How Phosphorus Fertilization Alleviates the Effect of Salinity on Sugar Beet ( Beta vulgaris L.) Productivity and Quality

: Salinity is a major problem affecting agriculture in many regions of the world, including Morocco. The best agronomic practices such as fertilization are used to cope with salinity stress and improve productivity under saline conditions. The objective of this study is to evaluate the interactive effect of phosphorus and salinity on sugar beet ( Beta vulgaris L.) cv. “Sporta” productivity and quality. A ﬁeld experiment was carried out, testing three levels of irrigation water salinity (ECw = 0.7; 4, 8, and 12 dS · m − 1 ) and three levels of phosphorus (100, 120, and 140 kg P 2 O 5 · ha − 1 ) organized in a split-plot design with three replicates. This research was conducted in the Tadla region (center of Morocco) during two seasons in 2019 and 2020. The obtained results show that irrigation water salinity had a negative effect on most growth and productivity parameters. For instance, sugar beet yield reduced by 21% and by 26% under saline irrigation, with an EC value equal to 4 and 8 dS · m − 1 , respectively, compared to the control during the 2018–2019 season, and by 1%, 19%, and 27% under saline irrigation, with an EC value equal to 4 and 8 and 12 dS · m − 1 , respectively compared to the control (0.7 dS · m − 1 ) during the 2019–2020 season. Total sugar content was signiﬁcantly increased by 5% and 7%, respectively, under saline irrigation, with an EC value of 4 and 8 dS · m − 1 , respectively, as compared with the control in the ﬁrst growing season in 2018–2019. However, in the second growing season (2019–2020), only the highest level of saline water (EC = 12 dS · m − 1 ) signiﬁcantly increased in sugar content by 15% compared to the control. Regarding the P fertilization effect, it was found that a P rate of 120 kg P 2 O 5 · ha − 1 was enough to improve the yield and sugar content of sugar beet under the tested salinity levels. Thus, P fertilization could be one of the best practices to enhance sugar beets’ tolerance of salinity. To obtain a maximum root and sugar yield under saline water, it is recommended to apply a phosphorus dose of 120 kg P 2 O 5 · ha − 1 .


Introduction
Salinity is a major problem that affects agricultural productivity by reducing the crop yield of a wide range of crop species in several regions of the world [1,2], and therefore, it affects agricultural production and income worldwide [3]. Salinization is continuously increasing in many parts of the world and has become a serious environmental problem facing the population, especially in arid regions. It has been estimated that more than half of agricultural lands could be salinized by the year 2050, mainly due to secondary salinization induced by human activity [4].
Estimates indicate that 50% of the irrigated land in some regions in North Africa has been affected by salinity [5]. Currently in Morocco, salinity affects about 350,000 ha of arable lands [6]. The Tadla plain is one of the main agricultural zones in Morocco affected

Experimental Site
This research was conducted between December 2018 and July 2020 at an experimental farm of the National Institute of Agronomic Research (INRA) in Tadla, Morocco (X = 32.2 • ; Y = 6.31 ; Z = 450 m). The soil was classified as Chromic Luvisols [30]. The climate is arid with an irregular rainfall averaging 278 mm. The average temperature is 18 • C, with a maximum in August that often exceeds 35 • C and a minimum in January of approximately 0 • C (Figure 1).

Experimental Site
This research was conducted between December 2018 and July 2020 at an experimental farm of the National Institute of Agronomic Research (INRA) in Tadla, Morocco (X = 32.2°; Y = 6.31′; Z = 450 m). The soil was classified as Chromic Luvisols [30]. The climate is arid with an irregular rainfall averaging 278 mm. The average temperature is 18 °C, with a maximum in August that often exceeds 35 °C and a minimum in January of approximately 0 °C (Figure 1).

