Effect of Biostimulants on Plant Growth and Leaf Functional Compounds of Passiflora Plants

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Yu-Chiao Chung Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Cheng-Hsuan Chen Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Yu-Sen Chang Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Kuan-Hung Lin Department of Horticulture and Biotechnology, Chinese Culture University, Taipei 111, Taiwan

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Chun-Wei Wu Department of Horticulture, Hungkuo Delin University of Technology, No. 1, Ln. 380, Qingyun Rd, Tucheng Dist, 236302 New Taipei City, Taiwan

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Abstract

The influence of biostimulant treatments on Passiflora species was assessed by observing changes in the growth and leaf functional compounds of plants exposed to humic acids (HAs) and seaweed extracts (SEs) to determine their optimal application doses. Four different concentrations of HA irrigation (0, 144, 192, and 285 mg·L−1 per pot assigned as HI-1, 2, 3, and 4, respectively), HA spraying (0, 96, 128, and 192 mg·L−1 as HS-1, 2, 3, and 4, respectively), SE irrigation (SI-1∼4 at 0, 1, 1.33, and 2 g·L−1 per pot, respectively), and SE spraying (SS-1∼4 at 0, 0.5, 0.67, and 1 g·L−1, respectively) treatments were applied to ‘Tainung No. 1’ and Passiflora suberosa cultivars every week to study their responses in plant growth traits and metabolites. Results show that leaf dry weight (DW) and root DW of ‘Tainung No. 1’ plants under SS-3 and HI-4 treatments, respectively, were significantly increased compared with controls. Both HI-3 and HS-3 treatments remarkably increased vine length, fresh weight (FW), and DW of leaves and shoots in P. suberosa plants compared with controls. Furthermore, ‘Tainung No. 1’ and P. suberosa plants respectively subjected to HI-2 and SS-4 treatments contributed to developing biostimulant applications for obtaining higher total phenol and flavonoid content per plant. Both Passiflora species are recommended for treatment with SS-4 and SE to maximize orientin and isovitexin content, and for all their beneficial applications and sustainable use in agriculture.

HAs, important components of humic substances, are known to be active at relatively low concentrations, and show positive effects on recalcitrance to soil microbial degradation (Lumactud et al. 2022), modifications in roots ultrastructure (Nunes et al. 2019), alterations in plant metabolism (Canellas et al. 2020), improvements in nutrient absorption (Bayat et al. 2021), and crop quality and yield (Gholami et al. 2018; Mahmood et al. 2020; Rathor et al. 2024; Souza et al. 2022). In addition, HA has multifunctional roles in mediating physiological processes and responses to abiotic/biotic stress tolerance in plants. Moreover, plant extracts have been applied as biostimulants for plant protection, increases in agroecological sustainability, and sustainable crop productivity (Ali et al. 2019; Parađiković et al. 2019). Among them, seaweeds constitute one potential resource for commercial exploitation with proven efficacy. SEs contain many biologically active substances (Vaghela et al. 2023) that help plants increase soil water retention; reduce soil nutrient deficiencies (Kocira et al. 2018); increase soil microbiota (Nanda et al. 2022; Rouphael et al. 2020); activate pathogen defense (Ali et al. 2022; Shukla et al. 2021); enhance plant growth, yield, and flowering (Dookie et al. 2021; Yusuf et al. 2017); and tolerate (a)biotic stresses (Ali et al. 2023; Frioni et al. 2019; Rasul et al. 2021; Shukla et al. 2019; Trivedi et al. 2018a). Despite the reportedly significant benefits of HA and SE on plants, their specific effects and underlying functional compounds are broadly dependent on the diverse compositions of these biostimulants, application rates, times, frequencies, and plant species to facilitate their most efficient and accurate application for optimizing plant growth and yield (Ali et al. 2021).

