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Plant growth regulators improve the yield of white lupin (Lupinus albus) by enhancing the plant morpho-physiological functions and photosynthesis under salt stress

BMC Plant Biology volume 24, Article number: 1020 (2024) Cite this article

Abstract

Background

White lupin (Lupinus albus L.) is a multi-purpose, climate resilient, pulse crop with exceptionally high protein content that makes it a suitable alternative of soybean in livestock feed. Although white lupin grows well on marginal sandy soils, previous studies have reported its sensitivity towards salinity stress. This experiment aims to assess the influence of salinity stress and mitigating role of plant growth regulators (PGRs) on performance of white lupin.

Methodology

The white lupin plants were sown in pots maintained at three salinity levels (1, 3 and 4.5 dS m− 1) throughout the growing season and foliar sprayed with different PGRs, including ascorbic acid, potassium chloride, boric acid, ammonium molybdate and methionine at sowing, four weeks after emergence and at the initiation of flowering. Foliar spray of distilled water and salinity level of 1 dS m− 1 were maintained as control treatments. Data were recorded for seed germination indices, plant growth, antioxidant enzymes and photosynthetic efficiency variables.

Results

The severe salinity stress (4.5 dS m− 1) reduced the germination indices by 9–50%, plant growth traits by 26–54%, root nodulation by 12–26%, grain development by 44–53%, antioxidant enzymes activity by 13–153% and photosynthetic attributes by 1–8% compared to control (1 dS m− 1). Different PGRs improved several morpho-physiological attributes in a varied manner. The application of potassium chloride improved seed vigour index by 53%, while ascorbic acid improved root nodulation by 12% and number of pods per cluster by 75% at the severe salinity level. The foliar application of PGRs also displayed a recovery of 140% in the activity of superoxide dismutase and 70% in catalase. The application of multi zinc displayed an improvement of 37% in plant relative chlorophyll, while ascorbic acid brought an increase of 25% in non-photochemical quenching and 21% in photochemical quenching coefficient at the severe salinity level. On contrary, the application of PGRs brought a relatively modest improvement (8–13%) in quantum yield of photosystem II at slight to moderate (3 dS m− 1) salinity stress. The correlation analysis confirmed a partial contribution of leaf area and seed vigour index to overall photosynthetic efficiency of white lupin.

Conclusions

Clearly, salinity exerted a negative impact on white lupin through a decline in chlorophyll content, activity of antioxidant enzymes and efficiency of photosynthetic apparatus. However,  PGRs, especially ascorbic acid and potassium chloride considerably improved white lupin growth and development by mitigating the negative effects of salinity stress.

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Background

White lupin is one of several species of the pea family (Fabaceae) domesticated as a pulse crops for their use in human food and stock feed before 2000 BC [1, 2]. Over 200 species of lupin genus have been reported worldwide and majority of them are distributed in the temperate and subtropical zones of South and North America [3]. Lupins are cultivated on an area of 1 million ha worldwide with total production of 1.385 million metric tons. Approximately, 63% lupins productions come from Australia [4]. Due to high concentration of proteins in their seed they are considered as potential alternate of soybean [Glycin max (L.) Merr.] in livestock and poultry feed [5].

This multi-purpose climate resilient pulse crop is erect in stature ranging from 20 to 160 cm tall with a strong herbaceous stem, tap root system, palmate leaf, hermaphroditic flower and often reproduce by self-pollination [6]. Seeds are produced within pods that are similar to field pea (Pisum sativum L.) and develop in clusters. The seed has 28–44% protein, 8–14% oil, and 30–40% fibre [5, 7]. Lupin seeds are lower in carbohydrates (up to 4%) as compared to other legumes (up to 50%) which make them ideal for ketogenic diets. Lupin plants fix atmospheric nitrogen through Bradyrhizobium, mobilize phosphorus through exudation of carboxylases, add organic matter, favour marginal sandy soils, and are an excellent break crop for cereal-based cropping system [8].

The need for new animal feed pulse crops, such as lupin, arises from several reasons, including the desire to diversify feed sources, reduce dependence on traditional feed ingredients like soybean, and enhance overall sustainability in livestock and poultry production. Lupin can offer a rich source of protein, essential amino acids, and other nutrients required for the healthy growth and development of livestock and poultry [9]. On the other hand, heavy reliance on soybean can lead to sudden price fluctuations and supply chain disruptions. Therefore, incorporating lupin in crop rotations can help reduce industry’s dependence on soybean, lowering transportation costs and supporting local feed supply chains [10].