Trial Set-Up
The field experiment was conducted in a split-plot design with three replicates applying four irrigation water salinity levels and three P fertilization rates. The tested salinity levels were freshwater with an EC value of 0.7 dS·m −1 and two levels of saline water with an EC value of 4 and 8 dS·m −1 in the 2018-2019 season and freshwater with an EC value of 0.7 dS·m −1 with three levels of saline water with an EC value of 4, 8, and 12 dS·m −1 in the 2019-2012 season. The high-salinity treatment of 12 dS·m −1 was added in the second season to evaluate the sugar beet responses to a high salinity level beyond its tolerance threshold (7-8 dS·m −1 ). Salinity levels were achieved by adding salt (NaCl) to freshwater. The P fertilization rate consisted of 100 (recommended dose used by farmers), 120, and 140 kg P2O5.ha −1 . The area of each plot was 20 m 2 (4 m × 5 m), and each consisted of six rows with a 50 cm interline. P was supplied under the form of triple superphosphate (45% of P2O5), which is commonly used in the region. Phosphorus fertilizer was incorporated into the soil before sowing. The tested variety of sugar beet was "Sporta", which was shown to be a salt-tolerant variety.
Other fertilizer requirements were applied equally for all treatments through fertigation with a drip irrigation system. Irrigation with saline water started 60 days after planting, and the crop was irrigated daily until harvest (1 June 2020) following the evapotranspiration method (ET0). Sugar beet was sown in December 2018 and harvested on 1 July 2019 for the first season, while in the second season, it was sown on 31 October 2019 and harvested on 1 June 2020. The recommended seed rate of 100,000 seeds per ha for sugar beets was used. Thinning of plants (two per hole) was performed before the treatment

Trial Set-Up
The field experiment was conducted in a split-plot design with three replicates applying four irrigation water salinity levels and three P fertilization rates. The tested salinity levels were freshwater with an EC value of 0.7 dS·m −1 and two levels of saline water with an EC value of 4 and 8 dS·m −1 in the 2018-2019 season and freshwater with an EC value of 0.7 dS·m −1 with three levels of saline water with an EC value of 4, 8, and 12 dS·m −1 in the 2019-2012 season. The high-salinity treatment of 12 dS·m −1 was added in the second season to evaluate the sugar beet responses to a high salinity level beyond its tolerance threshold (7-8 dS·m −1 ). Salinity levels were achieved by adding salt (NaCl) to freshwater. The P fertilization rate consisted of 100 (recommended dose used by farmers), 120, and 140 kg P 2 O 5 .ha −1 . The area of each plot was 20 m 2 (4 m × 5 m), and each consisted of six rows with a 50 cm interline. P was supplied under the form of triple superphosphate (45% of P 2 O 5 ), which is commonly used in the region. Phosphorus fertilizer was incorporated into the soil before sowing. The tested variety of sugar beet was "Sporta", which was shown to be a salt-tolerant variety.
Other fertilizer requirements were applied equally for all treatments through fertigation with a drip irrigation system. Irrigation with saline water started 60 days after planting, and the crop was irrigated daily until harvest (1 June 2020) following the evapotranspiration method (ET0). Sugar beet was sown in December 2018 and harvested on 1 July 2019 for the first season, while in the second season, it was sown on 31 October 2019 and harvested on 1 June 2020. The recommended seed rate of 100,000 seeds per ha for sugar beets was used. Thinning of plants (two per hole) was performed before the treatment application. During preparation and plant growth, the soil was supplemented with ammonium sulfate using a rate of 200 kg·ha −1 of nitrogen.

Physical and Chemical Analysis
Before sowing, the physical and chemical soil characteristics of two soil depths were determined according to Jackson [31]. The soil analysis results are reported in Table 1. The electrical conductivity of the soil was measured using the soil-saturated paste method with an EC meter (HI 9812, Hanna Instruments, Casablanca, Morocco). The ECe values were relatively low, which classed the soils as being nonsaline [32].

Yield Parameters
Sugar beet root yield was measured at harvest using the whole plot area (m 2 ) and then extrapolated to t·ha −1 . Yield components, including root weight, length, and diameter, were determined using values from four plants per plot.

Sugar Content Determination
Sugar content (% pol) was determined using the procedure described by Reinefeld et al. [33].

Stomatal Conductance Measurements
Stomatal conductance was measured using the SC-1 Leaf Porometer (Decagon Devices, Inc., Pullman, WA, USA). The stomatal conductance was determined between 10 a.m. and 12 p.m. on the upper leaf surface well exposed to sunlight. Three measurements per plant were carried out for four plants per plot once for each season.

