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. 2024 Oct 15;30(10):1659–1671. doi: 10.1007/s12298-024-01511-z

The role of rhamnolipids in the growth and defense responses of passion fruit plants

Ting Yang 1, Jihu Li 1, Yongkai Mao 1, Han Wu 1, Mingjiang Lin 1, Lijuan Chen 1,✉
PMCID: PMC11534940  PMID: 39506996

Abstract

Rhamnolipids (RLs) are bioactive compounds that have gained a lot of attention for their potential applications in agriculture. However, the exploration of RLs in passion fruit plants remains limited. This study aimed to investigate the role of RLs in passion fruit plants growth and defense responses. Firstly, the results demonstrated that RLs act as plant growth regulators, significantly enhancing the survival rate and root system development of passion fruit seedlings propagated by cutting. Further analyses suggested that RLs may enhance photosynthetic capacity and modulate the accumulation of indoleacetic acid (IAA) and cytokinin (CTK) in passion fruit cuttings, thereby promoting plant growth and development. Additionally, this study revealed that RLs effectively reduced susceptibility to viral pathogen telosma mosaic virus (TeMV) in passion fruit plants compared to distilled water-pretreated controls, resulting in alleviated disease symptoms. Significant up-regulation of antioxidative enzyme activities and reducing substances were observed in RL’s-pretreated plants upon TeMV-inoculation compared to distilled water-pretreated ones. Moreover, RLs were found to promote other defense-related signaling pathways upon TeMV-inoculation in passion fruit plants, including salicylic acid (SA) accumulation and expression levels of defense-related genes such as pathogenesis-related gene (PR3), phenylalanine ammonia-lyase (PAL), transcription factors (TFs) WRKY and NAC. Collectively, these findings underscored the positive roles played by RLs both in promoting growth and eliciting defense responses within passion fruit plants. These results provided valuable insights for designing environment-friendly management strategies for cutting propagation as well as prevention and control measures against viral diseases in passion fruits.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12298-024-01511-z.

Keywords: Rhamnolipids, Cuttings, Telosma mosaic virus, Defense responses, Passion fruit

Introduction

Passion fruit (Passiflora edulis) is widely cultivated throughout tropical and subtropical regions of the world. In recent years, the cultivation of passion fruit has been actively promoted in China due to its high nutritional and economic value. The Chinese market currently faces an urgent demand for passion fruit seedlings that are both high-quality and cost-effective. Various methods are available for propagating passion fruit plants, including tissue culture, grafting, branch cuttings, and true seeds. The technique of cutting propagation, which involves the utilization of a portion of the plant's vegetative organs as cuttings inserted into an appropriate substrate to generate completely new plants, is widely regarded as one of the most effective methods for large-scale propagation of high-quality varieties (Du et al. 2016). For passion fruit, asexual reproduction using healthy stems produces seedlings that can preserve positive maternal traits while effectively reducing mutation rates during reproduction. Additionally, it has a faster development speed compared to other methods and requires less investment in component. Therefore, growing seedlings through cutting propagation is one of the primary techniques used for breeding passion fruit seedlings in China at present.

In reality, there are several issues associated with cutting propagation for passion fruit seedlings. The primary concern is how to increase the survival rate during this process. Rapid formation of a root system is essential for shoot development in branches after cutting. Previous studies have indicated that various regulators, particularly plant hormones, play important roles in the process of root formation during seedling cuttings (Ercisli et al. 2003; Zhao et al. 2014; Alizadeh and Dumanoğlu 2022; Durul and Aktas 2023). For instance, cuttings of Ulmus wallichiana treated with indolebutyric acid at a concentration of 2000 ppm exhibited the highest level of sprouting and the longest length of rooting (Nazir et al. 2020). Auxin and cytokinin (CTK) are the main types of plant hormones participating in the formation of shoot and root meristems in poplar cuttings (Zhao et al 2014). Additionally, Pan et al (2020) demonstrated that indole-3-acetic acid (IAA), ethylene (ET), and brassinosteroids exhibit positive modulatory effects on adventitious root formation in sweet potato cuttings, while CTK and jasmonic acid (JA) exert inhibitory influences.

In addition to the need for high-quality seedlings, the threats caused by various environmental stress factors is another important problem that needs to be addressed for the development of the passion fruit industry. Among these threats, viral pathogens bring a serious influence on passion fruit. The causal agents of passion fruit viral disease are diverse and include members of the genus Potyvirus (Wylie and Jones 2011; Fukumoto et al. 2013; Garcêz et al. 2015; Yu et al. 2021), Cucumovirus Begomovirus (Gioria et al. 2011), Carlavirus (Spiegel et al. 2007), Begomovirus (Vaca-Vaca et al. 2017), and Cilevirus (Moraes et al. 2006). The occurrence of telosma mosaic virus (TeMV, genus Potyvirus) infection in passion fruit plants was first identified in Thailand (Chiemsombat et al. 2014). Subsequently, diseases caused by TeMV in passion fruit were reported in some areas of China, including Fujian province (Chen et al. 2018b), Hainan province (Yang et al. 2018) and Guangdong province (Chen et al. 2020). Passion fruit plants infected with TeMV exhibit severe disease symptoms such as mosaic and distorted leaves, mosaic skin on green fruit, and decreased fruit size (Chen et al. 2018b). To mitigate yield and quality losses caused by these pathogens, some chemicals have been used in production. However, long-term application of chemical agents in orchards has led to serious problems like microbial resistance, environmental pollution, and food safety concerns. Therefore, it is imperative to urgently develop a safe and efficient method for preventing and managing viral pathogens affecting passion fruits to ensure sustainable growth of this industry.