Agriculture in marginal areas faces several unique challenges due to its arid environment and salinity is one of them. Approximately, 20% of the world’s agricultural lands have already been affected by salinity [11]. Salinity causes over accumulation of toxic ions such as Na+ and Cl− that exhibit detrimental effects on plant metabolism and results in growth inhibition [12]. Generally, plant responses to salinity are evaluated by their growth, ion balance, compatible organic solutes synthesis, and osmotic adjustments [13].

Lupin is moderately tolerant to drought stress but severely sensitive to saline environments, especially to saline irrigation water. The L. termis plants exposed to salinity stress exhibited a significant decline in several growth parameters and photosynthetic pigment content [14]. In white lupin, salt stress has been reported to reduce growth, transpiration rate, photosynthetic rate and pigments content [15]. Moreover, increased NaCl stress decreased the leaf area, shoot length, root length, and shoot and root dry weights, while it enhanced the antioxidant enzymatic activities in Brassica olerace [16]. However, the effects of salinity on physiological attributes of white lupin are not well studied in the past.

Plant growth regulators (PGRs) help plants to mitigate detrimental effects of abiotic stresses through acting as a growth promoter, osmo-protectants, micronutrients or phytohormones [17]. For example, the exogenous application of methyl jasmonates, alpha-tocopherol, ascorbic acid, and brassinosteroids improved rice (Oryza sativa L.) growth and yield traits via enhanced photosynthesis, spikelet fertility, and grain filling duration [18, 19]. Exogenous foliar application of epibrassinolide improved common bean (Phaseolus vulgaris L.) grain yield by 42% under salinity stress while foliar spray of brassinosteroids increased field pea seed yield by 18–35% [20, 21]. Similarly, the application of potassium sulphate significantly improved the growth and yield of mung bean [Vigna radiata (L.) R. Wilczek] cultivars [22].

Ascorbic acid regulates salinity stress in plants by quenches ROS, recycling lipids, maintaining photosynthesis, cell wall expansion and synthesis of numerous hormones [23, 24]. Among the series of salinity stress mitigation responses, potassium plays a crucial role in maintaining cell homeostasis, mediate plant defense mechanism, acts antagonistically against accumulation of sodium and improve nitrogen use efficiency [25]. Boron alleviated the detrimental effects of sodium on Glycine max through attributing to an increase of potassium level, relative water content, soluble carbohydrates, maintaining cell osmotic potential, improvement in chlorophyll content and improving photosynthesis [26]. Molybdenum acts as a cofactor in reductase of nitrate, and linked with the assimilation of nitrogen [27]. Its deficiency caused necrosis in Avena sativa and Triticum aestivum, and improper seed filling. In Zea mays, molybdenum deficiency altered flowering through delayed emergence of tassels, smaller anthers and poor development of pollen grains [28]. Foliar application of Methionine successfully adjusted drought stress by reducing MDA and H2O2 content and up regulating the antioxidant enzymes, scavenging ROS, and improvement in potassium, calcium, and phosphorus content [29].

The role of PGRs in mitigating salinity stress in white lupin is underexplored. Therefore, the current study was undertaken to investigate the following objectives; (i) the detrimental effects of salinity stress on white lupin germination indices, growth traits, yield, chlorophyll fluorescence, photosynthesis and biochemical enzymes modulation, (ii) to evaluate the influence of PGRs in reversing the harmful effects of salinity stress on different plant organs, (iii) to elucidate the role of antioxidant enzymes influenced by PGRs to quench the oxidative damage caused by salinity stress, and (iv) to estimate the correlation among different growth, yield, biochemical and photosynthesis traits. The knowledge generated in this study will help to gain enhanced insights into the role of PGRs in salinity stress tolerance in white lupin.

Materials and methods

Experiment site and plant establishment

A pot experiment was performed in a covered wire house at the Desert Agriculture Research Area of the Cholistan Institute of Desert Studies (29.378°N; 71.759°E), in the Islamia University of Bahawalpur, Pakistan. The agro-climatic conditions of the experimental area are short, mild-cold winter and long, severe hot summer. The average (minimum-maximum) temperature from sowing to flowering ranges from 9.38 to 27.06 °C and from flowering to maturity 20.68–35.98 °C. The average daily evapotranspiration rate was 3.22 mm, total rainfall during the complete growing season was 26.2 mm and humidity rate ranges from 57 to 93%. The area is classified as arid with low precipitation and higher evapotranspiration, low organic matter and sandy saline-sodic soils. The pots measuring 250 mm × 200 mm (diameter × height) were filled with 5.25 kg soil mixture having ratio of sand, silt, clay, organic matter, and fertilizer (65:22:10:2:1, v: v). The soil mixture was free of salts. The water soluble NPK composite (50:25:25) fertilizer was applied at different intervals to complete the crop nutrients requirement. Vermicompost was mixed with the soil to attain the prerequisite fraction of organic matter content in the soil mixture. One third of the fertilizer dose was applied during the pot filling. The remaining fertilizer dose was applied in two equal splits after completion of germination stage and at the initiation of flowering stage. Weeds were manually pulled off at regular intervals.

