Abstract
Nutrient-depleted soil is a major constraint for crop production, particularly for fruits. Here, we investigated the different response of nitrogen (N), phosphorus (P), and potassium (K) deficiency on the growth and development of strawberry (Fragaria ×ananassa Duch.) in sand culture under greenhouse conditions. Compared with K, the lack of N or P is more unfavorable to strawberry growth and development. N deficiency affected shoot-root (S/R) ratio at different growth stages, and decreased the shoot biomass. P deficiency greatly increased the N content but decreased K content of the plants, which means P is of advantage to regulate the absorption and utilization of N and K nutrients in plants. Meanwhile, P has a profound influence on fruit quality, such as total soluble (TSS) sugar content. K deficiency is not conducive to fruit coloring and the formation of high-quality commercial fruits. The results contribute to a better understanding of the difference of N, P, or K deficiency on strawberry growth, nutrient absorption, and fruit quality during the whole growth period.
Strawberry (Fragaria ×ananassa Duch.) is one of the most popular fruits owing to its appealing appearance, flavor, and various health benefits (Zheng et al. 2021). The high market value of strawberry has significantly promoted its cultivation worldwide (Mezzetti et al. 2018), resulting in an annual production of ∼4.5 million tons of strawberry in the world (Weng et al. 2020). In China, strawberry is also one of the most profitable fruits. In 2016, China ranked third in global strawberry output with a yield of nearly 1.8 million tons among 79 countries, only next to the United States and Mexico (Yong et al. 2020). Thus, efficient management of strawberry nutrients is very critical to agricultural production.
Nutrients are required by organisms for growth, tissue maintenance, reproduction, and maintenance of their functions. Among plant nutrients, only 17 are essential for normal plant growth and development, with each nutrient playing specific roles. N, P, and K are primary mineral fertilizers. N is the most important nutrient for plant growth and fruit bud formation (Li and Lascano 2011), and its deficiency can severely decrease crop yield and quality (Tsialtas and Maslaris 2005). During the rapid growth period, N-deficient plants generally have very small leaves, and the color may change from green to light green or yellow. In old leaves, the petioles and leaves will turn to bright red (Lin et al. 2021; Lineberry and Burkhart 1943), accompanied by decreases in fruit size and the turning of calyx around the fruit to a red color. P is one of the 17 essential nutrients for plants present in every living plant cell. It is involved in various vital plant functions, including energy transfer, photosynthesis, sugar and starch transformation, and nutrient movement within the plant, and is also a part of the genetic material of all cells (DNA and RNA) (Grant et al. 2001; Li et al. 2014a). K is the second most abundant element in plant tissues next to N, which can help to enhance water uptake and fruit quality (Oosterhuis et al. 2014). K plays an important role in plant development by promoting the elongation of cells, water management of plants, and synthesis of carbohydrates. A sufficient K supply will enable strawberry plants to synthesize more sugar, resulting in sweeter strawberry fruit (Pettigrew 2008). Therefore, the management of N, P, and K nutrients is significant for strawberry production and promotion of the strawberry quality such as sweetness, firmness, and anthocyanin accumulation (Yoshida et al. 2000).
Previous studies have demonstrated the dynamics of nutrient uptake by strawberry plants grown in soil and soilless culture (Tagliavini et al. 2005). Besides, there have been some reports on strawberry nutrients under different stresses (Ipek et al. 2014; Kirnak et al. 2001). Nonetheless, less attention was paid to the difference of N, P, or K deficiency on strawberry planting. Therefore, this study investigated the phenotypic parameters, dynamic absorption of nutrients, and fruit yield under the stress of N, P, or K deficiency to better comprehend the importance of N, P, or K to strawberry. Our hypothesis is that the lack of N or P is more unfavorable to strawberry growth and development, compared with K. The study may help us provide more clues for improvement of nutrient management strategy in strawberry production.