With their environment-friendly nature, high biodegradability, low toxicity, and effectiveness even at extreme conditions, biosurfactants are considered promising materials for agricultural applications such as seedling breeding, growth promotion, and disease control. Rhamnolipids (RLs) are surface-active compounds that belong to the class of glycolipid biosurfactants mainly produced by the Pseudomonas and Burkholderia genera (Platel et al. 2022). Previous studies have demonstrated that RLs can effectively control plant pathogenic diseases in agriculture. For instance, Goswami et al (2015) showed that RLs inhibit infection caused by the pathogenic fungus Colletotrichum falcatum to treat red rot disease in sugarcane. Borah et al (2015) found that RLs produced by Pseudomonas aeruginosa SS14 completely suppress wilt caused by Fusarium oxysporum f. sp. pisi in Pisum sativum. Additionally, RLs have been shown to induce resistance against Alternaria alternata infection in cherry tomatoes through their response to oxidative stress by triggering antioxidant enzymes production to eliminate excessive reactive oxygen species (ROS) (Yan et al. 2016). Monnier et al (2020) reported that semipurified mixes of RLs can protect Brassica napus against Leptosphaeria maculans infections and trigger expression of some defense-related genes. Furthermore, it was reported that RLs can protect wheat against Zymoseptoria tritici primarily through direct antifungal activity without a major impact on leaf physiology (Platel et al. 2022). However, most previous studies have focused on preventing or managing plant diseases caused by fungal and bacterial pathogens. By contrast, there is a relative scarcity of research on the role of RLs in preventing and controlling viral diseases in plants.

Previous studies have suggested the potential of RLs in agricultural applications, yet there is lack of consistent research on their use in passion fruit plants. Understanding the effects of RLs on the growth and defense responses in passion fruit plants can promote sustainable and eco-friendly development within the industry. Therefore, this study aims to analyze the impact of RLs on the growth and development of passion fruit cutting seedlings, as well as investigate their role against viral pathogen attacks. The results obtained from this study demonstrated that RLs improve survival rate during cutting propagation and promote seedlings growth while also reducing susceptibility to viral pathogens such as TeMV by promoting several defense-related signaling pathways within passion fruit plants. These findings provided valuable reference for designing new environment-friendly management strategies for cutting propagation and virus control within the passion fruit industry.

Methods and materials

Raising passion fruit seedlings through cuttings

Select vigorous stems that are free from pests and disease, with buds measuring approximately 10 cm in length as passion fruit cuttings. Leave a flat incision of about 2 cm at the upper end and make a diagonal cut at the lower end of each cutting. Disinfect the cuttings by soaking them in a solution of abamectin (5 mL/L) for approximately 15 min, followed by a 30-min soak in distilled water. Drain the treated cuttings before using them in subsequent experiments. Next, prepare the substrate for the cuttings by mixing yellow mud with RLs aqueous solution (0.5 g/L) at a mass ratio of 1:6 for the experimental group (RLs group), and yellow mud with water at a mass ratio of 1:6 for the control group (Mock group). Place the substrate into seedling pots measuring 85 mm in diameter and 70 mm in height, followed by inserting the treated cuttings to a depth of 2–3 cm. The saturation of seedlings’ roots is achieved by pouring water from below into their basins. Two types of root water are used: distilled water and 0.5 g/L RLs solution. After these treatments, the seedlings, along with their basins, were placed inside a temperature-controlled growth chamber set to maintain an average temperature of 27 °C while providing moisture and shade conditions with relative humidity range between 80 and 90%. Shading was applied at a rate between 75 and 85%. Additionally, irrigation was performed twice weekly using either water or 0.5 g/L RLs solution. After several weeks, the survival rate of cuttings was assessed, and other relevant indicators were also measured.

Morphological analysis of plants

Several morphological analyses were performed on plants from different groups. For statistical analyses, at least 10 different plants were measured. Plant height was determined using a ruler. Root elongation was measured using IMAGE J software (https://imagej.nih.gov/ij/). Fresh and dry weights were assessed using an analytical balance (Eppendorf, Germany).