Statistical Analysis
Statistical analysis was carried out using SPSS 17.0 software. A two-way analysis of variance (ANOVA) was used to assess the effects of both salinity and phosphorus on monitored parameters. The level of significance was set to p < 0.05.
For each analysis, when ANOVA was significant, statistically significant differences between means were identified using Tukey's test (p ≤ 0.05). Figure 2 presents the obtained average results recorded in both seasons in terms of final growth parameters, including fresh root weight per plant, root length, root width, number of leaves per plant, leaf area, and fresh weight of leaves per plant subjected to the combined effect of both salinity and P application. It is obvious that salinity negatively affected most investigated parameters (p < 0.05), except the root length, where there was no significant difference between salinity levels, and the number of leaves per plant, where the highest level of salinity resulted in increased leaves number but with a lower leaf area. However, P application differently affected the investigated parameters depending on the salinity level. For instance, P application negatively affected (p < 0.05) all investigated parameters except for root length under control conditions, where a P application of 140 kg·ha −1 significantly increased this parameter. Phosphorus treatments under the same salinity level without a common letter are significantly different at p < 0.05.

Sugar Beet Yield
Statistical analysis indicated that the irrigation water salinity had a highly significant effect on the root yield in both seasons (p < 0.01), but the interaction between salinity and

Sugar Beet Yield
Statistical analysis indicated that the irrigation water salinity had a highly significant effect on the root yield in both seasons (p < 0.01), but the interaction between salinity and phosphorus was not significant (Figure 3). During the 2018-2019 season, salinity significantly reduced (p = 0.003) the root yield by 21% and by 26% under saline irrigation with an EC value equal to 4 and 8 dS·m −1 , respectively, compared to the control. Sugar beet yield responded positively to an additional supply of P fertilization under freshwater conditions and increased by 11% and 17% under a P application rate of 120 and 140 kg·ha −1 of P 2 O 5 , respectively, compared to the control (100 kg·ha −1 of P 2 O 5 ). Similar results were recorded at low salinity (ECw = 4 dS·m −1 ). The addition of phosphorus supply using a rate equal to 120 and 140 kg·ha −1 of P 2 O 5 increased the yield by 8% and 7.5%, respectively. At high salinity (8 dS·m −1 ), only a P application of 120 kg·ha −1 of P 2 O 5 increased the root yield of sugar beets by 7.5%, which indicates that the optimal phosphorus application for sugar beets under high salinity should not exceed 120 kg·ha −1 of P 2 O 5 .
Agronomy 2021, 11, x FOR PEER REVIEW 6 of 12 phosphorus was not significant (Figure 3). During the 2018-2019 season, salinity significantly reduced (p = 0.003) the root yield by 21% and by 26% under saline irrigation with an EC value equal to 4 and 8 dS·m −1 , respectively, compared to the control. Sugar beet yield responded positively to an additional supply of P fertilization under freshwater conditions and increased by 11% and 17% under a P application rate of 120 and 140 kg·ha −1 of P2O5, respectively, compared to the control (100 kg·ha −1 of P2O5). Similar results were recorded at low salinity (ECw = 4 dS·m −1 ). The addition of phosphorus supply using a rate equal to 120 and 140 kg·ha −1 of P2O5 increased the yield by 8% and 7.5%, respectively. At high salinity (8 dS·m −1 ), only a P application of 120 kg·ha −1 of P2O5 increased the root yield of sugar beets by 7.5%, which indicates that the optimal phosphorus application for sugar beets under high salinity should not exceed 120 kg·ha −1 of P2O5. During the second growing season (2019-2020), the salinity significantly reduced (p = 0.002) the root yield by 1%, 19%, and 27% under saline irrigation with an EC value equal to 4 and 8 and 12 dS·m −1 , respectively, compared to the control (0.7 dS·m −1 ). Under a high salinity level (12 dS·m −1 ), the phosphorus supply significantly increased (p = 0.04) the yield of sugar beets by 19 and 13% under a P application rate of 120 and 140 kg·ha −1 of P2O5, respectively, compared to the control (100 kg·ha −1 of P2O5).  Figure 4 shows the variation of the total sugar content of sugar beet under both salinity and P fertilization. During the first growing season (2018-2019), total sugar content was significantly increased by 5% and 7% under saline irrigation with an EC value of 4 and 8 dS·m −1 , respectively, as compared with the control (p = 0.04). However, in the second growing season (2019-2020), only the highest level of saline water (EC = 12 dS·m −1 ) significantly increased the sugar content by 15% compared to the control.