Materials and Methods
Plant materials and growth conditions
The strawberry cultivar Santa was used as the research subject in this study. The plug strawberry seedlings were washed with clear water, and three leaves and short roots with a length of 3 to 5 cm were left. Before planting, the seedlings were soaked in the mixture of 1500-fold solution of 20% penthiopyrad and 1000-fold solution of 50% carbendazim for 8 min to prevent diseases and build up resistance.
The sand was washed with clean water, mixed with vermiculite at a ratio of 1:1 and put into cylindrical pots (130 mm × 110 mm × 90 mm; 0.88 kg planting regimens for each pot). One strawberry seedling was planted in each pot. The bottom of the pot was covered with double gauze to prevent leakage.
Experimental treatment
Pot experiments were conducted in a multispan greenhouse at Tongshan Experimental Station, Xuzhou Institute of Agricultural Sciences of Xuhuai District of Jiangsu Province (117°E, 34°N) from 8 Sep to 10 Dec 2021. Four treatments were set in the experiment, including complete nutrient solution (CN), nitrogen-deficient nutrient solution (ND), phosphorus-deficient nutrient solution (PD), and potassium-deficient nutrient solution (KD), and pure water irrigation was used as the control (CK). A total of 25 pots were used for each treatment. The nutrient solution was an improved formula of strawberry Yamazaki nutrient solution, whose pH was adjusted to 5.5 to 6.5. The specific macroelements are shown in Table 1. The components of trace elements are as follows: 0.2 mmol⋅L−1 FeSO4, 0.26 mmol⋅L−1 EDTA, 46 μmol⋅L−1 H3BO3, 10 μmol⋅L−1 MnSO4, 0.76 μmol⋅L−1 ZnSO4, 0.32 μmol⋅L−1 CuSO4, and 0.0162 μmol⋅L−1 (NH4)6Mo7O24. Seedlings with consistent growth were selected and shaded with black shade after planting for 7 d. Watering was conducted at 4:00 pm on a sunny day. Each pot was watered with 100 mL of nutrient solution. After twice nutrient solution watering, clear water was poured once to prevent salt damage.
Improved formula of strawberry Yamazaki nutrient solution.
Sampling for biochemical assays
Plant sampling was conducted at 7, 22, 33, 47, 56, 72, and 93 d after treatment, corresponding to seven stages, including seedling stage (1), vegetative growth stage I (2), vegetative growth stage II (3), vegetative growth stage III (4), flower bud differentiation stage (5), flowering stage (6), and fruiting stage (7), among which stages 1 to 4 were vegetative growth stages and 5 to 7 were reproductive growth stages. The whole plant was sampled, and the pot was placed upside down during sampling to carefully remove the attachment on the root system.
Indicators and methods
Determination of the strawberry phenotypic index.
S/R ratio is obtained by dividing shoot dry weight by root dry weight. Natural plant height is the distance from the base to the top of the plant under the natural state. Leaf area (including terminal leaf and leaflet) is calculated as follows: leaf length × leaf width × 0.75, and length and width were measured by ruler.
Determination of the strawberry TSS.
TSS was determined by the anthrone-sulfuric acid method with 0.1g dry fruit (Shimadzu Spectrophotometer ultraviolet-2450; SHIMADZU Inc., Tokyo, Japan).
Determination of the strawberry yield.
Yield per plant is the weight of total fruits in a plant. Single fruit weight is the weight of every fruit. All fruit weights were determined and the average yield per plant was calculated at the fruit stage.
Determination of the strawberry N-P-K content.