Measurement of chlorophyll content and photosynthesis

The photosynthetic pigments were extracted from fresh leaves using 80% acetone at a temperature of 80 °C for 10 min, followed by cooling to room temperature and centrifugation. The resulting supernatant was spectrophotometrically analyzed for pigment quantification, following the methods described by Wellburn (1994). In this study, the photosynthetic pigments assessed included chlorophylls (Chl) a and b, as well as carotenoids. Stomatal conductance, net CO2 assimilation, and transpiration rate were measured using the portable photosynthesis system TPS-2 (PP Systems Company, England), according to the manufacturer’s instructions.

Plant cultivation and virus inoculation

Passion fruit seeds were cultivated in a temperature-controlled growth chamber maintained at an average temperature of 27 °C. The irradiation dose was 100 μM m−2 s−1 with a 16-h light/8-h dark cycle. Seedlings at the five-leaf stage were used for pathogen treatments. Two leaves from the bottom insertions were mechanically inoculated with TeMV. The viral isolates of TeMV, which were isolated from field disease samples by ourselves according to Koch's rule, were maintained in an aqueous suspension of 0.02 M sodium phosphate buffer (PBS) at 4 °C. Corresponding leaves of the control plants were mock-inoculated with PBS.

Measurement of virus content

The virus accumulation in TeMV-inoculated plants was measured using an enzyme-linked immunosorbent assay (ELISA) kit (Jiangshu Meibiao Biotechnology Co., Ltd., Yancheng, China), following the manufacturer’s instructions.

Oxidative damage estimation

The oxidative damage was reflected by electrolyte leakage and lipid peroxidation. Electrolyte leakage was assayed using a conductivity meter (Hanna Instruments) following the previously described methods (Chen et al. 2018a). The conductivity of the fresh leaves was recorded as C1. Then, the fresh samples were boiled for 15 min to achieve 100% electrolyte leakage (C2). The extent of electrolyte leakage was expressed as relative conductivity of plasma membranes [(C1/C2) × 100%]. Lipid peroxidation was estimated by measuring thiobarbituric acid-reactive substances (TBARS), following the previously described methods (Xi et al. 2007).

Determination of antioxidant enzymes

For the enzyme assays, 0.3 g of fresh leaf tissues were ground with 3 mL ice-cold 25 mM Hepes buffer (pH 7.8) containing 0.2 mM EDTA, 2 mM ascorbic acid, and 2% (w/v) polyvinylpyrrolidone. The homogenates were then centrifuged at 4 °C for 20 min at a speed of 12,000 × g, and the resulting supernatants were used to determine the activities of antioxidant enzymes. The activities of ascorbate peroxidase (APX), catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) were assayed using previously described methods (Chen et al. 2018a).

Determination of reducing substances

The levels of ascorbic acid (ASA) and reduced glutathione (GSH) were determined using an A009-1 assay kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China) and an A061-1 assay kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China), respectively, following the manufacturer’s recommended protocols.

Determination of IAA, CTK, SA, JA, and ET contents

The contents of IAA and CTK in the roots of passion fruit cutting seedlings were quantified using ELISA kits (Jiangshu Meibiao Biotechnology Co., Ltd., Yancheng, China) (Yang et al. 2022; Xu et al. 2024). Initially, the root samples were homogenized in PBS with liquid nitrogen at a weight/volume ratio of 10% tissue homogenate (9 times PBS volume). Subsequently, the homogenate was centrifuged at 2500 rpm for 20 min, and the resulting supernatant was used for IAA and CTK detection following the manufacturer's instructions. The specific procedures involved coating an ELISA plate with purified hormone, adding a detection antibody labeled with horse radish peroxidase to bind any target antigen already attached to the plate, forming an antibody-antigen-enzyme-antibody complex. Finally, tetramethyl benzidine (TMB) was added to the plate and the reaction converted TMB into a colored product. The change in color was measured spectrophotometrically at a wavelength of 450 nm. By comparing calibration curves generated from pure IAA and CTK standards, the concentration of each hormone in the samples was determined. Meanwhile, SA and JA concentrations in passion fruit leaves were quantified by high-performance liquid chromatography-mass spectrometry from crude plant extracts, employing previously established methods with some modification (Pan et al. 2010). In addition, the ET content in passion fruit leaves was measured as described previously (Xu et al. 2012).

RNA extraction and quantitative real‑time PCR

The total RNA was isolated from passion fruit leaves using TRIzol reagent (Invitrogen, Carlsbad, CA, USA) according to the manufacturer’s instructions. The RNA content was determined by measuring absorbance at 260 nm. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis (Bio-Rad Laboratories, Hercules, CA, USA) was performed to assess gene expression levels. cDNA amplification was carried out using SYBR Premix Ex Taq (TaKaRa Bio, Inc., Dalian, China). Target genes amplification was monitored for every cycle based on SYBR green I fluorescence. Each reaction was performed in triplicate for each of the three biological replicates. Amplification of the POPTR gene was used as an internal control. Relative quantification of target gene expression levels was performed using the comparative CT method (Livak and Schmittgen 2001). The primer sequences used in this study are shown in Supplementary Table 1.

