P did not decline (Figure 4E).
In addition, the basil plants cultured in the omissions of NH4+, S, and Fe notably improved the accumulation of Ca (Figure 4C). Similar to this, the deficiencies of P, NH4+, and Fe significantly increased the uptake of Mg (Figure 4D). However, only the NO3−-deficiency plants enhanced the uptake of S (Figure 4E).
3.4. Micronutrients Uptake
Similar to the macronutrient contents, the micronutrient uptake regarding Fe, Mn, B, Zn, Mo, and Cu were also distinctly altered in response to the specific nutrient deprivations. Still, the omitted specific micronutrients from culture solutions lead to the diminishments of corresponding specific nutrients (Figure 5).
Specifically, the internal Fe contents of the specific nutrient deficiency treatments were almost similar to that in CS (no statistical difference), with the exceptions of N- and P-omitted treatments. These two nutrient-deficient plants significantly improved the uptake of Fe (Figure 5A). Similar to Fe, omissions of P and S from the nutrient solutions drastically increased the uptake of Mo, while the omissions of N, P, and NO3− from the nutrient solutions significantly increased the uptake of Cu (Figure 5E,F).
On the other hand, it is highly noteworthy that the deficiency of S, Fe, B, Zn, and Cu rapidly reinforced the uptake of Mn (Figure 5B). On the contrary, with the exception of N and P deficiency, omissions of other recorded nutrients significantly declined the accumulation of B (Figure 5C). Meanwhile, merely P-omitted and Fe-omitted solution-treated plants notably improved the Zn concentration as compared to that in CS (Figure 5D).
3.5. Correlations
3.5.1. Correlations of Nutrients under Macronutrients Deficiencies
The correlations among the investigated concentrations of nutrients under the macronutrient deficiencies were greatly different (Figure S1). Taking the correlations among micronutrients aside, notably, the P was positively correlated with both K and Mg in CS, -N, -Ca, and -Mg, whereas it was negatively correlated with Mg and K, respectively, in -P and -K treatments (Figure S1A–F). The K was positively correlated with the P and Mg in CS, -N, -P, -Ca, and -Mg, while it had a negative correlation with P and Mg in K-deficiency plants (Figure S1D). Likewise, there was a negative correlation between the Ca and Mg in Mg-deficiency plants, while Ca was positively correlated with Mg in CS, -N, -P, -K, and -Ca treatments (Figure S1F). The Mg was positively correlated with P, K, and Ca in CS and when N and Ca were omitted (Figure S1A,B,E), but negative correlations were detected between Mg and P, K, together with Ca in -P, -K, and -Mg regimes, respectively (Figure S1C,D,F). Also, S was found to be positively correlated with Ca in CS, -P, -Ca, and -S treatments (Figure S1A,C,G), while it was negatively correlated with Ca in -N, -K, and -Mg groups (Figure S1B,D,F).
It is worth noting that minor correlations among nutrients were negative when either NO3− or NH4+ was omitted from the solutions. In particular, B was negatively correlated with K, Ca, Mg, Fe, Mn, Zn, Mo, and Cu (Figure S1H); P was negatively correlated with Ca, Mg, S, Fe, Mo, and Cu when the plants were cultured in NO3− deficiency solutions (Figure S1I).
3.5.2. Correlations of Nutrients under Micronutrients Deficiencies
Similar to the results found above, big differences in the correlations were also conferred when the micronutrients were omitted from the solutions (Figure S2). We noticed that minor negative correlations among the nutrients were pronounced when the solutions did not contain Mn and Mo (Figure S2B,E). For example, notably, K had a negative correlation with Ca, Mg, and S when Mo was omitted from the solutions (Figure S2E).