White lupin (Lupinus albus cv. V3/G125) seeds were sown in the prefilled pots on November 15, 2022. The advanced line of white lupin was imported for research purpose from Selcuk Univerisity Konya Türkiye. The seeds were multiplied under local environment for two seasons and then used for salinity trial. After maintaining the field capacity level in all the pre filled pots, ten healthy and uniform seeds of white lupin were sown in each pot. The daily germination count was recorded for 15 days after sowing to measure germination indices. The pots were thinned to five plants per pot to measure the initial growth data after completion of germination stage. Three plants were retained until the final maturity.

Application of salinity stress and plant growth regulators (PGRs)

Salinity stress was applied through irrigation with saline water. Three different sources of saline water having total dissolved solids (TDS) of 1 dS m− 1 = slightly saline (control), 3 dS m− 1 = moderately saline and 4.5 dS m− 1 = severely saline were used from sowing to harvesting of the experiment. All the pots were maintained at 75% of field capacity of the used soil. Six PGRs: Ascorbic acid, Potassium chloride, Boric acid, Ammonium molybdate, Methionine (Sigma-Aldrich Merck, Germany), Headline Multi (Swat Agro Chemicals, Pakistan) were foliar sprayed by using a manual knapsack sprayer. All growth regulators were applied at three crop growth stages, including at the time of sowing, at 30 days after seedling emergence and at the initiation of flowering at a dose of 200 ppm each time. To maintain uniformity of dose for all the PGRs and to avoid a concentration based variation in results, the same dose (200 ppm) of each PGR was applied as a foliar spray [30, 31]. A control treatment was maintained by spraying plants with distilled water.

Germination indices

The seed germination and early emergence indices were measured from the daily recorded germination count.

The germination percentage (G%) was calculated according to Fitch et al. [32].

$$G\:\text{\%}=\frac{Seeds\:germinated\:}{Total\:no\:of\:seeds}\times\:100$$
(1)

The mean emergence time (MET) indicates the length of time required for the seed to emerge. It was determined by using the equation that is shown below [33].

$$\text{M}\text{E}\text{T}=\frac{{\sum\:}_{i=1}^{k}ni\:ti}{{\sum\:}_{i=1}^{k}ni}$$
(2)

where; ni ti = the product of seeds emerged at interval ith with the corresponding time interval and ni = no. of seeds emerged in the ith time.

The Mean emergence rate (MER) is actually the reciprocal of the mean emergence time [34].

$$\text{M}\text{E}\text{R}=\frac{1}{MET}$$
(3)

Coefficient of velocity (Cvt) is used to compute the coefficient of variation of the emergence time [34]. where st; standard deviation of the emergence time.

$$CVt=\frac{St}{MET}\times\:100$$
(4)

The emergence index (GI) provides a rough estimate of the number of days necessary to achieve a certain percentage of emergence.

$$\:GI=\sum\:_{i=1}^{k}\raisebox{1ex}{$ni$}\!\left/\:\!\raisebox{-1ex}{$ti$}\right.$$
(5)

Time to 50% emergence (T50%) shows how much time it took for half of the seeds to emerge [35].

$$T50=\frac{ti+(\frac{\sum\:_{i=1\:}^{k}ni\:\:}{2}-ni)(tj-ti)}{nj-ni}$$
(6)

To get the values of ni and nj in the above equation, look at the cumulative number of seeds emerged, which the condition is given below.

$$ni<\frac{{\sum\:}_{i=1\:}^{k}ni}{2}\:<nj$$
(7)

Where ni = closest cumulative number of seeds that have emerged

$$Cni<\frac{{\sum\:}_{i=1\:}^{k}ni}{2}$$
(8)

nj = closest cumulative number of seeds that have emerged

$$Cnj>\frac{{\sum\:}_{i=1\:}^{k}ni}{2}$$
(9)

ti = the time interval corresponding to ni and tj = the time interval corresponding to nj.

Peak value (PV) refers to the total number of seeds that have emerged at the point on the emergence curve when the rate of emergence starts to decrease. Emergence value (EV) is an index of combining speed and completeness of seed emergence [36].

$$Emergence\:value=Peak\:value\:\times\:Germination\:\%$$
(10)

Seedling vigour index (SVI) is the sum total of those characteristics of the seed that determine the level of activity and performance of the seed [37].

$$SVI=Seedling\:length\:\left(cm\right)\times\:Germination\%$$
(11)

Plant growth and morphological attributes

Leaf area of the palmate leaf was measured at flowering by using a digital leaf area scanner (AM-300, ADC Bioscientific Ltd., England). Plant growth and root traits were measured at the harvest of the experiment (20 April 2022). Plant height was recorded with the measuring tape from the base of the stem to the tip of the flower. Root length was measured by spreading the washed roots on a working desk and identifying the longest root. Shoot and root fresh weight was measured after harvesting the fresh plants and cleaning with a tissue paper by using a digital balance. The plant samples were sun dried for 48 h. and then oven dried at 70 °C for 72 h. The number of main stem branches and root nodules were manually counted.