Statistical analyses

The results are expressed as the means of at least three independent measurements, and the data were statistically evaluated using standard deviations and one-way analyses of variance (ANOVAs). Differences were considered to be statistically significant when P < 0.05.

Results

RLs enhance the development of root systems in passion fruit cutting seedlings

In practical production, the survival rate poses a significantly challenge in passion fruit cutting propagation. To enhance the quality and quantity of passion fruit cutting seedlings, RLs treatment was employed in this study. The results indicated that RLs treatment significantly improves the survival rate of passion fruit cutting seedlings compared to the mock group (Fig. 1a). The development of root systems plays a crucial role in cutting propagation, therefore, the development of root systems was examined in passion fruit cutting seedlings. The results indicated that the root systems exhibit more advanced growth in the RLs-treated group than in the mock group (Fig. 1b). Additionally, there is a significant increase observed in root length for the RLs-treated group compared to that of the mock group (Fig. 1c). Furthermore, the results showed a substantial elevation in fresh weight and dry weight of roots in the RLs-treated group as compared to those of the mock group (Fig. 1d, e). These results suggested that RLs can effectively enhance root system development in passion fruit cutting seedlings.

Fig. 1.

Fig. 1

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The survival rate of passion fruit cutting seedlings after approximately two weeks of growth (a); Root phenotype (b), root length (c), root fresh weight (d), and root dry weight (e) in passion fruit cutting seedlings after approximately three weeks of growth. “Mock” indicates seedlings treated with distilled water; “RLs” indicates seedlings treated with 0.5 g/L RLs. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

Considering the intricate regulation of cutting propagation by multiple plant hormones, particularly auxin and CTK as crucial regulators (Zhao et al. 2014), the accumulations of IAA and CTK were quantified in the roots of passion fruit cutting seedlings across different groups. These findings demonstrated a significant induction of IAA accumulation by RLs compared to the mock group (Fig. 2a). However, RLs were found to down-regulate CTK accumulation in the roots of passion fruit cutting seedlings compared to IAA accumulation (Fig. 2b). The results indicated that RLs promote the development of root system, which is associated with changes in the accumulation of IAA and CTK in passion fruit cutting seedlings.

Fig. 2.

Fig. 2

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The accumulation of IAA (a) and CTK (b) in the roots of passion fruit cutting seedlings after approximately three weeks of growth. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

RLs promote the growth of passion fruit cutting seedlings

After approximately six weeks of growth, it was observed that both the size and height of seedlings treated with RLs showed a significant increase compared to those in the mock group (Fig. 3a). The height of seedlings was measured, revealing a significant elevation in the RLs treatment group compared to that in the mock group (Fig. 3b). Additionally, RLs also exhibited an enhancing effect on both fresh and dry weights of the seedlings when compared to those in the mock group (Fig. 3c, d). Together, these results indicated that RLs can effectively promote the growth of passion fruit cutting seedlings, suggesting their potential application in passion fruits cultivation.

Fig. 3.

Fig. 3

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Phenotypic traits of passion fruit cutting seedlings after approximately six weeks of growth (a); Plant height (b), fresh weight of overground plant (c) and dry weight of overground plant (d) in these passion fruit cutting seedlings after approximately six weeks of growth. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

RLs enhance the photosynthetic system of passion fruit cutting seedlings

The photosynthetic system plays an indispensable role in the growth and development of plants. Therefore, an investigation was conducted on several parameters associated with plant photosynthesis. The results indicated a significant increase in the levels of chlorophyll-a and chlorophyll-b in passion fruit leaves when exposed to RLs (Fig. 4a, b). Carotenoids assist chloroplasts in absorbing light that chloroplasts cannot absorb, thereby enhancing photosynthetic efficiency. The content of carotenoids exhibited a similar trend to that of chlorophyll (Fig. 4c). Stomatal closure leads to a reduction in carbon dioxide absorption, subsequently decreasing plant photosynthesis. However, an increase in stomatal conductance can partially mitigate this effect and improve plant photosynthesis. Net CO2 assimilation is also referred to as the net photosynthetic rate. The findings indicated that RLs treatment significantly enhances both stomatal conductance and net CO2 assimilation in passion fruit leaves (Fig. 4d, e). Similarly, RLs treatment elevated the transpiration rate of passion fruit leaves (Fig. 4f). These results suggested that RLs have the potential to enhance the photosynthetic efficiency of passion fruit cutting seedlings.

Fig. 4.