Passiflora, the largest genus of the Passifloraceae family, includes more than 500 species of passion fruit found in tropical and subtropical regions of the world, with emphasis on the purple Passiflora edulis Sims and yellow P. edulis flavicarpa (Guimaraes et al. 2020; He et al. 2020; Melo et al. 2020). P. suberosa L. is native to the Americas and was introduced to Asia and Oceania including Taiwan. This species is cultivated in family farming as an important medicinal plant to treat several diseases and leaves from this plant are consumed as a fresh green vegetable (Wu et al. 2004). Moreover, ‘Tainung No. 1’ passion fruit, a commercial hybrid (P. edulis × P. edulis f. flavicarpa), is the main variety and the most popular passion fruit cultivated in Taiwan, and widely used by the juice industry and for its nutritional consumption as well (Liu et al. 2015). In addition, because their pharmacological properties are known in popular medicine, passion fruit varieties are considered functional foods. Its seeds have significantly higher phenolic compounds, alkaloids, and antioxidant activity compared with the peel and pulp (da Costa et al. 2023). Extracts of Passiflora species leaves are used in folk herbal medicines to treat diabetes, hypertension, skin diseases, anxiety, irritability, migraines, insomnia, opiate withdrawal, and attention deficit hyperactivity, due to the presence of bioactive compounds such as flavonoids (da Fonseca et al. 2020), isovitexin (apigenin-6-C-glucoside), and orientin (OR, luteolin-8-C-glucoside) (Alves et al. 2020; Coleta et al. 2006). Isovitexin (IV), an isomer of vitexin, can be found in Passiflora, bamboo, pigeon pea, and mimosa, and their bioactive ingredients contain various biological activities, such as antioxidant, anti-inflammatory, and anti-Alzheimer’s activity (He et al. 2016). Orientin, a water-soluble flavonoid, exists in various plants, is widely studied for its medicinal properties, including antioxidant, anti-aging, antiviral, antibacterial, anti-inflammation, vasodilatation and cardioprotective, radiation protective, neuroprotective, antidepressant, and antinociceptive effects (Lam et al. 2016; Schäfer et al. 2022). Furthermore, the fruit pulp of Passiflora species is used as a cardiac tonic, a moderate diuretic, and digestive stimulant, and to treat asthma, bronchitis, whooping cough, and urinary infections (Amaral et al. 2020). However, there are no reports of HA and SE enhancing plant growth and leaf functional compounds of any Passiflora plants. The mechanisms of these two biostimulants’ actions on the growth and physiological processes of Passiflora plants remain unknown. Thus, the optimized biosynthesis of these functional metabolites can confer more significant medicinal activity to passion fruit phytomass by the addition of these natural substances to plant cultivation.

It is unknown whether concentrations of IV and OR in Passiflora species are affected by different biostimulants, so the contents of these particular flavonoids in the leaves of Passiflora species were examined in this study. The objectives of the present study were to evaluate and compare the effects of optimal concentrations of HA and SE treatments on phenotypic performance and leaf functional compounds of ‘Tainung No. 1’ and P. suberosa. The hypothesis of this research was that some physiological components and the production of secondary metabolite accumulation in leaves might exhibit distinguishable differences between plant species under different concentrations in HA- and SE-treated plants. This research provides a scientific basis for using optimal levels of these biostimulants in the cultivation and management of these Passiflora species.

Materials and Methods

Plant materials and cultural practice

Healthy plants of Passiflora suberosa L. and ‘Tainung No. 1’ were obtained from local shops in Taipei, Taiwan, and grown in the greenhouse at National Taiwan University (lat. 25.01 ° N) in Apr 2021. The culture and management of these plants were previously described by Ni et al. (2020). Plants were grown for 50 d, and those of uniform size were selected and randomly separated into four groups for the biostimulant experiments. Each biostimulant treatment group was independent of the others.

Biostimulant treatments

One group of eight pots (one plant per pot) of each species was irrigated with a commercial HA containing 11.5% of HA (BT023B20, GROW MORE, Gardena, CA, USA) at four concentrations of aqueous solutions (dissolved in 200 mL of distilled deionized water), including 0 (untreated plants as control), 144, 192, and 285 mg·L−1 per pot, and assigned as HI-1, -2, -3, and -4, respectively. These aqueous HA solutions were applied to the top 5-cm soil layer of each pot every week. Another group of eight pots in each species were leaf-sprayed with HA at 0 (water spray as control), 96, 128, and 192 mg·L−1, and assigned as HS-1, -2, -3, and -4, respectively. These aqueous HA solutions (dissolved in distilled deionized water) were sprayed onto plant leaves every week with a hand-held power sprayer until saturated. The third group of eight pots in each species were irrigated with aqueous solutions of a commercial SE powder product (Acadian® Marine Plant Extract Powder; Acadian Seaplants Limited, Dartmouth, NS, Canada) at 0, 1.00, 1.33, and 2.00 g·L−1 with 200 mL per pot, and assigned as SI-1, -2, -3, and -4, respectively. These aqueous solutions of SE were applied to the top 5-cm soil layer of each pot every week. The fourth group of eight pots in each species were foliage-treated with SE at 0, 0.50, 0.67, and 1.00 g·L−1, and assigned as SS-1, -2, -3, and -4, respectively. These aqueous SE solutions were sprayed onto plant leaves every week with a hand-held power sprayer until saturated. Biostimulant solution concentrations were selected based on data from our preliminary study modified from Chen and Aviad (1990) and Polo and Mata (2017). Plants without biostimulant treatment were considered controls to provide a basis for comparison with the effects of biostimulant treatments. During the biostimulant treatment period, 150 mL of the above-mentioned water-soluble fertilizer solution (20N–8.8P–16.6K) with a 1000x dilution was added to each pot every week, and after at least 3 d followed by an individual biostimulant treatment.