Chlorophyll florescence and photosynthetic activity

Chlorophyll florescence and photosynthetic efficiency of white lupin leaves were measured at the flowering stage by using a portable PhotosynQ supported with an android system (Mutis-peq VII, USA). For the precise measurement the pots were shifted to an open environment directly exposed to sunlight with no shade. All measurements were made early in the morning (09:00 to 10:00 am) to avoid the effect of high temperature stress. The untouched most recently emerged fully expanded top leaves were selected to measure the linear electron flow (LEF), relative chlorophyll (RC), maximum photochemical efficiency of photosystem II (FvP/FmP), quantum yield of photosystem II (Phi2), photochemical quenching coefficient (qL), non-photochemical quenching (PhiNPQ), The quantity of light that enters the plant is controlled away from the photosynthetic process during non-photochemical quenching (NPQt) and ratio of incoming light that is lost via non-regulated processes (PhiNO) [38].

Grain yield components

Effect of salinity and PGRs were also measured on white lupin grain yield and yield contributing traits. The total number of pods was harvested and threshed from each pot separately and the grains were weighted to determine the grain yield per plant. Similarly, the clusters per plant were recorded by manual counting the total number of pods bearing bunches on each plant. Similarly, the number of pods per cluster was counted and pod length was noted by using a measuring scale.

Antioxidants enzymes and biochemical variables

At the initiation of flowering stage, leaf samples were collected and stored at chilling temperature to perform various biochemical analysis. Using a pre-chilled pestle and mortar grinded, 2 g fresh sample of white lupin leaves were standardized in 10 mL of reaction mixture consisting of HCl: acetone: methanol (2:8:90) to determine the total phenolic content (TPC) and total antioxidant capacity (TAEC). The TPC was measured by using the Folin-Ciocalteu (FC) reagent method. A 2,2-diphenyl-1-picrylhydrazyl radical (DPPH) assay was used to assess the TAEC in the leaves. The TAEC was established by utilizing the methodology presented [39]. The absorbance was measured at 765 nm for TPC and 517 mm for TAEC. The total soluble proteins (TSP) were measured by using a semi-automatic Kjeldahl apparatus and multiplying it by a factor of 6.25.

Fresh leaves weighing 10 g were ground in a pre-chilled pestle and mortar with 20 mL of phosphate buffer solution with a pH of 7.2 and a final volume of 1 l. The mixture was spun in a centrifuge for 5 min at 9000 rpm at 4 °C. The supernatant was used to determine the activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD). The SOD was measured by adopting the procedure described by Giannopolitis and Ries [40]. The CAT and POD were noted buy using the method of Liu and Xiong [41]. The absorbance of POD, CAT and POD were measured by setting the wavelength of a single beam spectrophotometer at 560 nm, 240 nm and 470 nm, respectively.

Statistical analysis

The experiment was laid out in a completely randomized design with a 6 × 3 factorial arrangement using three replicates for each treatment. The data were analysed using the analysis of variance (ANOVA) to determine the significant differences among treatments. The Fisher’s least significant difference (LSD) test was performed at 5% probability to compare the differences among treatment means. Correlation analysis was performed for different growth, yield, biochemical and photosynthetic attributes against seed vigour index and leaf area by using the R Studio software version 4.3.1 [42] Correlation graphs were created by using R studio and MS-Excel (Microsoft Corporation, Albuquerque, New Mexico, United States).

Results

Seed germination indices

In comparison to control treatment, the application of salinity resulted in a significant reduction in all studied white lupin germination indices, whereas the application of PGRs brought a substantial improvement. The interaction of salinity×PGRs resulted in a non-significant change in G%, MET, MER and PV but had a significant positive effect on Cvt, EI, T50%, EV and SVI (Table 1). With an increase in salinity levels, it considerably (31%) reduced the EI while it moderately (24%) declined EV and SVI while application of ascorbic acid, potassium chloride and multi zinc recovered the detrimental effects of salinity stress through demonstrating an improvement of 58% under severe salinity stress (Table 2). Despite the fact, the severe salinity has extensively stretched (46–50%) the T50% and Cvt as compared to control yet the application of ammonium molybdate narrowed the difference in above traits by 35% at severe salinity. Therefore, it is obvious from the data that both variation in emergence time and delay in completing germination (47–50%) are the key germination indices that are negatively affected at the initial stages of crop development under salinity stress. With an increase in salinity, a gradual decline recorded in G% age and MER. On contrary, increasing salinity levels extended the MET and PV (Table 3). The PGRs helped white lupin to tolerate salinity at early growth stages through bringing an improvement in different germination indices. The application of potassium chloride produced the highest G% age, while ascorbic acid produced the highest values for MER and the lowest values for MET and PV (Table 4). However, among tested PGRs, the methionine contributed the least in plant recovery at seedling stage against applied levels of salinity.