Additionally, more important is that P was positively correlated with Mg in Fe deficiency plants, whereas the relation between them was negative when B, Zn, and Cu were omitted from the solution (Figure S2A,C,D,F). There was a negative relationship between K and Ca in -Fe and -Cu treatments, but K was positively correlated with Ca in B-deficiency and Zn-deficiency plants (Figure S2A,C,D,F). Mg was positively correlated with S in the plants treated with -B, -Zn, and -Cu, while it was negatively correlated with S when Fe was omitted from the solution (Figure S2A).
3.6. Principal Component Analysis (PCA)
To visualize the relationships of the studied nutrient deficiencies together with the investigated specific nutrient contents under nutrient deficiency. Principal component analysis (PCA) on the basis of the treatments and corresponding nutrient concentrations dataset was performed.
The PCA embodied the recorded parameters along the first two principal dimensions (PC1 = 38.2% and PC2 = 18.2%) that accounted for 56.4% of the data variability (Figure 6). On the whole, the majority of the samples cultivated in the macronutrient omitted solutions were distributed on the right quadrants of the PC1 scatter plot, whereas micronutrient deficiency samples were separated in the left quadrants of the PC1 scatter plot, which showed the contrasting traits of plants between the micronutrient deficiencies and macronutrient deficiencies (Figure 6 ‘PC1’).
In addition, P-omitted and N-omitted solutions-treated plants possessed higher contents of Fe, Cu, Zn, and B; K-deficiency-treated plants displayed higher contents of Ca and Mg, presenting a negative correlation of the NO3−-deficiency counterparts (Figure 6 ‘PC2’). Also, the distributions of S-deficiency samples were similar to the Fe deficiencies, simultaneously exhibiting a relatively higher content of Mn.
4. Discussion
Generally, each nutrient is capable of delivering a specific function in the plants. On the other hand, omissions of the specific elements in plants were associated with the symptoms or toxicity [26]. While certain basil nutrient deficiency symptoms have been reported in early publications, rigorous symptomatic progressions remain limited or non-existent according to the literature [1,27,28]. Besides, the responses of internal nutrient changes and the relations of the recorded nutrients under the nutrient deficiency treatments have been rarely studied. Therefore, the current study evaluated and compared the impacts of specific nutrient deficiency on plant growth traits (including the symptoms or toxicity), photosynthesis, internal nutrient concentrations, and the correlations of the investigated nutrients.
4.1. Basil Growth and Photosynthetic Ability as Affected by Nutrient Deficiency
Nutrient deficiency is linked to the modulations of plant processes, disturbing the growth and morphology, eventually imparting the symptoms or toxicity [29]. In this study, the basil plants grown with deficiencies of N, P, S, and Fe solutions apparently developed chlorosis and curtailed the leaf size (Figure 2). These findings were consistent with the previous reports [30,31,32]. Concurrently, NO3−-omitted solutions-treated basil plants developed the NH4+ toxicity symptoms, which indicated that basil was a NH4+-sensitive species. Accordingly, the basil growth and development were highly limited by N, P, S, Fe, and NO3−.
N was associated with many metabolic and biosynthetic pathways and played an important role in determining crop yield [33]. We found that the omission of N significantly suppressed the fresh weight, shoot length, and leaf area (Table 1). Similar inhibitions were also presented by Nurzynska-Weirdak et al. [34]. Lack of N could also influence cell synthesis and the photosynthesis process. It has been well demonstrated that deprivation of N for plants could lower the photosynthesis pigments [35]. In this study, the chlorophyll contents and carotenoids markedly decreased when the plants were treated without N (Figure 3). Similar to N deficiency, the omissions of P from the nutrient solutions significantly declined the growth parameters and eventually presented the corresponding visual nutrient deficiency symptoms (Table 2; Figure 2). The deficiency of P could also reduce the basil dry mass, which is in line with the previous results by Deroles [36]. As a mobile element, P was considered an activator for many metabolic enzymes related to the carbohydrate metabolism and phosphate transfer process, such as plant growth and photosynthesis [37]. Indeed, P-omitted basil rapidly decreased the chlorophylls a and b, together with the Fv/Fm (Figure 3B). The Fv/Fm value refers to the reflection on the maximum photosynthesis II photochemistry (PSII). It has been widely adopted as a reflection on the stress degree of plants [38]. We also found that the omissions of S, Fe, and NO3− from the nutrient solutions significantly decreased the Fv/Fm value compared to the plants in CS (Figure 3B). Both S and Fe were intimately utilized by plants in the formation of proteins, such as chlorophylls, and they were required for chloroplast morphology and cell development [39,40]. It showed that the basil plants treated without S and Fe notably suffered the loss of photosynthesis pigments (Figure 3A). And deficiencies of S- and Fe-generated chlorosis can be found in a wide variety of plants, osculating from vegetables to fruits [41,42].