After washing and drying, the plant was divided into four parts, including the root, stem, leaf, and fruit, which were then respectively put into an oven for enzyme deactivation at 105 °C for 30 min, and the dry weight was measured after drying at 80 °C for 24 h. Subsequently, the tissues were ground and digested with H2SO4–H2O2, and used for the determination of mineral nutrient content. Total N was determined with the Kjeldahl nitrogen determination method (Kjeltec 8100; Foss Inc., Hilleroed, Denmark); the P content of the plants was estimated with the vanadomolybdate phosphoric acid method (Thermo Scientific Microplate Reader; Thermo Fisher Scientific Inc., Waltham, MA, USA) (Sharma and Sharma, 2019); and available K was determined by flame photometer (FP6410; PI Inc., Shanghai, China). Each treatment was repeated three times.
Statistical analysis
All data were analyzed through SPSS (IBM SPSS Statistics version 20.0; IBM Corp., Armonk, NY, USA), and the results were presented as the sample mean ± SD (n = 3). Statistical analysis was performed with the Duncan’s test at a significance level of P = 0.05. The figures and tables were generated with Microsoft Excel 2007.
Results
Symptoms and biomass allocation of strawberry under N, P, and K deficiency.
The N, P, and K deficiency symptoms of strawberry at fruiting stage are presented in Fig. 1. The strawberry plants cultured in CN (Fig. 1) were well developed, with compact plant structure, green leaves, plentiful and robust flower buds, plump fruit, and fairly well-distributed color. However, the strawberry plants cultured in nutrient-deficient solutions showed prominent symptoms of N, P, and K deficiency, respectively. Specifically, the strawberry plants cultured in ND (Fig. 1) exhibited small plant type, small and curled new leaves, chlorotic and margin-scorched old leaves, and disintegrated and meagre flower buds. The strawberry plants cultured in PD (Fig. 1) displayed small plant type, small and unstretched new leaves, dark green color, old leaves with a gradual outside-in purplish color, and undifferentiated flower buds. The strawberry plants cultured in KD (Fig. 1) showed obviously uneven fruit color. In terms of the CK group, the plants were characterized by the phenotype of both N and P deficiency, including small plant type, small and dense new leaves, yellow or purple old leaves, and undifferentiated flower buds.
Symptoms of nitrogen (N), phosphorus (P), and potassium (K) deficiency in strawberry at fruiting stage. CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
The response of plant biomass to N, P, and K deficiency is quite different (Fig. 2). In terms of the dry mass of root (DMR) (Fig. 2A), no significant difference was found among treatments in the vegetative growth period. The DMR under ND, PD, and CK treatments was lower than that under CN and KD treatments at the flowering stage, but significantly increased to be higher than that of CN and KD treatments at the fruiting stage. In terms of the dry mass of shoot (DMS) (Fig. 2B), it showed an increasing trend under all treatments except for the ND treatment, which exhibited a significant decrease from flower bud differentiation to flowering. In the reproductive period, KD and CN treatments resulted in significantly higher DMS than ND, PD and CK treatments. The results indicate that N and P deficiency are not conducive to shoot growth; and N deficiency is even worse. In contrast, K deficiency hinders root growth.
Biomass allocation of root and shoot in strawberry under nitrogen (N), phosphorus (P), and potassium (K) deficiency during the whole growth period. (A) Biomass allocation of root under N, P, and K deficiency. (B) Biomass allocation of shoot under N, P, and K deficiency. Bars represent the standard error of the mean n = 3. The abscissa number represents the sampling times. 1 = 7 d after treatment (seedling stage); 2 = 22 d after treatment (vegetative growth stage I); 3 = 33 d after treatment (vegetative growth stage II); 4 = 47 d after treatment (vegetative growth stage III); 5 = 56 d after treatment (flower bud differentiation stage); 6 = 72 d after treatment (flowering stage); 7 = 93 d after treatment (fruiting stage). CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
Dynamic absorption of N, P, and K in strawberry under different treatments.