Table 1 Analysis of variance (ANOVA) for different germination indices as affected by salinity levels and foliar applied plant growth regulators
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Table 2 Emergence indices of white lupin as affected by salinity stress under combined application of different plant growth regulators
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Table 3 Emergence indices of white lupin as affected by different levels of salinity stress
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Table 4 Emergence indices of white lupin as affected by foliar application of different plant growth regulators
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Plant growth and root traits

Effects of salinity, PGRs and their interaction were significant (p ≤ 0.05) for plant height, root length, leaf area, shoot-root fresh and dry biomass accumulation while the effect of PGRs and its interaction with salinity were non-significant for the number of branches per plant and root nodulation (Table 5). The rise in salinity levels noticeably reduced the plant height (26%), leaf area (46%),and biomass accumulation (54%) however slightly increased root length (16%) as compared to control, though, the foliar spray of potassium chloride displayed a substantial improvement in plant height (41%), ascorbic acid considerably increased root length (49%), root fresh and dry weight (93 − 67%), multi zinc expanded leaflet area (51%) and ammonium molybdate improved shoot fresh and dry weight accumulation (46–95%) at severe salinity (Table 6).

Table 5 Analysis of variance (ANOVA) for different shoot and root growth parameters affected by salinity levels and foliar applied plant growth regulators
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Table 6 White lupin shoot and root growth parameters influenced by salinity stress under combined application of different plant growth regulators
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The rise in salinity has decreased the number of branches per plant (28%) and root nodulation (26%) as compared to control (Table 7). The application of ascorbic acid produced the highest number of root nodules that was followed by ammonium molybdate and potassium chloride. However, the application of PGRs produced non-significant effect on number of branches per plant. Similar to growth traits, the application of salinity negatively affected white lupin root development. The application of ammonium molybdate produced the longest roots without salinity stress but the use of methionine and ascorbic acid produced the longer roots at moderate and severe salinity respectively.

Table 7 White lupins shoot and root growth parameters influenced by different levels of salinity stress
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Antioxidant enzymes and biochemical traits

Effects of salinity, PGRs and their interaction were highly significant (p ≤ 0.05) for SOD, CAT, POD, TSP, TPC and TAEC activity (Fig. 1). A gradual decline was observed in POD, TPC and TAEC content at moderate salinity while a sudden decline was noticed in the activity of SOD and CAT at severe salinity. On contrary, with an increase in salinity, the activity of TSP was significantly improved especially at the highest salinity. The foliar supplementation of potassium chloride, methionine, multi zinc, methionine and ascorbic acid displayed a recovery of 140% in the activity of SOD, 70% in CAT, 60% in POD, 15% in TPC and 11% in TAEC respectively at moderate salinity when compared to their respective control. Application of multi zinc improved TSP by more than 50% at severe salinity stress. Thus, the antioxidants enzymes activity responded inversely while the TSP content was directly interrelated with the increase in salinity.

Fig. 1
figure 1

Effect of plant growth regulators (PGRs) and salinity stress (SS) on antioxidants and biochemical parameters of L. albus. SOD; superoxide dismutase, CAT; catalase, POD; peroxidase, TSP; total soluble proteins, TPC; total phenolic contents, TAEC; total antioxidants capacity, Cont; control, Asc acid; ascorbic acid, Pot chl; potassium chloride, Bor acid; boric acid, Amm mol; ammonium molybdate, Meth; methionine, Mul zinc; multi zinc

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Chlorophyll florescence and photosynthetic efficiency