Interestingly, the NH4+ toxicity symptoms were developed in the NO3−-deficiency basil plants, indicating that the basil plants were highly sensitive to high NH4+ nutrition. We previously showed that cabbage and salvia were NH4+-sensitive plants, and the NO3−-omitted solution used in this study was identical to our previous studies [43,44]. Also, the photosynthetic ability regarding the Fv/Fm and the greenness index were highly disturbed (Figure 3B,C).
Additionally, taking the Fe-omitted and Mo-omitted plants aside, the whole fresh weight of basil plants cultured in the solutions without Mn, B, Zn, and Cu exhibited no difference from that in CS. Other investigated growth traits were significantly decreased compared to those in CS (Table 2). Notable diminishments of these growth parameters were also observed in many plant species when lacking Mn, B, Zn, and Cu, such as cabbage [45], tobacco [46], and lettuce [47]. However, for these mentioned micronutrient deficiencies, we found that only slight nutrient deficiency symptoms were developed in leaves (Figure 2) due to the fact that the visual symptoms only appeared when the plant growth was severely depressed [42,48]. These four micronutrients were strongly related to photosynthesis. The deprivations of these four microelements resulted in the breakdown of Chl and carotenoids [42,49]. Indeed, the current study showed that the basil plants grown in the solutions omitted Mn, B, Zn, and Cu had markedly decreased the chlorophylls and Fv/Fm ratio (Figure 3), illustrating the finite photosynthesis by nutrient deficiency.
4.2. Nutrient Uptake as Affected by Nutrient Deficiency
In this study, the nutrient uptake was significantly influenced when the specific nutrient was omitted from the solutions, irrespective of the macro- or micronutrients considered (Figure 4). Similar results were also found by Campos et al. in cucumber [50]. However, the nutrient uptake efficiency and the influences of specific nutrient deficiency on the other nutrients vary greatly among plant species.
Specifically, a consensus finding for all the treatments is that lack of the specific nutrient could lead to the decline of the corresponding nutrient (Figure 4 and Figure 5). The omissions of K and Zn from the solutions significantly accumulated the uptake of P in the plants, while the N-omitted and NO3−-omitted plants had the lowest P concentrations (Figure 4A). Zhu et al. showed that the availability of P was negatively correlated with Zn uptake [51]; Wang et al. advocated that the enhancement of P by the starvation of K was attributed to the efflux of certain organic acids [52]. The starvation of N and NO3− readily resulted in the decrease in P due to the fact that both elements were critical constituents of nucleic acids, amino acids, and protein, thereby lowering the P accumulations [30].
Many pioneer studies have disclosed that the K deficiency could regulate the Ca sensors and concurrently stimulate the modulations of intracellular calcium levels [53]. Besides, an antagonistic interaction was observed between the K and Mg, which was regarded as a major cause of Mg deficiency [54]. Consistently, we found that the omission of Ca significantly promoted the increase in K while the omission of K notably accelerated the uptake of Ca (Figure 4B,C), whereas both K-deficiency and Ca-deficiency plants drastically improved the contents of Mg (Figure 4D). This phenomenon occurred probably because the plants took up more Mg ions toward the nutritional balance in order to compensate for the large amount of loss of K and Ca [55]. Moreover, for the K deficiency, Ca deficiency, Mg deficiency, NH4+ deficiency, and micronutrients deficiency, the basil plants rapidly declined the accumulations of S (Figure 4E), suggesting that the importance of S was related to the other ions activities and diverse biological processes, such as redox modulators and stress alleviations [56].