These four groups of plants in each biostimulant treatment were independent and arranged in a completely randomized design, with a total of 32 pots of each variety used. In each experiment, all plants from HI or HS (SI or SS) in each genotype were harvested at the same time of day and used for plant growth components and leaf functional compound measurements, and data were recorded and calculated after 3 months. The influence of the applied treatments was investigated via the below-listed parameters.

Plant growth measurements

From each treatment, healthy and fully expanded leaves were taken and dried in a drying oven for 50 h at 65 °C before weighing, followed by the DW of leaves, shoots, and roots being measured with an electronic balance.

Determination of TP, TF, and flavone content

After biostimulant treatment for 3 months, healthy and fully expanded fresh leaves of two Passiflora species were collected and dried for 4 d at 35 °C in a drying oven (Pereira et al. 2005), followed by grinding up with a grinder. The dry powdered leaf sample (1 g) was mixed in 10 mL of hot water (90 °C) in a water bath at 90 °C for 15 min. The liquid phase was then separated from debris using a syringe filter (13 mm × 0.22 μm, Millex-GV; Millipore, Sigma-Aldrich, St. Louis, MO, USA) under a vacuum (Rapidvp Vacuum Evaporation System; Labconco, Kansas City, MO, USA) to obtain crude Passiflora leaf extract (PLE), which was used for analysis of flavones, TP, and TF as previously described (Ni et al. 2020).

High-performance liquid chromatography for flavone content.

Reverse-phase C18 high-performance liquid chromatography (HPLC) was used to separate and identify flavone compounds in the PLE. A Hypersil ODS C18 column (250 × 4.6 mm, 5 μm) was connected to the LC-200 HPLC system (Perkin-Elmer, Waltham, MA, USA), and equilibrated with 0.05% aqueous trifluoroacetic acid. Ten microliters of hot water-extracted PLE was used for the HPLC analysis after filtration through a 0.22-μm syringe filter (Millex-GV, Millipore, Sigma-Aldrich), which was injected and eluted with 0.2% aqueous formic acid and acetonitrile. The flow rate was 1 mL·min−1 at 35 °C, and the injection dose 20 μL. Collected fractions of the eluent were all in 1-mL aliquots, and the eluent absorbance at 345 nm scanned with an LC-785A ultraviolet/VIS detector (Perkin-Elmer). Peaks were identified by comparing the retention time and ultraviolet absorption spectrum of the eluting peaks with flavone standards. The peak wave front area of the liquid sample was tested and converted to concentrations of μg·g−1 according to the calibration line of OR and IV standard products, followed by converting into content according to the DW of the analyzed leaves, expressed in μg per plant. Authentic standards for OR and IV (Sigma-Aldrich) were used to identify the flavone compounds of Passiflora species. A series of standard solutions ranging 0.625 ∼100 μg·mL−1 was tested to determine the calibration curve. Regression equations for OR and IV were calculated in the form of y = ax + b, where y and x were the peak area and amount of standard injected, respectively, and all calibration curves had coefficients of linear correlation R2 of >0.990.

Determination of TP and TF contents.

For TP content, standard gallic acid and an aliquot of PLE were diluted with an acidified methanol solution containing 1% HCl. Two milliliters of 2% Na2CO3 was mixed into each 100-μL sample and allowed to equilibrate for 2 min before adding 50% Folin-Ciocalteau reagent (Sigma-Aldrich). Absorbance at 725 nm was measured at room temperature using a microplate reader (InterMed, South Portland, ME, USA). A standard curve for gallic acid was used to calculate TP levels. The TP content was expressed as mg gallic acid equivalent (GAE) per plant (mg GAE per plant). The assay was run in triplicate for each sample. For TF content, 1 mL of PLE (5 mg·mL−1) was mixed with 1 mL AlNO3 (10%). The mixture was stirred and kept at room temperature for 15 min. Absorbance was measured at 510 nm on a spectrophotometer. Rutin was used as a reference standard, and TF content expressed as mg of rutin equivalent (RE) per plant. (mg RE per plant). The linear range of the calibration curve was 5.625 ∼ 200 mg·L−1 (R2 > 0.990).

Statistical analysis

The measurements of plant growth traits, OR and IV contents, and metabolites in Passiflora species with HI, HS, SI, and SS treatments were evaluated for significance using an analysis of variance followed by a least significant difference test at P ≦ 0.05. Each treatment was assumed to be independent on the other and arranged in a completely randomized design, with a total of 32 pots of each variety used. Data were recorded and calculated after 3 months of irrigation or spraying with HA or SE of eight replicates. All statistical analyses were conducted using CoStat 6.4 (CoHort Software, Monterey, CA, USA).