Fig. 4

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Analysis of the parameters associated with photosynthesis in passion fruit cutting seedlings. Chlorophyll-a content (a), chlorophyll-b content (b), carotenoid content (c), stomatal conductance (d), net CO2 assimilation (e), and transpiration rate (f) in the leaves of passion fruit cutting seedlings after approximately six weeks of growth. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

RLs reduce the susceptibility of passion fruit plants to TeMV

Previous studies have demonstrated the antimicrobial and antifungal properties of RLs (Borah et al. 2015; Goswami et al. 2015). However, their potential as antiviral agents against viral pathogens in passion fruit plants has not been previously reported. Therefore, the efficacy of RLs as prospective antiviral agents against TeMV in passion fruit plants was evaluated. More severe disease symptoms were observed in the systemic leaves of passion fruit plants inoculated with TeMV without pretreatment with RLs (TeMV) compared to those on the TeMV-inoculated plants that had undergone pretreatment with RLs (RLs + TeMV) at 10 days post-inoculation (dpi) (Fig. 5a). The stunting and mosaicing on the systemic leaves in virus-inoculated plants were more pronounced compared to those that had received RLs pretreatment (Fig. 5a). Virus accumulation was quantified by ELISA in all TeMV-inoculated plants at 10 dpi, revealing a significant reduction in virus levels due to RLs pretreatment (Fig. 5b). Furthermore, expression analysis of the TeMV coat protein (CP) gene showed significantly lower levels in TeMV-inoculated plants that had undergone pretreatment with RLs than those without such pretreatment (Fig. 5c).

Fig. 5.

Fig. 5

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Disease symptoms of TeMV-inoculated passion fruit plants at 10 days post-inoculation (dpi) (a); ELISA analysis of the virus accumulation levels in TeMV-inoculated passion fruit plants (b); qRT-PCR analysis of the virus mRNA accumulation levels in TeMV-inoculated passion fruit plants (c); Electrolyte leakage (d) and TBARS content (e) in TeMV-inoculated passion fruit plants. “CK” indicates plants pretreated with distilled water and mock-inoculated with phosphate buffer; “RLs” indicates plants pretreated with 0.5 g/L RLs and mock-inoculated with phosphate buffer; “TeMV” indicates plants pretreated with distilled water and inoculated with TeMV; “RLs + TeMV” indicates plants pretreated with 0.5 g/L RLs and inoculated with TeMV. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

The assessment of oxidative damage, a crucial indicator of plant injury under stress conditions, was investigated by quantifying electrolyte leakage and TBARS levels at 10 dpi. Virus inoculation resulted in an increase in electrolyte leakage. However, TeMV-inoculated plants pretreated with RLs exhibited significantly reduced leakage compared to TeMV-inoculated plants without RLs pretreatment (Fig. 5d). The levels of TBARS showed a consistent trend with the electrolyte leakage (Fig. 5e). These findings suggested that RLs can enhance the tolerance of passion fruit plants against TeMV infection and mitigate cellular damage caused by virus attack.

RLs up-regulate ROS-scavenging enzymes and reducing substances in passion fruit plants in response to TeMV

In the following experiment, the activities of ROS-scavenging enzymes were quantified in different groups. The APX activity exhibited a significant increase in virus-inoculated plants compared to mock-inoculated plants. However, pretreatment with RLs further enhanced TeMV-induced up-regulation of APX activity compared to plants pretreated with distilled water (Fig. 6a). Similar trends were observed for CAT, POD, and SOD activities as seen with APX activity. The up-regulation of CAT, POD, and SOD activities induced by TeMV were further promoted by RLs (Fig. 6b–d). Additionally, the results indicated that RLs induced CAT, POD, and SOD activities in passion fruit plants even without virus inoculation except for APX (Fig. 6b–d).

Fig. 6.

Fig. 6

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Analysis of ROS-scavenging enzymes and reducing substance in TeMV-inoculated passion fruit plants. The activities of ROS-scavenging enzymes (a–d) and reducing substances (e and f) in TeMV-inoculated passion fruit plants at 10 dpi. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

Considering the important roles of reducing substances in mitigating ROS levels during plants’ response to pathogen attack, the levels of ASA and GSH were also assessed in different groups. After TeMV inoculation, a significant induction of ASA was observed, with a more obvious up-regulation in the plants pretreated with RLs (Fig. 6e). Additionally, TeMV infection resulted in an up-regulation of GSH accumulation in passion fruit plants. Notably, pretreatment with RLs further enhanced the up-regulation of GSH accumulation upon TeMV infection (Fig. 6f).

RLs affect several defense-related signaling pathways in passion fruit plants in response to TeMV

Signaling molecules SA, JA, and ET are crucial endogenous phytohormones that play a pivotal role in systemic immunity by mediating plant defense responses against pathogen attacks. The accumulations of these phytohormones were detected in TeMV-inoculated plants at 10 dpi. The results demonstrated significantly elevated levels of endogenous SA in all TeMV-inoculated plants compared to the mock-inoculated plants, with much higher levels observed in TeMV-inoculated plants pretreated with RLs (Fig. 7a). Additionally, it is noted that the accumulation of SA in passion fruits leaves is significantly induced by RLs pretreatment in the mock-inoculated group (Fig. 7a). The inoculation of TeMV resulted in the induction of JA accumulation in passion fruit plants. However, pretreatment with RLs did not exert any influence on the TeMV-induced JA accumulation compared to SA (Fig. 7b). The accumulation of ET was reduced upon TeMV inoculation in passion fruit plants compared to the levels of SA and JA accumulations. Furthermore, this decline resulting from virus inoculation remained unaffected by RLs pretreatment (Fig. 7c).