Meanwhile, the basil plants cultivated in the NO3−-deficiency solutions significantly decreased the contents of P, K, Ca, and Mg, whereas the content of S increased (Figure 4). Similar results were found in salvia [44], cabbage [23], and beans [57]. They were identified as the NH4+-sensitive plants. One of the key NH4+ toxicity symptoms was the notable decrease in the net efflux of cations, such as K+ and Ca2+; thus, basil was a NH4+-sensitive species in this study.
The plants grown in the P-deficiency and N-deficiency solutions drastically improved the uptake of Fe (Figure 5A). This finding agrees well with the fact that the availability of P was involved in the uptake of Fe in plants, and this interaction between them influenced diverse biological processes [58], and the deficiency of P could elicit the accumulation and assimilations of Fe as previously noted [59,60]. Nitrogen and iron (Fe) are essential to the proper functioning of the photosynthetic apparatus, and Fe is required for the uptake, transport, and assimilation participating in the N metabolism pathway [61,62]. The basil plants absorbed more Fe as the deprivation of N to cope with the disequilibrium of nutrition [63]. Similar results were obtained that the Cu contents were improved when N was omitted and P was omitted (Figure 5F). Consistently, Cu fertilizer can depress the deficiencies of N and P, according to Chaudhry and Loneragan [64].
We found that the lack of either P or S notably increased the contents of Mo (Figure 5E). Molybdenum (Mo) is a vital constitute in plant nutrition, and it is known to be obligatory of an element catalytically active catalyzing the enzymes, in particular of the P- and S-containing proteins [65,66]. However, Zn content was found to increase when P was omitted and Fe was omitted (Figure 5D). It has been advocated that Zn had an antagonistic relationship with Fe. In other words, the uptake of Zn was interfered with by Fe translocation, and the deficiency of Fe could lead to the increase in Zn [67,68]. The Mn level was significantly enhanced when S and the studied micronutrients regarding Fe, B, Zn, and Cu were respectively omitted (Figure 5B). The Mn is also an essential element and is involved in diverse plant processes, such as photosynthesis and hormone signaling. It has been shown that Mn is required as an enzyme cofactor for biological reactions, and it is interchangeable with certain divalent cations, like Cu or Zn [69]. Thus, Mn is able to replace S, Fe, B, Zn, and Cu, participating in the active site of enzymes.
4.3. The Relations of Nutrient Uptake under Nutrient Deficiency
In order to deal with the nutrition deficiencies, the basil plants are required to harmonize the multiple-nutrient homeostasis [70]. In the present study, among all the treatments, the P nutrition was negatively correlated with Mg in the plants when treated with P-omitted, NO3−-omitted, Zn-omitted, B-omitted, and Cu-omitted solutions, whereas this relation was shown to be positive in CS (Figures S1 and S2). Indeed, it has been advocated that Mg is a promoter for numerous kinase enzymes and triggers the majority of phosphate transfer processes [29]. Also, the supplementary of P could mitigate the Mg-deficiency symptoms in field-grown vines [71].
The K nutrition was negatively correlated with Ca nutrition in CS, -Mg, -S, -K, -Ca, -Fe, -Mo, and -Cu solutions, but it was positively correlated with Ca in -N, -P, -NH4+, -NO3−, -Zn, -Mn, and -B solutions (Figures S1 and S2). In addition to the competitive interactive effect between the absorptions of K and Ca, other inhibitory impacts of Ca on K by short-term trials have also been reported [72]. Thus, this negative relation was pronounced when either K or Ca was deficient. But, in such N- or P-deficiency conditions, the plants might facilitate the accumulations of Ca and K to reduce the detrimental effects caused by the deficiencies of N or P [73].