The chlorophyll florescence parameters of white lupin displayed differences in their standard functioning through a substantial drop in Phi2 and the FvP/FmP with the rise in salinity stress (Fig. 2). The plant NPQt, qL, PhiNPQ, and PhiNO activity significantly improved with the application of ascorbic acid, multi zinc, ascorbic acid, and ammonium molybdate respectively under salinity. Some PGRs declined leaf activity, such as boric acid reduced leaf thickness and potassium chloride lowered leaf temperature under severe salinity. Averaged across salinity levels and PGRs, data analysis recorded a decrease of 6% in LEF, 2.5% in leaf thickness, 0.98% in leaf temperature, 7% in FvP/FmP, 8% in Phi2, and 7.5% in PhiNO under severe salinity. On contrary, the application of PGRs brought a reasonable improvement 23% in RC, 5% qL, 8% in PhiNPQ and 33% in NPQt under severe salinity. Thus, the adverse effects of salinity on the photosynthetic attributes were mitigated by the strategic use of PGRs. The ascorbic acid and potassium chloride were the most effective PGRs that noticeably mitigated the adverse effects of salinity on some important traits of photosynthesis. Nonetheless, substantial reduction in vital chlorophyll florescence trait i.e., Phi2 indicates that the PGRs had a limited role to alleviate adverse effects at severe salinity in white lupin.

Fig. 2
figure 2

Effect of plant growth regulators (PGRs) and salinity stress (SS) on chlorophyll fluorescence parameters of L. albus. LEF; linear electron flow, RC; relative chlorophyll, FvP/FmP; maximum photochemical efficiency of photosystem II, Phi2; quantum yield of photosystem II, qL; photochemical quenching coefficient, PhiNPQ; non-photochemical quenching, NPQt; the quantity of light that enters the plant is controlled away from the photosynthetic process during non-photochemical quenching, PhiNO; ratio of incoming light that is lost via non-regulated processes, Cont; control, Asc acid; ascorbic acid, Pot chl; potassium chloride, Bor acid; boric acid, Amm mol; ammonium molybdate, Meth; methionine, Mul zinc; multi zinc

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Yield and contributing traits

All grain contributing traits significantly declined (44–53%) with the intensity of salinity levels and the maximum reduction noticed in pods per cluster (Fig. 3). Application of PGRs considerably helped plants to fight adverse effects of salinity and recovered grain yield. The application of ascorbic acid has incremented the grain yield by 29%, clusters per plant by 52%, pods per cluster by 75% and pod length by 35% under severe salinity. The application of boric acid and methionine were the least effective PGRs against salinity.

Fig. 3
figure 3

Effect of plant growth regulators (PGRs) and salinity stress (SS) on yield contributing traits of L. albus. GY; grain yield, CP; clusters per plant, PC; pods per cluster, PL; pod length

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Correlation of seedling vigor index (SVI) with physiological and morphological attributes

The SVI displayed a positive correlation with CAT, POD, TAEC, LEF, FvP/FmP, Phi2 and PhiNO with values ranging from 0.0063 to 0.75 under control. Albeit, the negative correlation was recorded for SOD, TSP, TPC, LTH, RC, LT, qL, PhiNPQ and NPQt and the values varied from − 0.0493 to -0.4378 (Fig. 4). Under moderate salinity, the positive association of SVI with SOD, CAT, TSP, TPC, TAEC, RC, FvP/FmP and PhiNO with values ranging from 0.059 to 0.63. The negative association of SVI was found with LEF, NPQt, POD, LTH, LT, Phi2, PhiNPQ and qL, the pearson correlation ranging from − 0.0125 to -0.3382. Under severe salinity a positive correlation was found among POD, TSP, TPC, LTH, RC, FvP/FmP, PhiNPQ and PhiNO and the correlation values ranged from 0.0195 to 0.6754. The negative association was found for SOD, CAT, TAEC, LEF, LT, Phi2, qL and NPQt, and the correlation values ranged from − 0.0358 to -0.5356.

Fig. 4
figure 4

Correlation coefficients of different biochemical parameters with seedling vigor index (SVI) of L. albus. SOD; superoxide dismutase, CAT; catalase, POD; peroxidase, TSP; total soluble proteins, TPC; total phenolic contents, TAEC; total antioxidants capacity, LEF; linear electron flow, RC; relative chlorophyll, LT; leaf temperature, FvP/FmP; maximum photochemical efficiency of photosystem II, Phi2; quantum yield of photosystem II, qL; photochemical quenching coefficient, PhiNPQ; non-photochemical quenching, NPQt; the quantity of light that enters the plant is controlled away from the photosynthetic process during non-photochemical quenching, PhiNO; ratio of incoming light that is lost via non-regulated processes

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Correlation of seedling leaf area (LA) with physiological and morphological attributes

At control, the LA showed a positive association with CAT, POD, TPC, TAEC LEF, LTH, FvP/FmP, Phi2 and PhiNO, with correlation values ranging from 0.0194 to 0.8315 (Fig. 5). A negative correlation was found for SOD, TSP, RC, LT, qL, PhiNPQ and NPQt with the numeric values ranging from − 0.1132 to -0.6123. Under moderate salinity, the association of LA with SOD, CAT, TSP, TPC, TAEC, LEF, RC, FvP/FmP and PhiNO and has correlation values ranging from 0.1 to 0.4344. The negative association of LA exists with POD, LTH, LT, Phi2, qL, PhiNPQ and NPQt, and with association values ranging from − 0.0587 to -0.4776. Under severe salinity the LA showed a positive association with CAT, POD, TSP, TPC, TAEC, LEF, LTH, RC, FvP/FmP, Phi2 and qL, having the correlation values ranged from 0.026 to 0.4248. The negative association of LA was found with SOD, LT, PhiNPQ, NPQt and PhiNO, and which has association values from − 0.0937 to -0.041.