Results

HA concentrations affect plant growth and metabolites

Table 1 lists how plant growth and leaf functional compounds differed in ‘Tainung No. 1’ plants after 3 months of cultivation in four different concentrations of HA irrigation (0, 144, 192, and 285 mg·L−1 per pot assigned as HI-1, -2, -3, and -4, respectively) or HA spraying (0, 96, 128, and 192 mg·L−1 as HS-1, -2, -3, and -4, respectively) treatments every week. Significantly higher vine length (190 cm) was detected under HI-3 treatment compared with HI-1 (control, 176.5 cm) and HI-2 (179 cm) treatments. Moreover, significantly higher root DWs were detected with both HI-2 (2.82 g per plant) and HI-4 (2.92 g per plant) treatments compared with control (2.25 g per plant) and HI-3 treatments (2.28 g per plant), whereas all FW and DW of leaves and shoots were nonsignificant in all HI treatments. In addition, TP content at all HI treatments in ‘Tainung No. 1’ (12.07 ∼ 12.77 mg GAE per plant) were significantly higher than in controls (10.18 mg GAE per plant). Significant differences in TF content were observed in all HI treatments compared with controls (5.71 mg RE per plant), and HI-2 treatment exhibited significantly higher TF content (7.86 mg RE per plant) than HI-3 and HI-4 treatments (6.31 and 6.74 mg RE per plant, respectively). Nevertheless, when ‘Tainung No. 1’ plant leaves sprayed with HA were compared across concentrations (HS-1∼4), all plant growth parameters and leaf functional compounds showed no significant differences for all concentrations of HS treatments.

Table 1.

Effects of irrigating and spraying humic acid concentration on vine length, leaf number, total leaf fresh weight, total leaf dry weight, shoot fresh weight, shoot dry weight, root dry weight and total phenol and total flavonoids content in passion fruit ‘Tainung No. 1’ leaves. HI-1, -2, -3, and -4 represent the average of humic acid irrigation in each concentration at 0, 144 mg·L−1, 192 mg·L−1, and 285 mg·L−1, respectively, with 200 mL per pot weekly. HS-1, -2, -3, and -4 represent the average of humic acid spraying in each treatment at 0, 96 mg·L−1, 128 mg·L−1, and 192 mg·L−1 weekly, respectively.

Table 1.

In Table 2, P. suberosa plants had significantly higher vine length (240.75 cm) in HI-3 treatment compared with HI-2 and HI-4 treatments (217.36 and 218.25 cm, respectively). Furthermore, P. suberosa also had significantly higher leaf FW in HI-3 treatment (31.86 g per plant) compared with HI-4 treatment (28.43 g per plant), but no significant differences in both leaf and root DW were observed in any HI treatment. Maximal and significant increases in shoot FW (37.80 g per plant) and DW (5.99 g per plant) occurred in the HI-3 treatment compared with HI-4 treatment (33.09 and 5.24 g per plant, respectively). In addition, the TP content of P. suberosa with HI-3 treatment (4.99 mg GAE per plant) was significantly higher than with HI-2 treatment (3.32 mg GAE per plant) and controls (2.83 mg GAE per plant). Similar trends in TF contents were also observed in P. suberosa plants, and maximal and significant increases in TF content were detected in HI-3 treatment at 1.31 mg RE per plant compared with HI-2 treatment and controls at 1.04 and 1.08 mg RE per plant, respectively. When P. suberosa plant leaves sprayed with HA were compared across concentrations, P. suberosa subjected to HS-3 treatment (234 cm) exhibited a significantly higher vine length compared with HS-2 treatment (210.83 cm) and controls (207.33 cm). FW and DW of leaves and shoots of P. suberosa plants under HS-3 treatments (at 31.96, 4.37, 36.43, and 5.77 g per plant, respectively) were significantly higher than in controls (at 28.69, 3.90, 32.43, and 5.18 g per plant, respectively), but no significant differences in root DW were observed in P. suberosa subjected to all HS treatments. In addition, P. suberosa plants had significantly higher TP content in response to HS-3 treatment (5.38 mg GAE per plant) compared with HS-4 treatment (3.67 mg GAE per plant) and controls (3.86 mg GAE per plant). Significantly higher TF content was observed in HS-2 and HS-3 treatments (0.96 and 0.86 mg RE per plant, respectively) compared with HS-4 treatment and controls (0.79 mg RE per plant).

Table 2.

Effects of irrigating and spraying humic acid concentration on vine length, total leaf fresh weight, total leaf dry weight, shoot fresh weight, shoot dry weight, root dry weight, and total phenol and total flavonoids content in passion fruit Passiflora suberosa leaves. HI-1, -2, -3, and -4 represent the average of humic acid irrigation in each concentration at 0, 144 mg·L−1, 192 mg·L−1, and 285 mg·L−1, respectively, with 200 mL per pot weekly. HS-1, -2, -3, and -4 represent the average of humic acid spraying in each treatment at 0, 96 mg·L−1, 128 mg·L−1, and 192 mg·L−1 weekly, respectively.