The S nutrition was positively correlated with Fe in the basil plants treated with CS, -N, -P, -S, -NH4+, -Ca, and -NO3−; however, this correlation was shown to be negative when the plants were grown in -Mg, -K, -Fe, and -Zn (Figures S1 and S2). The positive interaction between S and Fe is associated with the fact that the former can be directly bound to the latter to form chemical complexes, such as Fe-S clusters [74]. Intriguingly, S was negatively correlated with Fe in plants when they were cultured in the Fe-omitted regime. This may be interpreted by the finding that the deprivation of Fe could stimulate the rise of the demand for S, and this can be overcome by the improved acquisition of S [75]. Similar results were observed in the plants when grown in the Mg-omitted, K-omitted, and Zn-omitted solutions. This phenomenon is probably because the element deficiencies altered the plant’s nutritional status. Thereby, the S- or Fe-involving biological processes required the presence of one of these two nutrients [76].
5. Conclusions
To sum up, the current work delivers the foundation for symptoms of nutrient disorders of basil ‘Sweet Basil’ and provides detailed descriptions together with diagnostic images to assist in identifying nutrient deficiencies. Overall, the decline of studied growth parameters, including the plant weight, shoot length and diameter, leaf area, leaf length and width, etc., were observed for the omission of different nutrient elements. The most apparent symptoms, such as chlorosis, stunted growth, and leaf discoloration, were considerably developed as the studied macronutrients and Fe were omitted. Meanwhile, the omissions of certain micronutrients, including Mn, B, Zn, and Cu, slightly conferred chlorosis and leaf discoloration. Outstandingly, the basil plants grown in the NO3−-omitted regime significantly developed the NH4+ toxicity symptoms, suggesting that basil was a NH4+-sensitive species. These findings could be set as new guidelines for nursery managers and farmers applying the correct fertilizer to deal with the exact nutrient deficiency.
The photosynthetic capacity of basil plants significantly decreased when treated with N-omitted, NO3−-omitted, S-omitted, and Fe-omitted solutions. In addition, the specific nutrient deficiency resulted in the overall remarkable difference in nutrient uptake patterns and the modulations of plant internal nutrition levels. Concomitantly, the relationships among the various nutrient elements when under a specific nutrient deficiency condition were significantly altered. Taken together, these data could provide knowledge on the basil nutrient uptake mode and the correlations of nutrient networks under nutrient deficiencies.
Conceptualization, B.R.J. and J.S.; methodology, B.R.J. and J.S.; software, J.S. and J.Y.; validation, B.R.J. and J.S.; formal analysis, B.R.J. and J.S.; investigation, J.S. and J.Y.; resources, B.R.J.; data curation, J.S.; writing—original draft preparation, J.S.; writing—review and editing, B.R.J. and J.S.; supervision, B.R.J.; project administration, B.R.J.; funding acquisition, B.R.J. All authors have read and agreed to the published version of the manuscript.
The original contributions presented in the study are included in the article, further inquiries can be directed to the first author (Jinnan Song).
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. The spectrum distribution of the white LED light generated from the LG hydroponic cultivator.
Enlarge this image.Figure 2. Symptoms of nutritional deficiencies of basil leaves and roots regarding (A) macronutrients and (B) micronutrients. Scale bars in (A) -a, -b, and -c refer to 3 cm, 3 cm, and 1 cm, respectively, and were applied to other corresponding groups.
Enlarge this image.Figure 3. The photosynthetic capacity of basil plants regarding (A) photosynthesis pigments, (B) Fv/Fm, and (C) greenness index. The significant differences among treatments were denoted by different lowercase letters according to one-way ANOVA following Duncan’s multiple range test at p = 0.05.