Sugar Content of the Roots
During the 2018-2019 season, P application had no effect on total sugar content (p = 0.4), while in the 2019-2020 season, the sugar beet plants were able to produce more sugar content in their roots. In fact, increased P application significantly improved (p > 0.05) the sugar content compared to the control (100 kg of P2O5·ha −1 ) under all tested salinity levels,   During the second growing season (2019-2020), the salinity significantly reduced (p = 0.002) the root yield by 1%, 19%, and 27% under saline irrigation with an EC value equal to 4 and 8 and 12 dS·m −1 , respectively, compared to the control (0.7 dS·m −1 ). Under a high salinity level (12 dS·m −1 ), the phosphorus supply significantly increased (p = 0.04) the yield of sugar beets by 19 and 13% under a P application rate of 120 and 140 kg·ha −1 of P 2 O 5 , respectively, compared to the control (100 kg·ha −1 of P 2 O 5 ). Figure 4 shows the variation of the total sugar content of sugar beet under both salinity and P fertilization. During the first growing season (2018-2019), total sugar content was significantly increased by 5% and 7% under saline irrigation with an EC value of 4 and 8 dS·m −1 , respectively, as compared with the control (p = 0.04). However, in the second growing season (2019-2020), only the highest level of saline water (EC = 12 dS·m −1 ) significantly increased the sugar content by 15% compared to the control.

Sugar Content of the Roots
White sugar yield (root yield × total sugar content) was also significantly affected by salinity level (p < 0.01). In fact, in the 2018-2019 season, it was reduced by 18 and 20% under 4 and 8 dS·m −1 , respectively, compared to the control, while in the 2019-2020 season, white sugar yield increased by 2% under 4 dS·m −1 and reduced by 16% under both 8 and 12 dS·m −1 . Regarding the P application effect on white sugar yield, a rate of 120 kg of P2O5·ha −1 provided the highest yield under all salinity levels in both growing seasons.

Stomatal Conductance
Average data of stomatal conductance of both seasons are shown in Figure 5. The stomatal conductance significantly decreased under salinity conditions (p < 0.01). However, the phosphorus tended to increase the stomatal conductance of sugar beets, especially under saline irrigation, with an EC value equal to 4 and 12 dS·m −1 , while P application had no effect under irrigation with an EC value equal to 0.7 and 8 dS·m −1 .   During the 2018-2019 season, P application had no effect on total sugar content (p = 0.4), while in the 2019-2020 season, the sugar beet plants were able to produce more sugar content in their roots. In fact, increased P application significantly improved (p > 0.05) the sugar content compared to the control (100 kg of P 2 O 5 ·ha −1 ) under all tested salinity levels, and a maximum sugar content was observed for all salinity treatments under 120 kg of P 2 O 5 ·ha −1 .
White sugar yield (root yield × total sugar content) was also significantly affected by salinity level (p < 0.01). In fact, in the 2018-2019 season, it was reduced by 18 and 20% under 4 and 8 dS·m −1 , respectively, compared to the control, while in the 2019-2020 season, white sugar yield increased by 2% under 4 dS·m −1 and reduced by 16% under both 8 and 12 dS·m −1 . Regarding the P application effect on white sugar yield, a rate of 120 kg of P 2 O 5 ·ha −1 provided the highest yield under all salinity levels in both growing seasons.

Stomatal Conductance
Average data of stomatal conductance of both seasons are shown in Figure 5. The stomatal conductance significantly decreased under salinity conditions (p < 0.01). However, the phosphorus tended to increase the stomatal conductance of sugar beets, especially under saline irrigation, with an EC value equal to 4 and 12 dS·m −1 , while P application had no effect under irrigation with an EC value equal to 0.7 and 8 dS·m −1 .