Fig. 7.

Fig. 7

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Analysis of phytohormones in passion fruit plant response to TeMV. The accumulation of SA (a), JA (b) and ET (c) in TeMV-inoculated passion fruit plants at 10 dpi. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

Next, the expression levels of several passion fruit defense-related genes, including PR3 (a pathogenesis-related protein gene), PAL (a gene involved in the phenylpropanoid pathway and related to SA biosynthesis), and LOX2 (a gene related to JA biosynthesis and involved in plants response to biotic stress), were analyzed in different groups (Santos-Jiménez et al. 2022). The expression level of PR3 was significantly upregulated by virus inoculation compared with mock-inoculated groups, and TeMV-induced upregulation of PR3 expression was further promoted by RLs pretreatment (Fig. 8a). Additionally, the expression level of PR3 was significantly induced by RLs pretreatment in the mock-inoculated group (Fig. 8a). The expression level of PAL exhibited a similar trend to that of PR3 (Fig. 8b). Virus attack also upregulated the expression level of LOX2. However, pretreatment with RLs did not exert any influence on TeMV-induced LOX2 expression in passion fruit plants (Fig. 8c). Compared to PR3 and PAL, there were no obvious differences in the expression level of LOX2 in mock-inoculated plants with or without RLs pretreatment (Fig. 8c).

Fig. 8.

Fig. 8

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qRT-PCR analysis of the expression levels of defense-related genes in TeMV-inoculated passion fruit plants at 10 dpi. The error bars represent the means and standard deviations of values obtained from three biological replicates at the indicated time points. Significant differences are denoted by different lowercase letters

Considering that transcription factors (TFs) are involved in plants’ defense against pathogens by modulating the expression of other defense genes or hormone signaling, the expression levels of several TFs were also detected in this study. The results demonstrated a significant increase in the expression levels of WRKY45 and WRKY47 in all TeMV-inoculated plants compared to mock-inoculated plants. Furthermore, RLs pretreatment significantly enhanced the up-regulation of WRKY45 and WRKY47 upon TeMV infection (Fig. 8d, e). The expression level of NAC100 was also up-regulated by TeMV inoculation, and RLs further enhanced its expression during virus infection in passion fruits plants (Fig. 8f). In contrast to WRKY45, WRKY47, and NAC100, the expression level of MYB43 was down-regulated by TeMV inoculation in passion fruit plants, and the down-regulation was not noticeably affected by RLs pretreatment (Fig. 8g). Additionally, the expression level of ERF4 was also down-regulated by TeMV inoculation, while the down-regulation of ERF4 expression caused by TeMV inoculation was further reduced by RLs (Fig. 8h).

Discussion

As representative members of biosurfactants, RLs have been extensively investigated for their potential agricultural applications. This study presented novel findings that demonstrate the active roles of RLs in promoting growth and defense responses in passion fruit plants. These research findings confirmed that the high efficacy of RLs in promoting seedling growth through cutting propagation, suppressing disease symptoms caused by TeMV inoculation, and inducing defense-related signaling pathways in passion fruit plants upon TeMV inoculation. These results provided valuable insights for the development of sustainable and environment friendly strategies for passion fruit cutting propagation and virus control in field applications which are currently lacking.

The results obtained in this study demonstrated that RLs function as plant growth regulators and significantly enhance the survival rate of passion fruit seedlings propagated by cutting. Additionally, other related events including root phenotype, root length, fresh weight, and dry weight of roots were analyzed in the passion fruit cutting seedlings after approximately three weeks of growth with RLs treatment (Fig. 1). These findings suggested that RLs can promote the development of root systems in cutting-propagated passion fruit seedlings. Notably, Sancheti et al (2020) also reported that RLs at a concentration range of 0.5–1 g/L could induce increased lateral root and shoot growth in soybean plants. The plant root system is a key factor related to seedling growth, and previous studies have reported that cutting-propagated seedlings would not be reproduced unless the adventitious roots are generated (Du et al. 2016). Several plant hormones have been identified as effective regulators promoting root development in cutting-propagated seedlings (Majeed et al. 2009; Pan et al. 2020; Ai et al. 2023). Zhao et al (2014) suggested that auxin and CTK are main types of plant hormones involved in shoot and root meristems formation in poplar cuttings. In this study, the results indicated that RLs up-regulate the accumulation of IAA but down-regulate the accumulation of CTK in the roots of cutting-propagated passion fruit seedlings (Fig. 2). Thus, it can be hypothesized that RLs promote root system development in passion fruit cutting-propagated seedlings by modulating these two types of plant hormones in their roots. In the future, RLs may be considered as a potential growth regulator to enhance survival rates during passion fruit propagation through cuttings. Additionally, considering that plant hormones do not act independently in influencing the rooting ability of cuttings, previous studies have suggested an antagonistic relationship between auxin and CTK during root development (Fukaki and Tasaka 2009). Some hormone levels are influenced by the physiological condition of the cutting during collection, while other are related to the plant’s genotype or rooting medium (Zhao et al. 2014). Therefore, further investigation is needed to elucidate how RLs modulate the interplay among plant hormones in passion fruit cutting seedlings.