Enlarge this image.Figure 4. Certain macronutrient levels in basil plants regarding (A) P content, (B) K content, (C) Ca content, (D) Mg content, and (E) S content under CS and specific omitted nutrient conditions. The significant differences among different treatments were determined by one-way ANOVA of Duncan’s multiple range test at p = 0.05 and denoted by different lowercase letters over bars.
Enlarge this image.Figure 5. Certain micronutrient concentrations in basil plants regarding (A) Fe content, (B) Mn content, (C) B content, (D) Zn content, (E) Mo content, and (F) Cu content under CS and specific omitted nutrient conditions. The significant differences among different treatments were determined by one-way ANOVA of Duncan’s multiple range test at p = 0.05 and denoted by different lowercase letters over bars.
Enlarge this image.Figure 6. Data analysis using the principal component analysis (PCA) on the indices involving certain nutrient contents under CS and one single nutrient deficiency condition.
Nutrient compositions for treatment solutions used in this study.
| Nutrient Source | CS | -N | -P | -K | -Ca | -Mg | -NH4+ | -NO3− | -S | -Fe | -Mn | -Zn | -Cu | -Mo | -B |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Macronutrient (me·L−1) | |||||||||||||||
| Ca(NO3)2·4H2O | 4.0 | - | 4.0 | 4.0 | - | 5.0 | 4.8 | - | 4.0 | 4.0 | 4.0 | 4.0 | 4.0 | 4.0 | 4.0 |
| KNO3 | 2.0 | - | 2.0 | - | 3.0 | 1.0 | 2.8 | - | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 |
| KH2PO4 | 4.0 | 2.0 | - | - | 2.0 | 2.0 | 2.0 | - | 2.0 | 4.0 | 4.0 | 4.0 | 4.0 | 4.0 | 4.0 |
| MgSO4·7H2O | 2.0 | 2.0 | 2.0 | 2.0 | - | - | 2.0 | 2.0 | - | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 | 2.0 |
| NH4NO3 | 1.0 | - | 1.0 | - | 1.0 | 1.0 | - | - | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 | 1.0 |
| CaCl2 | - | 3.0 | - | - | - | - | - | 3.0 | - | - | - | - | - | - | - |
| K2SO4 | - | - | 2.0 | - | 2.0 | 2.0 | - | 2.0 | - | - | - | - | - | - | - |
| NH4H2PO4 | - | - | - | 1.0 | - | - | - | 2.0 | - | - | - | - | - | - | - |
| Mg(NO3)2·6H2O | - | - | - | - | 3.0 | - | 0.4 | - | 2.0 | - | - | - | - | - | - |
| (NH4)2SO4 | - | - | - | - | - | - | - | 4.0 | - | - | - | - | - | - | - |
| Micronutrient (ppm) | |||||||||||||||
| Fe-EDTA | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 | - | 15.0 | 15.0 | 15.0 | 15.0 | 15.0 |
| H3BO3 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | 1.4 | - |
| CuSO4·5H2O | 0.2 | 0.2 | 0.2 | 0.2 | 0.2 | 0.2 | 0.2 | 0.2 | - | 0.2 | 0.2 | 0.2 | - | 0.2 | 0.2 |
| MnSO4·4H2O | 2.1 | 2.1 | 2.1 | 2.1 | 2.1 | 2.1 | 2.1 | 2.1 | - | 2.1 | - | 2.1 | 2.1 | 2.1 | 2.1 |
| Na2MoO4·2H2O | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | 0.12 | - | 0.12 |
| ZnSO4·7H2O | 0.8 | 0.8 | 0.8 | 0.8 | 0.8 | 0.8 | 0.8 | 0.8 | - | 0.8 | 0.8 | - | 0.8 | 0.8 | 0.8 |
| CuCl2·2H2O | - | - | - | - | - | - | - | - | 0.14 | - | - | - | - | - | - |
| MnCl2·4H2O | - | - | - | - | - | - | - | - | 1.8 | - | - | - | - | - | - |
| ZnCl2 | - | - | - | - | - | - | - | - | 0.42 | - | - | - | - | - | - |
Whole plant weight and dry weight, shoot length and diameter, leaf area, leaf length and width, tap root diameter, and tap root length as affected by CS and nutrient deficiency treatments.