Fig. 5
figure 5

Correlation coefficients of different biochemical parameters with leaf area (LA) of L. albus. SOD; superoxide dismutase, CAT; catalase, POD; peroxidase, TSP; total soluble proteins, TPC; total phenolic contents, TAEC; total antioxidants capacity, LEF; linear electron flow, RC; relative chlorophyll, LT; leaf temperature, FvP/FmP; maximum photochemical efficiency of photosystem II, Phi2; quantum yield of photosystem II, qL; photochemical quenching coefficient, PhiNPQ; non-photochemical quenching, NPQt; the quantity of light that enters the plant is controlled away from the photosynthetic process during non-photochemical quenching, PhiNO; ratio of incoming light that is lost via non-regulated processes

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Discussion

The application of salinity hampered the seed emergence and delayed the early seedling establishment as well as growth. A decline in emergence indices might be due to the over accumulation of salts in the germinating embryos. Higher salinity is known to cause ionic imbalance, impair nutrient availability and uptake, compromise water retention, impact plant metabolism, disrupt effective regulation of enzymes and ultimately injure the germinating plumule [43, 44]. Previously, this trend has been reported in other crop species. For example, germination percentage, germination rate and seedling establishment in field pea significantly declined with the accumulation of salts and almost reached to 0% germination at 16 dS m− 1 [45, 46].

Plant species, growth stage, concentration and type of salts determine the toxicity level. In comparison to Vicia faba, white lupin is considered highly sensitive to salinity stress. In current study, the rise in salinity resulted in serious negative effect on the leaf area and plant biomass accumulation however; it slightly reduced the branching capacity of the plant. Similar to our findings, the application of 300 mM NaCl solution resulted in a significant decline in white lupin shoot and root growth traits [14]. A significant reduction has also been reported in plant height, leaf area, root fresh and dry biomass, and shoot dry biomass that impeded leaf expansion, photosynthesis and nutrient uptake under salinity [47,48,49,50]. Salinity led to a decline in root length and formation of healthy nodules reflecting the inhibitory effect of salts on root development and nitrogen-fixing symbiotic associations in white lupin [51, 52].

The applied PGRs unevenly reversed the negative effects of salinity on white lupin germination, growth and yield traits including root nodulation. This is mainly because of differential mitigating role of different compounds in regulating various physiological functions. Abdalla [53] reported that soil fertilization of white lupin plants by diatomite significantly improved growth and yield parameters such as shoot and root length, fresh and dry biomass accumulation, and the number of pods plant− 1 under water stress. According to another study, foliar applied ascorbic acid considerably increased the pod length, number of pods per plant, 1000 grain weight and grain yield in field pea under NaCl stress [54]. The agronomic biofortification of spinach with potassium dihydrogen phosphate improved growth and antioxidant enzymes activity under salinity stress [55]. Application of ammonium molybdate in combination with rhizobium and phosphorus solubilizing bacteria significantly increased number and size of nodules, plant height, branches plant− 1, pods plant− 1 and grain yield in field grown chickpea [56]. A significant rise in uptake of ions (N, K, P, Ca, Mg) in salt grown white lupin by the foliar application of ascorbic acid helped the plant to maintain osmotic balance, improve nutrient availability and perform biochemical functions [57].

Salinity disrupts biochemical functioning in plants through formation of reactive oxygen species (ROS) such as superoxide anion, hydrogen peroxide and hydroxyl radicals. The overproduction of ROS causes chlorophyll degradation, denaturation of proteins, membrane damage and electrolytes leakage. It further disturbs cell water balance, loss of turgor pressure, closure of stomata, imbalance in growth hormones, reduction in photosynthesis and inhibition of normal growth [58]. Salinity stress increased xylem transport of abscisic acid by up to 10 folds in white lupin [59]. To encounter the salinity stress, plants activated their antioxidant enzymes (SOD, CAT, APX) system, improved energy conservation rate, photochemical quenching and reduced the linear electron flow and quantum yield of photosystem-II [16]. The sodium bicarbonate stress decreased chlorophyll content, total protein, total alkaloids, total flavonoids and secondary metabolite production in white lupin [48, 50].