Discussion
Sugar beet (Beta vulgaris L.) is known to be a salt-tolerant crop. Its salt-tolerance threshold was reported to be between 7 and 9 dS·m −1 [34,35], and it can be grown under moderately saline conditions [36]. It is highly salt-tolerant during vegetative growth [37]. Plant species have variable responses to salinity in terms of their growth and productivity. Crop and forage species can be classified according to their salt tolerance (or sensitivity) based on two parameters: the threshold ECw and the slope, i.e., percentage of yield reduction per unit of ECw. The ECw threshold is defined as the salinity level that does not significantly reduce the yield and at which the yield starts to decrease. According to this approach, sugar beet was classified as a salt-tolerant species, with an EC threshold of 7.0 dS·m −1 [28]. Moreover, it is well documented that various genotypes respond differently to salt stress, which means that the EC threshold can be less or more than 7 dS·m −1 [38,39].
In this study, we investigated the combined effect of salinity and P fertilization on the growth and productivity of sugar beet. In this study, salinity reduced most growth and productivity parameters, which can be explained by the inhibition of photosynthetic activity, sugar synthesis and translocation, and cell elongation [9]. Our findings clearly indicate that salinity reduced the fresh root weight, root length, leaf area, and fresh weight of leaves, while it increased the number of leaves per plant. Similar results were obtained by Ghoulam et al. [40], who found that an increased Na + concentration led to a great reduction in growth parameters such as leaf area and leaf and root weight, while the leaf number was less affected by the increased salinity level; therefore, it seems that the reduction of leaf area and keeping the same number of leaves is one of the adaptation strategies adopted by sugar beet to cope with salinity stress. Jamil et al. [38] also showed that salinity significantly reduced the leaf area of sugar beet.
The findings of this study indicate that irrigation water salinity had a significant effect on the root yield of sugar beets. The obtained data from the first season (2018-2019) show that salinity significantly decreased the root yield by 21% and 26% under saline irrigation, with an EC value equal to 4 and 8 dS·m −1 , respectively, compared to the control. The results are similar to the findings of Zaki et al. [41] and Khafagi and El-Lawandy [42], who reported that soil salinity may lead to a reduction in terms of sugar beet yield. Moreover, it has been confirmed that salinity significantly reduces root and shoot growth, as well as biomass accumulation [43]. Our results are in agreement with those recorded by Eid and Ibrahim [44], who reported that irrigating sugar beet crops with drainage water with an EC value equal to 3.8 dS·m −1 reduced root and sugar yield by about 21% and 42% compared to freshwater (0.5 dS·m −1 ).
Our findings are also in line with the previous findings of Zaki et al. [41], who reported that sugar yield is reduced due to absorbed Na + ions. Similarly, it was demonstrated by Çimrin et al. [45] that salinity stress reduced root and shoot biomass accumulation. The negative effect of salinity on root yield is probably due to the osmotic inhibition of water absorption due to the high salt concentration in the soil, the accumulation of certain ions such as Na + and Cl − in high concentrations in plant cells, the disruption of the mineral balance of plants [42], or the reduction in photosynthetic activity and carbohydrate metabolism [43]. The reduction in beet yield was possibly due to reduced water and nutrient uptake under a high-salinity environment [46]. Contrarily, it was reported by Moreno et al. [34] that beet and sugar yields were significantly increased under irrigation with saline water (5.9-7.0 dS·m −1 ) compared to non saline irrigation (1.7 dS·m −1 ). Another study also found that the root weight of some cultivars of sugar beet plants increased with a mild level of water salinity (EC = 5.5 dS·m −1 ) [47]. Contrarily, Feizi et al. [48] reported that the irrigation water salinity with an EC value up to 12.3 dS·m −1 had no significant effect on the root yield of sugar beets.
Regarding the P fertilization effect on sugar beet yield, our finding suggests that under salinity, a P fertilization rate of 120 kg of P 2 O 5 ·ha −1 resulted in a yield increase. In fact, it is well known that P fertilization improves crop yield under salinity conditions. For instance, Hussain et al. [49] reported that the addition of 60 and 120 kg of P 2 O 5 ·ha −1 increased sugar beet yield under salinity (3 dS·m −1 ) by 37 and 47% over control (0 kg of P 2 O 5 ·ha −1 ). In another study conducted by Khan et al. [50], it was reported that increasing rates of P fertilization increased root, sugar yields, and root sucrose content. El-Tilib et al. [51] reported that P fertilization resulted in a significant increase in cane and sugar yields. Bargaz et al. [52] suggested adequate P fertilization under salinity conditions is likely a promising strategy to improve salinity tolerance and productivity of P. vulgaris, a response relationship that seems to be P-rate dependent.