Table 2.

A significant increase in OR content was noted in ‘Tainung No. 1’ plants under HI-3 treatment (93.83 μg per plant) compared with HI-4 treatment (83.90 μg per plant) and controls (Fig. 1A), whereas a significant increase in OR content was detected in P. suberosa plants under HI-3 treatment (65.38 μg per plant) compared with controls (50.14 μg per plant). Furthermore, Fig. 1B shows that ‘Tainung No. 1’ plants in response to both HI-3 and HI-4 treatments had significantly higher IV content (99.01 μg and 87.61 μg per plant, respectively) than controls (64.70 μg per plant), but P. suberosa plants did not show any significant differences in all HI treatments. Significantly higher OR content was detected in ‘Tainung No. 1’ plants under HS-2 and HS-3 treatments (89.23 μg and 92.28 μg per plant, respectively) compared with controls (83.58 μg per plant); moreover, significantly higher OR content in P. suberosa plants was detected in HS-3 treatment (65.38 μg per plant) compared with controls (50.14 μg per plant) (Fig. 1C). The IV content of ‘Tainung No. 1’ plants under HS-3 treatment (101.18 μg per plant) was significantly higher than under controls (74.58 μg per plant), but P. suberosa plants did not show any significant differences in all HS treatments (Fig. 1D).

Fig. 1.
Fig. 1.

The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different humic acid treatments. Means within the same humic acid irrigation (HI) or humic acid spraying (HS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be independent on the other.

Citation: HortScience 59, 11; 10.21273/HORTSCI18105-24

SE concentrations affect plant growth and metabolites

The highest root DW and leaf DW of ‘Tainung No. 1’ plants were recorded in SI-4 (2.07 g per plant) and SS-3 (9.32 g per plant), which had a significant difference with controls at 1.82 and 7.46 g per plant, respectively, whereas the other morphological traits had nonsignificant differences with SE applications (Table 3). Similar trends were found in TP and TF contents of ‘Tainung No. 1’ plants, and the highest TF (4.47 mg RE per plant) and TP content (13.73 mg GAE per plant) was obtained in SI-4 and SS-3, respectively, which was significant compared with controls at 4.08 mg RE per plant and 11.11 mg GAE per plant, respectively, whereas TP and TF contents of ‘Tainung No. 1’ had nonsignificant differences with applications of SI and SS (Table 3). No significant differences were measured in all plant growth traits of P. suberosa plants under various SI and SS treatments, but the patterns and trends in the TP content of P. suberosa were similar to TF content under various SI and SS treatments (Table 4). Notably, TP content in P. suberosa under SI-2 and SI-3 treatment (9.57 and 9.40 mg GAE per plant, respectively) exhibited significant increases compared with controls (8.22 mg GAE per plant), and TF content in P. suberosa under SI-2 and SI-3 treatment (2.71 and 2.62 mg RE per plant, respectively) exhibited significant increases compared with controls (2.36 mg RE per plant). In addition, TP content in P. suberosa plants under SS-4 treatment (11.25 mg GAE per plant) exhibited a significantly higher level than in controls (9.54 mg GAE per plant), and SS-4 treated P. suberosa plants had a significantly higher TF content (3.06 mg RE per plant) than controls (2.57 mg RE per plant) (Table 4).

Table 3.

Effects of irrigating and spraying humic acid concentration on vine length, leaf number, total leaf fresh weight, total leaf dry weight, shoot fresh weight, shoot dry weight and root dry weight, and total phenol, total flavonoids content in ‘Tainung No. 1’ leaves. SI-1, -2, -3, and -4 represent the average of seaweed extract irrigation in each treatment at 0, 1 g·L−1, 1.33 g·L−1, and 2 g·L−1 with 200 mL per pot per week, respectively. SS-1, -2, -3, and -4 represent the average of seaweed extract spraying in each treatment at 0, 0.5 g·L−1, 0.67 g·L−1, and 1 g·L−1 per week, respectively.

Table 3.
Table 4.

Effects of irrigating and spraying humic acid concentration on vine length, leaf number, total leaf fresh weight, total leaf dry weight, shoot fresh weight, shoot dry weight, root dry weight and total phenol, total flavonoids content in passion fruit Passiflora suberosa leaves. SI-1, -2, -3, and -4 represent the average of seaweed extract irrigation in each treatment at 0, 1 g·L−1, 1.33 g·L−1, and 2 g·L−1 with 200 mL per pot per week, respectively. SS-1, -2, -3, and -4 represent the average of seaweed extract spraying in each treatment at 0, 0.5 g·L−1, 0.67 g·L−1, and 1 g·L−1 per week, respectively.

Table 4.