Chloroplast pigments can serve as potential indicators for determining the photosynthetic capacity of plants (Riaz et al. 2021). The results presented here revealed that passion fruit seedlings treated with RLs exhibited elevated levels of chloroplast pigments, including chlorophyll-a, chlorophyll-b, and carotenoids (Fig. 4). Furthermore, RLs treatment also led to elevated stomatal conductance, net CO2 assimilation, and transpiration rate in passion fruit leaves (Fig. 4). Hu et al (2022) reported that the combined application of RLs and choline chloride in tomatoes resulted in increased chlorophyll content, net photosynthetic rate, transpiration rate, yield and quality of fruit. Based on these findings, it can be suggested that RLs may increase the photosynthetic capacity of passion fruit cutting seeding, and then promote plant growth and development as evidenced by increased plant size and weight (Fig. 3). These results highlight a positive role of RLs in enhancing seedling growth which could be proposed as an effective approach to improve both the yield and quality of passion fruit in agriculture practices.

The results presented in this study revealed that pretreatment with RLs reduced the susceptibility of passion fruit plants to TeMV and alleviated disease symptoms compared to plants pretreated with distilled water (Fig. 5). We sought to obtain the potential molecular mechanism underlying virus resistance in passion fruit plants induced by RLs. Previous studies have indicated that plants possess a diverse range of antioxidants, which play a crucial role in their defense against pathogen attacks. Khanam et al (2005) reported a significant increase in CAT activity under red light, leading to the inhibition of lesion formation in broad bean leaves infected with Botrytis cinerea. Piriformospora indica, a root endophytic fungus, enhances the antioxidant enzyme defense system in chickpea plants and protects them against the pathogenic fungus B. cinerea (Narayan et al. 2017). In this study, significant increases were observed in ROS-scavenging enzymes activities and reducing substances in TeMV-inoculated plants compared to mock-inoculated ones (Fig. 6). These findings are consistent with those of Chen et al (2018b), who reported an obvious increase in SOD and CAT activities in TeMV-infected passion fruit plants compared to healthy ones. Additionally, it was observed that significant up-regulation of antioxidative enzymes activities and reducing substances induced by TeMV inoculation in RLs-pretreated plants compared to distilled water-pretreated ones (Fig. 6). In fact, Yan et al (2016) demonstrated that exogenous RLs effectively reduce disease incidence caused by Alternaria alternata in cherry tomatoes through oxidative stress response mechanisms, such as increased expression of related genes like SOD and CAT2, as well as enhanced enzyme activities like APX and glutathione reductase while regulating ROS production. Hu et al (2022) found that RLs enhance cell antioxidation levels by increasing the contents of POD in tomato leaves, thereby effectively alleviating cell membrane damage caused by salt stress. Therefore, it could be proposed that RLs have a positive impact on antioxidant mechanisms in passion fruit plants, thereby contributing to their reduced susceptibility to TeMV.

The endogenous phytohormones SA, JA, and ET play crucial roles in orchestrating plant defense responses (Aerts et al. 2021). In this study, the levels of both SA and JA were significantly induced in all TeMV-inoculated plants, including the RLs-pretreatment and water-pretreatment groups. However, virus inoculation down-regulated ET accumulation in passion fruit plants (Fig. 7). These findings suggested that SA and JA may exert positive effects while ET plays a negative role in passion fruit plant defense against TeMV attack. Furthermore, the present results indicated that RLs pretreatment can effectively enhance SA accumulation in passion fruit plants upon TeMV inoculation (Fig. 7a). Nevertheless, minimal differences were observed in both JA and ET accumulation between the RLs-pretreatment and water-pretreatment groups after TeMV inoculation (Fig. 7b, c). Therefore, it is proposed that up-regulated SA accumulation following RLs pretreatment may be associated with an enhanced defense capacity against TeMV infection in passion fruit plants. Actually, previous studies have demonstrated that RLs-mediated resistance is regulated by different signaling molecules depending on the type of pathogen (Varnier et al 2009; Monnier et al. 2020). For instance, JA and ET play differential roles based on the pathogen’s lifestyle, while SA serves as a central signaling molecules in overall RLs-induced resistance (Sanchez et al. 2012). These previous findings highlighted how RLs modulate plant defense mechanisms through their impact on phytohormones-mediated resistance pathways during both bacterium and fungus infections. However, limited research has been conducted to investigate whether RLs can trigger or influence phytohormones-related defense pathway in plants responding to viral pathogens. Therefore, this present study is the first to show that RLs act as potent elicitor of phytohormones-mediated defense responses in plants upon viral pathogen attack.