In the whole growth period, the N content in the plant exhibited an upward trend (Fig. 3D), and the N allocation under different treatments followed the order of leaf > root > stem (Fig. 3A–C). The N content in the root under ND treatment was decreased at the fruiting stage, and the N content in the root under PD treatment was significantly higher than that under CN treatment at the reproductive growth stage (Fig. 3A). Besides, the N content in leaves under treatment with ND, PD, and KD was significantly lower than that under CN treatment at the fruiting stage (Fig. 3C). The N content in stems and leaves increased significantly at the vegetative growth stage I, whereas the N content in roots and leaves under all treatments decreased in the process of turning from vegetative growth to reproductive growth (Fig. 3A and C).
Dynamic absorption of nitrogen (N) in strawberry under N, phosphorus (P), and potassium (K) deficiency. (A) N content of root in different period under N, P, and K deficiency. (B) N content of stem in different period under N, P, and K deficiency. (C) N content of leaf in different period under N, P, and K deficiency. (D) N content of the whole plant in different period under N, P, and K deficiency. Bars represent the standard error of the mean, n = 3. The abscissa number represents the sampling times. 1 = 7 d after treatment (seedling stage); 2 = 22 d after treatment (vegetative growth stage I); 3 = 33 d after treatment (vegetative growth stage II); 4 = 47 d after treatment (vegetative growth stage III); 5 = 56 d after treatment (flower bud differentiation stage); 6 = 72 d after treatment (flowering stage); 7 = 93 d after treatment (fruiting stage). CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
Throughout the whole growth period, the P content in each tissue under PD and CK treatments was significantly lower than that under CN treatment, whereas that under ND treatment was always at high levels (Fig. 4A–C). Interestingly, the P content was at a lower level under ND treatment at the flowering stage, and in the whole plant under KD treatment decreased significantly from the flowering stage to the fruiting stage (Fig. 4D).
Dynamic absorption of phosphorous (P) in strawberry under nitrogen (N), P, and potassium (K) deficiency. (A) P content of root in different period under N, P, and K deficiency. (B) P content of stem in different period under N, P, and K deficiency. (C) P content of leaf in different period under N, P, and K deficiency. (D) P content of the whole plant in different period under N, P, and K deficiency. Bars represent the standard error of the mean, n = 3. The abscissa number represents the sampling times. 1 = 7 d after treatment (seedling stage); 2 = 22 d after treatment (vegetative growth stage I); 3 = 33 d after treatment (vegetative growth stage II); 4 = 47 d after treatment (vegetative growth stage III); 5 = 56 d after treatment (flower bud differentiation stage); 6 = 72 d after treatment (flowering stage); 7 = 93 d after treatment (fruiting stage). CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
In the whole growth period, the K content in the whole plant exhibited an upward trend (Fig. 5D), and the K allocation under different treatments followed the order of stem > leaf > root (Fig. 5A–C). More interestingly, the K content in all tissues under PD treatment was significantly lower than that under CN treatment. These results indicated that lack of P inhibits the absorption and utilization of K in the reproductive growth period. In addition, the K content in the whole plant under ND, PD, and CK treatments was significantly lower than that under CN treatment at the flowering and fruiting stage (Fig. 5D).
Dynamic absorption of potassium (K) in strawberry under nitrogen (N), phosphorus (P), and K deficiency. (A) K content of root in different period under N, P, and K deficiency. (B) K content of stem in different period under N, P, and K deficiency. (C) K content of leaf in different period under N, P, and K deficiency. (D) K content of the whole plant in different period under N, P, and K deficiency. Bars represent the standard error of the mean, n = 3. The abscissa number represents the sampling times. 1 = 7 d after treatment (seedling stage); 2 = 22 d after treatment (vegetative growth stage I); 3 = 33 d after treatment (vegetative growth stage II); 4 = 47 d after treatment (vegetative growth stage III); 5 = 56 d after treatment (flower bud differentiation stage); 6 = 72 d after treatment (flowering stage); 7 = 93 d after treatment (fruiting stage). CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
Growth traits of strawberry at vegetative and reproductive growth stage under different nutrient deficiency treatments.