SI-2 treatment significantly increased OR content in ‘Tainung No. 1’ plants (143.73 μg per plant) compared with controls (113.21 μg per plant) (Fig. 2A). Meanwhile, significantly higher OR content (139.43 μg per plant) was also detected in P. suberosa plants under SI-2 treatment than in controls (118.46 μg per plant) and SI-4 treatment (101.21 μg per plant). Although no significant differences were observed between all SI treatments and controls in the IV content of ‘Tainung No. 1’ plants, both SI-2 and SI-3 treatment significantly increased the IV content of P. suberosa plants respectively up to 152.12 μg and 159.11 μg per plant compared with controls (122.55 μg per plant) and SI-4 treatment (131.57 μg per plant) (Fig. 2B). Regarding OR content (Fig. 2C), significantly increased OR levels were observed in SS-4 treated ‘Tainung No. 1’ plants (156.01 μg per plant) compared with controls (133.60 μg per plant) and SS-2 treatment (128.07 per plant), and also in both SS-3 and SS-4 treated P. suberosa plants (120.67 μg and 120.04 μg per plant) compared with controls (100.80 μg per plant) and SS-2 treatment (103.58 μg per plant). Significant increases in IV content (135∼181 μg per plant) in ‘Tainung No. 1’ plants subjected to all SS treatments were observed compared with controls (135.38 μg per plant) (Fig. 2D). Moreover, significant increases in IV content in P. suberosa plants were also detected among SS-2 and SS-4 treatments (121.75 μg and 124.15 μg per plant) with respect to controls (105.63 μg per plant).

Fig. 2.
Fig. 2.

The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different seaweed extract treatments. Means within the same seaweed extract irrigation (SI) or spraying (SS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be dependent on the other.

Citation: HortScience 59, 11; 10.21273/HORTSCI18105-24

Discussion

The applications of HA and SE did not significantly increase FW and DW of leaves and shoots, except that both HI-3 and HS-3 treatments remarkably increased FW and DW of leaves and shoots in P. suberosa plants compared with controls (Table 2), and SS-3 treatments significantly increased leaf DW of ‘Tainung No. 1’ plants compared with controls (Table 3). The root DW of ‘Tainung No. 1’ under both HI-4 and SI-4 treatments significantly increased compared with controls (Tables 1 and 3). The HI-3 treated ‘Tainung No. 1’ plants and HS-3 treated P. suberosa plants stimulated significantly higher vine length compared with controls (Tables 1 and 2), and the vine lengths of P. suberosa plants under all treatments displayed remarkable increases compared with ‘Tainung No. 1’ plants.

Silva et al. (2016) showed that the use of humic substances and nitrogen mixtures led to higher concentrations of nitrogen in the leaves of passion fruit, with an increase in stem diameter and yields of treated plants. Hassan and Fahmy (2020) reported that the foliar application of HA significantly increased yield components and essential oil content in chamomile plants. Boveiri Dehsheikh et al. (2020) found that HA application increased soil organic matter content and improved Thai basil plant growth potential and essential oil yield. Rasouli et al. (2022) indicated that both fertilizer and HA improved morphological traits, total soluble protein content, photosynthesis pigments, macro- and micronutrient content, and the content and yield of coriander essential oil as well. Nasiroleslami et al. (2021) revealed that HA induced the biosynthesis of amino acids and improved biological yield in wheat with the regulation and activation of protein metabolic pathways and enzyme activity. The increased DW of leaves and roots and vine length of plants imply that efficient mineral nutrients and photoassimilates released from HA and SE might be available and uptake by the treated plants. Commercial product Acadian® was based on Ascophyllum nodosum brown SE containing organic matter, amino acids, carbohydrates, growth hormones, and some mineral ions (de Mendonca et al. 2020), which could make it an ideal product for maximizing plant growth and maintaining optimum metabolism of leaf functional compounds of Passiflora plants. In addition, several humic-based commercial products have been developed as plant biostimulants and used in the agriculture and horticulture industry worldwide (Rathor et al. 2023). Different concentrations of HA and SE treatments could stimulate the biosynthesis pathways and support the biosynthesis with needed nutrients or catalysts. The changes of phenotypic traits and leaf functional compounds observed in the presence of HA and SE treatments could be due to the mixture of these chemical compounds rather than a single bioactive compound. Therefore, more research is needed to validate the role of HA or SE as signaling molecules. To further optimize the production and application of these biostimulants, it is important to understand which compounds are responsible and perceived by the plant species for the observed effects, as well as their mode of action in plants (Deolu‐Ajayi et al. 2022).