The application of α‑tocopherol as a growth stimulator significantly improved white lupin chlorophyll content, proteins, carbohydrates, alkaloids and carotenoids under salinity [60]. Foliar spray of indole acetic acid and cytokinin enhanced the growth, ionic uptake (K, Ca, Mg), accumulation of amino acid and sugars, and the activity of antioxidant enzymes (SOD, CAT, POX, APX) in faba bean under salinity [61]. Combined application of salicylic acid and methyl jasmonate alleviated the adverse effects of high temperature stress in wheat through a significant improvement in SOD, Phi2, NPQt, grain protein content and grain filling duration [62]. Chitosan application enhanced leaf proline, total phenolics, linear electron flow and non-photochemical quenching in eggplant [63].

Improvement in growth and morphological parameters through PGRs is associated with improvements in physiological functions. Similarly to our findings, the foliar spray of PGR (arginine) mitigated salt stress by inducing antioxidant enzyme activity and improving morpho-physiological traits in white lupin [14]. The PGRs such as salicylic acid and methyl jasmonate increased LEF, supporting the idea that they enhance photosynthetic activity under stress. Salinity stress slightly decreased Phi2 in our study, suggesting some disruption in the photosynthetic electron transport channel however, PGRs improved Phi2, indicating their role in stabilizing photosynthetic processes. The PGRs increased qL, which suggests enhanced energy dissipation and protection of PSII under abiotic stresses [62].

Conclusion

Current results demonstrated sensitivity of white lupin to rising salinity stress. The application of PGRs especially ascorbic acid, potassium chloride, and ammonium molybdate helped white lupin to fight salinity stress from emergence to grain filling. The application of ascorbic acid reduced the time taken to complete germination both under stressed and non-stressed conditions. Similarly, ascorbic acid and multi zinc recovered the plant height, leaf area and grain productivity while ammonium molybdate favoured the plant biomass accumulation under salinity stress. The foliar application of ascorbic acid and potassium chloride considerably supported antioxidant enzymes activity but slightly improved the photosynthetic efficiency traits under severe salinity. The key photosynthetic processes impeded by the salinity were linear electron flow, efficiency of photosystem II and photochemical quenching. The use of PGRs should be encouraged to mitigate negative impacts of salinity in white lupin as a short term management strategy.

Data availability

All data generated or analysed during this study are included in this article.

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Acknowledgements

The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP2024R356), King Saud University, Riyadh, Saudi Arabia. M.Z.I appreciates Agricultural Linkages Program, ALP-PARC (Project No, CS-905) for research grant support. A.A.B. is thankful to La Trobe University for continuing support enabling collaborative international research and publications.

Funding

The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP2024R356), King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Cholistan Institute of Desert Studies, The Islamia University of Bahawalpur, Bahawalpur, 63100, Pakistan

    Muhammad Zahid Ihsan

  2. Department of Botany, The Islamia University of Bahawalpur, Bahawalpur, 63100, Pakistan

    Shamshad Kanwal

  3. Department of Agronomy, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, 23200, Pakistan

    Shah Fahad

  4. Oilseeds Research Institute, AARI, Faisalabad, 38000, Pakistan

    Waqas Shafqat Chattha

  5. Botany and Microbiology Department, College of Science, King Saud University, P.O. Box. 2460, Riyadh, 11451, Saudi Arabia

    Abeer Hashem

  6. Plant Production Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box. 2460, Riyadh, 11451, Saudi Arabia

    Elsayed Fathi Abd-Allah

  7. Arid Zone Research Institute Bahawalpur, PARC, P.O. Box. 1031, Islamabad, Pakistan

    Mumtaz Hussain

  8. La Trobe Institute of Sustainable Agriculture and Food (LISAF), Department of Animal, Plant and Soil Sciences, AgriBio, La Trobe University, Melbourne, 3086, Australia

    Ali Ahsan Bajwa

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Contributions

Conceptualization: M.Z.I., S.K., S.F. and A.A.B.; methodology, data collection and original data analysis: S.K., W.S.C., M.H. and S.F.; data presentation, writing: M.Z.I., A.H., and S.K.; reviewing and editing: M.Z.I., A.A.B., A.H. and E.F.A.; funding acquisition: M.Z.I., A.H. and E.F.A. All authors have read and agreed to the published version of the manuscript.

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Ihsan, M.Z., Kanwal, S., Fahad, S. et al. Plant growth regulators improve the yield of white lupin (Lupinus albus) by enhancing the plant morpho-physiological functions and photosynthesis under salt stress. BMC Plant Biol 24, 1020 (2024). https://doi.org/10.1186/s12870-024-05676-3

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