| Treatment | Fresh Weight (g) | Dry Weight (g) | Shoot Length (cm) | Shoot Diameter (mm) | Leaf Area (cm2) | Leaf Length (cm) | Leaf Width (cm) | Tap Root Diameter (mm) | Tap Root Length (cm) |
|---|---|---|---|---|---|---|---|---|---|
| CS | 5.45 z a y | 0.32a | 6.01a | 2.43ab | 30.19a | 6.71a | 5.82a | 1.3a | 19.8ab |
| -N | 0.83d | 0.06de | 3.88c | 1.32f | 3.88e | 2.81e | 2.23f | 0.7cd | 21.7a |
| -P | 0.76d | 0.04de | 3.40c | 1.20f | 4.90e | 2.60e | 2.24f | 0.6de | 19.8ab |
| -K | 2.76c | 0.19c | 3.80c | 1.83cd | 19.44b | 4.93c | 4.31de | 0.6de | 21.0a |
| -Ca | 4.90ab | 0.26b | 4.90bc | 2.48a | 28.01ab | 6.02b | 5.01bc | 0.9bc | 19.9ab |
| -Mg | 3.96b | 0.23bc | 4.98b | 2.16c | 27.73b | 6.03b | 5.30b | 1.1ab | 19.3ab |
| -NH4+ | 4.97ab | 0.25b | 4.95b | 2.26bc | 28.83a | 6.25b | 5.70ab | 1.2a | 19.1ab |
| -NO3− | 0.44d | 0.09d | 2.40d | 1.56e | 5.07d | 2.72e | 2.43f | 0.4e | 4.2e |
| -S | 3.80b | 0.23bc | 5.30b | 2.14c | 21.18b | 6.01b | 5.02c | 1.0ab | 16.6b |
| -Fe | 0.86d | 0.06de | 4.01c | 1.29f | 3.89e | 2.73e | 2.30f | 0.2e | 2.6e |
| -Mn | 4.92ab | 0.24bc | 5.02b | 1.82cd | 19.01bc | 4.71c | 4.42d | 0.8bc | 13.6bc |
| -B | 4.83ab | 0.23bc | 3.82c | 1.86cd | 18.86c | 4.53c | 4.36d | 0.8bc | 13.2bc |
| -Zn | 5.13a | 0.28b | 4.91bc | 1.96cd | 20.01b | 4.62c | 4.57d | 0.7cd | 14.3bc |
| -Mo | 2.06c | 0.16cd | 3.72c | 1.73d | 9.23d | 3.26de | 2.93f | 0.6de | 10.5d |
| -Cu | 4.87ab | 0.23bc | 4.83bc | 1.85cd | 18.98c | 3.96d | 4.39d | 0.6de | 13.1bc |
z The presented data in each column are means ± SE (n = 6). y The significant differences among different treatments were determined by one-way ANOVA following Duncan’s multiple range test at p = 0.05 and denoted by different lowercase letters.
Supplementary Materials
The following supporting information can be downloaded at:
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; Yang, Jingli 1
; Jeong, Byoung Ryong 2
1 Shandong Provincial University Laboratory for Protected Horticulture, Weifang University of Science and Technology, Shouguang 262700, China;
2 Department of Horticulture, Division of Applied Life Science (BK21 Four Program), Graduate School of Gyeongsang National University, Jinju 52828, Republic of Korea; Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Republic of Korea; Research Institute of Life Science, Gyeongsang National University, Jinju 52828, Republic of Korea