Studies have suggested that key functional groups in HA might trigger physiological and molecular responses through phytohormonal regulation, and improve plant growth and leaf functional compounds directly and indirectly (Gerke 2021; Nardi et al. 2021; Souza et al. 2022). Nardi et al. (2009) also suggested that HA may act as a signaling molecule due to its hormone-like activities, but HA modulates the alteration in overall hormonal balance rather than a specific single hormone (Souza et al. 2022). The biologically active components in HA can hold together by hydrogen and covalent bonds in a supermolecular structure for plant growth, and these bonds can be easily disrupted by organic acids released from roots thereby exposing several small bioactive molecules (Rathor et al. 2023). These bioactive compounds could flow into the apoplast and access the plasma membrane resulting in the alteration of physiological processes and metabolic pathways related to photosynthesis, cellular respiration, nutrient uptake, secondary metabolism, the regulation of reactive oxygen species, and the antioxidant system and improved tolerance to biotic and abiotic stresses (Nardi et al. 2021; Zanin et al. 2019).

Schiavon et al. (2010) found that amino acid metabolism, such as phenylalanine and tyrosine in phenylalanine ammonia-lyase (PAL) pathway, was altered in the HA-treated maize seedlings, and PAL activity and phenolic and flavonoid accumulations were also induced by the application of HA. Cavalcante et al. (2013) sprayed HA on the leaves of P. edulis plants, inducing an increase in seedling biomass. Furthermore, HA could induce modifications in the ultrastructure of roots and trigger the emergence and production of secondary roots, root hairs, and root elongation through nitric oxide and auxin signal transduction pathways (Elmongy et al. 2020). Nunes et al. (2019) reported that the effects of HA on maize root architecture, such as induction of lateral root growth and biomass increase, were accompanied by changes in proteins involved in energy metabolism, protein folding, cytoskeleton organization, RNA processing, stress response, N assimilation, transport of proteins, and vesicle transport.

Compounds in SE may act as signaling molecules regulating key pathways at the transcriptional and/or posttranslational levels, causing differential expression of essential genes in crops that contribute to increased plant growth and abiotic stress resilience (Deolu‐Ajayi et al. 2022). Ashour et al. (2023) illustrated that root length, leaf area, plant FW, fruit weight, yield, and total phenolic content of strawberries were significantly improved by foliar spray with a commercial seaweed liquid extract TAM® (50%) compared with control. SE treatment increased phenylalanine levels leading to induce PAL activity of the maize plants (Shukla et al. 2019), and the increased phenylalanine levels also induced the phenylpropanoid pathway, an epicenter of defense-related metabolites (Nephali et al. 2021). Phenylalanine may act as a precursor of secondary metabolites, such as flavonoids, alkaloids, and phenylpropanoids, and as a stress-related signal (Trivedi et al. 2018b). In our study, HA and SE might affect the PAL activity of Passiflora plants and generate a large number of precursors of flavonoids, thereby increasing the production and synthesis of OR and IV in those plants. It is worthy to study on analyzing the PAL-related genes and PAL activity and determine optimal application concentrations of HA and SE. In addition, Al-Rawi and Al-Hadethi (2016) reported that foliar application of SE at 0.2% and 0.4% significantly increased higher total leaf area and chlorophyll content in peach trees compared with controls. The foliar spray of SE was more efficacious in increasing vegetative growth, yield, fruit chemical and physical characteristics, and leaf nutritional status than untreated trees in grape (El-Sese et al. 2020; Irani et al. 2021; Omar et al. 2020) and apple cultivars (Mosa et al. 2023). Marhoon and Abbas (2015) suggested that 6 mL·L−1 of SE-treated sweet pepper plants had remarkable increases in plant height, number of branches, and percentage of shoot dry matter. Yildiztekin et al. (2018) observed that SE treatments increased vegetative growth in pepper plants at all concentrations applied under saline conditions.

The concentration of bioactive molecules in HA or SE and the amount applied to plants are critical considerations, as HA or SE at higher concentrations exhibit toxic effects on plant growth and development (Pizzeghello et al. 2020). Under high concentrations, it is more likely that HA accumulates in pores and blocks water flow, resulting in stunted growth (Rathor et al. 2023). An optimal concentration of HA- and SE-treated plants would increase plant growth and leaf functional compounds. As the concentration of HI increased, TP and TF content in ‘Tainung No. 1’ increased and decreased, respectively, indicating that TP and TF contents were affected by HI treatments (Table 1). In addition, different HI and HS treatments also displayed variations in their TP and TF content in P. suberosa, where HI-3 and HS-3 treatments stimulated higher TP and TF content than other treatments and controls (Table 2). Furthermore, in ‘Tainung No. 1’, SI-3 and SS-3 treatments also stimulate higher TF and TP content, respectively, than controls (Table 3), whereas SS-3 and SS-4 treatments stimulated both TF and TP content in P. suberosa compared with controls (Table 4). All TP contents were higher than TF regardless of biostimulant treatments, and generally, TP and TF contents in ‘Tainung No. 1’ were notably higher than in P. suberosa plants under HA and SE treatments. Interestingly, both TP and TF content in P. suberosa slowly increased as the SS concentration increased. Particularly, HI-treated ‘Tainung No. 1’ plants stimulated higher TP (>12 mg GAE per plant) and TF content (>6 mg RE per plant) compared with HS, SI, and SS treatments (Tables 1 and 3), whereas SS-treated P. suberosa plants stimulated higher TP (>10 mg GAE per plant) and TF content (>2 mg RE per plant) compared with HI, HS, and SI treatments (Tables 2 and 4). Therefore, ‘Tainung No. 1’ and P. suberosa plants subjected to HI-2 and SS-4 treatment, respectively, are recommended for supporting the ecological intensification of agriculture and contributing to developing biostimulants for more TP and TF content.