Vegetative and reproductive growth are two important stages in the process of plant growth and development. Table 2 shows the growth characteristic parameters at the vegetative and reproductive growth stages. The S/R ratio can represent the relationship between the growth of the shoot and root. The S/R ratio under CN and KD treatments was significantly higher than that under ND and CK treatments at the vegetative growth stage, whereas no obvious difference in S/R ratio was observed among different treatments at the reproductive growth stage. However, the S/R ratio under ND and CK treatments at the reproductive growth stage was higher than that at the vegetative growth stage, while it was the opposite case for the CN, PD, and KD treatments, which means that N is closely related to the transformation from vegetative growth to reproductive growth. When changing from vegetative growth to reproductive growth, strawberry plants showed increases in the area of apical leaves and shoulder leaves, as well as an increase in natural plant height. The leaf area and natural plant height under all nutrient deficiency treatments except for the KD treatment were significantly lower than those of CN treatment.
Effects of different nutrient deficiency on growth traits of strawberry at vegetative and reproductive growth phase.
Yield and quality of strawberry under different nutrient deficiency treatments.
Unexpectedly, the strawberry fruit treated with PD showed the highest content of N, indicating that P deficiency promotes the absorption of N by strawberry fruit. Surprisingly, the K content was not significantly different between KD and CN treatments, but significantly different between PD and CN treatments, suggesting that K deficiency has no obvious effect on K content in strawberry fruit, while P deficiency inhibits the absorption of K by the fruit. The average yield per plant under all nutrient deficiency treatments except for KD was significantly reduced compared with that under CN treatment. These results indicated that K deficiency has no obvious effect on fruit yield, whereas N and P play an important role in strawberry fruit growth and development. Compared with the CN treatment, the PD and CK treatments significantly decreased the TSS content in strawberry fruit, whereas the ND and KD treatments resulted in no significant difference. These results indicated that the application of P plays an important role in sugar metabolism in strawberry fruit.
It can be seen from Table 3 that there is no significant difference in average yield between CN treatment and KD treatment. To study the effect of K deficiency on the weight of single fruit, a box plot was drawn. As shown in Fig. 6, the single fruit weight of strawberry treated with ND, PD, and CK was significantly lower than that treated with CN and KD, all of which were below 8 g. These results showed that the lack of N and P has a great influence on the weight of strawberry fruit. Compared with the CN treatment, K deficiency showed no obvious effect on strawberry fruit yield and soluble sugar content (Table 3). Interestingly, the single fruit weight of strawberry under KD treatment ranged from 8 to 12 g, and that of strawberry under CN treatment was 10 to 16 g (Fig. 6). The results indicated that K deficiency does not affect the overall yield of strawberry fruit, but can reduce the single fruit weight.
Effects of different nutrient deficiency on yield and quality of strawberry.
Distribution of single fruit weight of strawberry under different nutrient deficiency treatments. CK = control; CN = complete nutrient solution; KD = potassium-deficient nutrient solution; ND = nitrogen-deficient nutrient solution; PD = phosphorus-deficient nutrient solution.
Citation: HortScience 58, 6; 10.21273/HORTSCI17086-23
Discussion
Effect of N deficiency on growth and development of strawberry.
The growth and development of strawberry were significantly inhibited by N deficiency as indicated by the reduced dry weight at the reproductive growth stage. The ND-treated plants showed small plant type, small new leaves, and curled, chlorotic, and margin-scorched old leaves (Fig. 1). These findings are similar to previous reports (Huang et al. 2020; Tucker 1984; Uchida 2000). The S/R ratio of strawberry plants was significantly affected by N deficiency. The S/R ratio under ND treatment at the vegetative growth stage was lowest in all treatments (Table 2). Many studies have shown that a higher S/R ratio in the early stage are beneficial to the increase in yield (Ågren and Ingestad 1987; Sainju et al. 2017), which means that the large and fine root system in the early stage is beneficial to the growth and development of the plant in the later stage. Without doubt, N deficiency reduces the yield and N content (Varvel et al. 1997). The N content (Fig. 3) and yield (Table 3) of strawberry under ND treatment had no difference from those under CK treatment, indicating the importance of N to plant growth and development.