An increase in sugar content was observed due to increased irrigation water salinity. In fact, during the first season (2018-2019), this parameter increased by about 5 and 7% under saline irrigation with an EC value equal to 4 and 8 dS·m −1 , respectively, compared to the control. Our results are well aligned with those reported by Hajiboland et al. [47], who showed that salinity increased the sugar content in sugar beets. Moreover, it was reported by Abdel-Mawly and Zanouny [53] that total soluble sugar (TSS) in the root of sugar beets increased with an increasing level of irrigation water salinity. The increase in TSS may be due to more salt absorption by plants under increased salinity levels, which consequently decreases purity and negatively affects the refinable sugar percentage. The increase in sugar content is mainly explained by the osmotic adjustment phenomenon to maintain equilibrium between the vacuole and cell cytoplasm to allow water uptake. In fact, plants accumulate compatible solutes such as soluble sugars in the cell cytoplasm to cope with salt-induced water stress [54]. In some plants, in response to salt stress, the accumulation of sugars is considered an important mechanism in osmotic adjustment [55]. An efficient accumulation of sugar in the sugar beet roots is linked to the effect of plant growth regulators in the anatomy modification of storage roots with increasing effects on sucrose concentration [56]. However, it was reported by El-Maghraby et al. [57] and Khalil et al. [58] that sucrose, TSS, and the purity of sugar beet juice increased with increasing K levels but reduced due to salinity stress.
The obtained results regarding sugar content show that sugar beet plants were able to produce more sugar content in their roots under phosphorus supply at all salinity levels, including the control. On other hand, it was reported by Shahriaripour et al. [59] that sugar content in pistachio seedlings was reduced by applying phosphorus.
The stomatal conductance was significantly reduced under saline irrigation. However, phosphorus tends to increase the stomatal conductance of sugar beets under EC 4 and 12 dS·m −1 , but this effect is not significant. Katerji et al. [29] reported that the stomatal conductance of sugar beet was negatively affected by increased salinity, and sugar beet cultivated under saline conditions was able to maintain production under severe water stress. Furthermore, the evapotranspiration and yield of sugar beet were slightly decreased due to salinity because of the slight reduction in leaf area and the maintenance of photosynthetic activity under saline conditions. The finding of an experiment carried out by Dadkhah [60], who investigated the effect of several salinity levels reaching 350 mM of NaCl in sugar beet, suggested that net photosynthesis and stomatal conductance (gs) were greatly and negatively affected by increased salinity, whereas leaves from plants exposed to 50 mM salinity showed little change in photosynthesis, whereas the photosynthetic rates of leaves treated by high levels of salinity had up to a 91.5% reduction with an increase in the CO 2 compensation point. Regarding other species, it was reported by Zribi et al. [61] that pepper's stomatal conductance was significantly reduced under the effect of salt stress. These results agree with those obtained with peppers [37] and tomatoes [62], which reported that salinity can inhibit and reduce net photosynthesis and stomatal conductance due to a decline of the CO 2 supply, resulting from the partial closure of the stomata either by disrupting the biochemical mechanism of CO 2 fixation or by both mechanisms.

Conclusions
The findings of our study reveal that the irrigation water salinity increment led to significant reductions in the sugar beet growth, yield, root weight, and white sugar yield. However, the sugar content was improved under increased salinity. On the other hand, P fertilization was shown to improve sugar yield and content as well as stomatal conductance under most of the salinity conditions tested. Therefore, the phosphorus supply can reduce the adverse effects of high salinity on plant growth and physiological development. In light of the results obtained, P fertilization could be one of the best practices to enhance sugar beets' tolerance of salinity. Thus, to obtain a maximum root and sugar yield under saline water, application of a phosphorus dose of 120 kg of P2O5·ha -1 may be recommended.