Biostimulation promotes the modulation of phytohormones such as auxins, ethylene, and gibberellins, and the chemical priming effect of HA might induce the synthesis of secondary metabolites (Canellas et al. 2020; Santos-Jiménez et al. 2022). In addition, SE contains various organic compounds such as polysaccharides, laminarin, ulvans, alginates, galactans, and many other bio-molecules that potentially enhance plant growth and development as well as trigger priming and resistance to stresses (Hassan et al. 2021a; Tinte et al. 2022). Many commercial products derived from SE have been developed and their effectiveness demonstrated (Ashour et al. 2020; Hassan et al. 2021b; Shukla et al. 2019). Ashour et al. (2021) demonstrated that yield, chlorophyll, ascorbic, phenolic compounds, flavonoids, and total nutrients of the pepper plants were significantly improved in all SE treatments compared with controls. We investigated the effects of biostimulants on leaf growth and secondary metabolite accumulation in Passiflora species. Application of HA and SE can efficiently determine biostimulant-induced changes in TP and TF content in Passiflora species and allows the exploration of specific varietal responses to individual biostimulants. Functional constituents in the leaves of Passiflora plants contain antidepressant and anti-anxiety effects beneficial to human health and fitness. Flavanols in plant tissues are mostly in the form of O-glycosides, and flavones are mainly represented in plants by C-glucosides of apigenin and luteolin. Schäfer et al. (2022) reported that OR and IV of P. incarnata plants are substrates of organic anion transporting polypeptides and affect transporter-mediated estrone 3-sulfate uptake. In Figs. 1 and 2, when genotypes were compared across HI, HS, and SS treatments, ‘Tainung No. 1’ plants exhibited remarkably higher OR and IV content than P. suberosa plants in all treatments. In addition, notably higher OR and IV contents were stimulated by SI and SS treatments (>100 mg per plant) than by HI and HS treatments (<100 mg per plant) in all plants. Thus, we recommend that Passiflora plants be subjected to SS-4 treatment (1.00 g·L–1) and that SE be exploited to maximize OR and IV content for all their beneficial applications and sustainable use in agriculture. Our findings can help Passiflora producers select varieties and apply HA or SE to achieve their goals for leaf production and accumulation of secondary metabolite content and develop stable and reliable functional food products. Both HA and SE can be used as environmentally friendly, multifunctional biostimulants in agricultural for more sustainable production, in addition to reducing the use of hazardous synthetic fertilizers.

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  • Fig. 1.

    The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different humic acid treatments. Means within the same humic acid irrigation (HI) or humic acid spraying (HS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be independent on the other.

  • Fig. 2.

    The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different seaweed extract treatments. Means within the same seaweed extract irrigation (SI) or spraying (SS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be dependent on the other.

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Yu-Chiao Chung Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Cheng-Hsuan Chen Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Yu-Sen Chang Department of Horticulture and Landscape Architecture, National Taiwan University, Taipei 106, Taiwan

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Kuan-Hung Lin Department of Horticulture and Biotechnology, Chinese Culture University, Taipei 111, Taiwan

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Chun-Wei Wu Department of Horticulture, Hungkuo Delin University of Technology, No. 1, Ln. 380, Qingyun Rd, Tucheng Dist, 236302 New Taipei City, Taiwan

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Contributor Notes

Y.C.C. and K.-H.L. contributed equally to this work.

Y.-S.C. and C.-W.W. are the corresponding authors. E-mail: yschang@ntu.edu.tw and hunterwu@mail.hdut.edu.tw.

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  • Fig. 1.

    The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different humic acid treatments. Means within the same humic acid irrigation (HI) or humic acid spraying (HS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be independent on the other.

  • Fig. 2.

    The content of orientin (A, C) and isovitexin (B, D) in ‘Tainung No. 1’ (black) and Passiflora suberosa (gray) leaf with different seaweed extract treatments. Means within the same seaweed extract irrigation (SI) or spraying (SS) treatment of the two species followed by different lowercase letters and capital letters in ‘Tainung No. 1’ and P. suberosa, respectively, significantly differ at P ≤ 0.05 by the least significant difference test. Each treatment was assumed to be dependent on the other.

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