Effect of P deficiency on growth and development of strawberry.
The strawberry plants cultured in PD solution showed obvious symptoms of gradually outside-in purplish old leaves and undifferentiated flower buds (Fig. 1). P demand increases at the flowering stage (Ye et al. 2019). Inadequate supply of P can affect the synthesis of nucleic acids, thereby inhibiting the growth and development of crops and delaying the growth period (Malhotra et al. 2018). The older leaves acquire a purplish pigmentation due to the synthesis of more anthocyanins under limited P conditions (Li et al. 2014b). As previously reported (Abel et al. 2002), plants respond to P deficiency by decreasing the S/R ratio to allow a more thorough exploitation of P resources. In the present study, the S/R ratio of strawberry decreased from the vegetative growth stage to the reproductive growth stage (Table 2). P and N have been found to have a synergistic interaction (Zeng et al. 2016); however, this study showed that at the reproductive growth stage, the content of N was high in roots and fruit under PD treatment (Fig. 3). With the decline of P level, the absorption efficiency of plants for K decreased significantly. In this study, the K content in all tissues under PD treatment decreased at the reproductive growth stage and was significantly lower than that under CN treatment (Fig. 5), indicating that lack of P inhibits the absorption and utilization of K, which was also reported in other studies (Malvi 2011). The improving effect of P on fruit quality cannot be underestimated. Previous studies have indicated that application of P fertilizer can increase soluble sugar concentrations by improving sucrose metabolism and sink strength in fruit due to the upregulated activities of sucrose-degrading and sucrose-synthesizing enzymes (Dayal et al. 2004; Wu et al. 2021). Compared with CN treatment, PD treatment significantly decreased the soluble sugar content of fruit in the present study.
Effect of K deficiency on growth and development of strawberry.
Unexpectedly, K deficiency had little obvious effect on seedling growth of strawberry, but the following three findings are noteworthy. First, different from N and P deficiency treatments, the KD treatment resulted in almost the same phenotype and even higher DMS compared with that under CN treatment (Figs. 1 and 2). One reason may be that K deficiency is associated with stomatal closure, which lowers the transpiration rate and thus elevates the dry matter percentage in plant tissues (Hsiao and Lauchli 1986). Second, strawberry plants cultured in KD solution showed a visual symptom of uneven fruit color (Fig. 1). Consistently, in tomato, adequate K supply can improve the fruit quality since it alleviates several color disorders in tomato fruit (Hernández-Pérez et al. 2020). In a final note, the results showed that the lack of K does not affect the overall yield, but reduces the single fruit weight. The finding is similar to that of Zhong et al. (2018), who reported that plants supplied with 0.1 mm K had a decrease in single fruit weight of all plants. Therefore, K deficiency is not conducive to the formation of high-quality commercial fruits.
Conclusion
Obvious phenotypic changes were observed on strawberry under the treatment of N and P deficiency. N deficiency greatly reduced S/R ratio, especially the shoot biomass. As a result, the growth and development of strawberry plants was blocked and stunted. P deficiency greatly increased the N content but decreased K content in strawberry plants, which means P is of advantage to regulate the absorption and utilization of N and K nutrients in plants. Meanwhile, P has a profound influence on fruit quality, such as TSS content. K deficiency is not conducive to fruit coloring and the formation of high-quality commercial fruits. In summary, N is beneficial to accumulation of shoot biomass; P is beneficial to regulation of nutrients; and K is beneficial to fruit coloring. These results provide important reference for growth characteristics, nutrient content, and fruit quality of strawberry plants under different nutrient deficiency conditions.
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