PR proteins are among the defense activated locally and at distal parts of the plants (Van Loon and Van Strien 1999). In passion fruit plants, Parkinson et al (2015) found that acibenzolar-S-methyl enhances resistance to passion fruit woodiness virus in the plants is associated with the increase in the activities of two PR proteins, chitinase and β-1, 3-glucanase. The expression of PR3 in passion fruit plants was upregulated by a fungal glycoprotein, which can mitigate passion fruit woodiness disease caused by cowpea aphid-borne mosaic virus (Santos-Jiménez et al. 2022). The results of the present study showed that the expression of PR3 was significantly upregulated by virus inoculation, suggesting the PR3 participated in passion fruit plants response to TeMV attack. Moreover, RLs can further promote TeMV-induced upregulation of PR3 expression (Fig. 8a), potentially contributing to increased resistance against TeMV in RLs-pretreated passion fruit plants. Previous studies have suggested that the expression of PAL, involved in phenylpropanoid pathway, may lead to the production of SA and phenolic compounds, which function in plant defense against various pathogens attack. For instance, Kim and Hwang (2014) found that pepper PAL1 acts as a positive regulator of SA-dependent defense signaling to combat microbial pathogens via its enzymatic activity in the phenylpropanoid pathway. An increased expression level of PAL was observed in passion fruit plants after treatment with fungal glycoprotein, making the plants more tolerant to cowpea aphid-borne mosaic virus (Santos-Jiménez et al. 2022). The results of the present study indicated that RLs potentiate the expression of PAL after TeMV challenge (Fig. 8), reinforcing the potential positive role of PAL in the resistance of passion fruit plants induced by some elicitor. As an essential enzyme for JA biosynthesis, the expression of LOX participated in plant defense. The expression level of LOX2 was induced by glycoprotein in passion fruit plants with cowpea aphid-borne mosaic virus inoculation (Santos-Jiménez et al. 2022). The results of this study indicated that the expression level of LOX2 was induced by TeMV inoculation, whereas RLs has no obvious influence on the expression level of LOX2 in passion fruit plants induced by TeMV. These results reflected that elicitor-mediated resistances are regulated by different signaling pathways depending on the differences in the interactions between specific pathogens and their respective hosts.

TFs have been demonstrated to play a crucial role in plant defense against pathogens by modulating the expression of defense genes or hormone signaling pathways (Alves et al. 2014). Our previous study revealed that various TFs families are involved in the defense response of passion fruit plants against CMV infection, with notable up-regulation observed for WRKY and NAC gene families (Chen et al. 2021). In Brassica napus, it has been reported that RLs trigger the expression of BnWRKY33 and BnERF1, which confers protection against Leptosphaeria maculans infections (Monnier et al. 2020). In this study, the results demonstrated that TeMV inoculation induced the up-regulation of WRKY45, WRKY47, and NAC100, suggesting their active involvement in defending passion fruit plants against TeMV attack. Furthermore, it was observed significant down-regulation of both MYB43 and ERF4 expression upon virus inoculation compared to WRKY and NAC gene families. These results indicated distinct roles played by different members within TFs families during passion fruit plants’ response to virus challenge. Additionally, RLs promoted the up-regulation of WRKY45, WRKY47, and NAC100 induced by TeMV in passion fruits plants (Fig. 8). However, RLs further decreased the ERF4 expression level in passion fruit plants after TeMV inoculation. Therefore, it could be proposed that changes in the expression of these TF genes are closely associated with the increased defense capacity observed in RLs-pretreated passion fruit plants against TeMV inoculation. However, the underlying mechanism governing how RLs modulate these TFs-mediated defense pathways needs to be investigated in future studies.

In conclusion, the findings presented in this study indicated that RLs play a beneficial role in promoting the growth of passion fruit cuttings and enhancing defense responses of passion fruit plants against viral pathogens. These findings provided valuable theoretical references for cutting propagation and preventing and controlling virus diseases in passion fruit production. Further research is needed to elucidate the specific mechanisms through which RLs modulate these signaling pathways in passion fruit plants.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 13 KB) (13.1KB, docx)

Author contributions

LJC and TY contributed to the study conception and design. Material preparation, data collection and analysis were performed by TY, JHL, YKM and HW. MJL gave some beneficial suggestions for experiment operation. The first draft of the manuscript was written by LJC. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by the GDAS’ Project of Science and Technology Development (2020GDASYL-20200103050).

Declarations

Conflict of interests

The authors have no relevant financial or non-financial interests to disclose.

Footnotes

Publisher's Note

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