Physiological and biochemical effects elicitors on melon cultivated in area with root rot history

doi:10.21203/rs.3.rs-4688662/v1

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Physiological and biochemical effects elicitors on melon cultivated in area with root rot history

https://doi.org/10.21203/rs.3.rs-4688662/v1

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Rot in the root system is one of the main diseases of melon, which causes significant losses in yield. Therefore, increasing plant resistance levels can be a viable strategy for the management of this disease. Thus, the objective of this study was to know the physiological and biochemical effects of resistance elicitors on melon cultivated in an area with history of root rot. During the study, three experiments were conducted, one preliminary in masonry beds and two identical under field conditions. In the preliminary experiment, three abiotic elicitors (salicylic acid, Agro Mos® and Bion®) were applied alone and associated with a biotic elicitor (Compost Aid®). The treatments that promoted the lowest disease severity levels were selected (unpublished data), and the field experiments were conducted on a melon-producing farm. In the field experiments, a randomized block design was used, with five treatments and four replicates with eight plants each. The treatments were: standard (Management adopted by the farm), Bion®, Compost Aid®, Bion® + Compost Aid® and absolute control. Epidemiological, biochemical and physiological variables were evaluated. The association Bion® + Compost Aid® reduced the disease severity index by 68.1 and 65.4% compared to the absolute control and the standard, respectively. The elicitors Bion® + Compost Aid® when applied in association activate plant defense through increments in peroxidase, catalase and polyphenol oxidase enzymes and positively influence gas exchange and chlorophyll content.

Antioxidant

Cucumis melo L.

Soil-inhabiting fungi

Induced resistance

Melon (Cucumis melo L.) has great economic importance worldwide, especially in China, the world’s largest producer (FAO, 2023). In Brazil, the Northeast region is the main melon producer, concentrating 96.8% of the national production (IBGE, 2023). However, the yield of this crop can be reduced by many pathogenic agents.

Many pathogenic agents affect the melon crop in Brazil, including fungi, responsible for large yield losses, mainly resulting from damage to the root system, which leads to rot and death of plants (Nascimento et al., 2018). Root rot, one of the main diseases of melon, has different causative agents reported, including the fungi Fusarium solani (Mart) Sacc., Macrophomina phaseolina (Tassi) Goid., Monosporascus cannonballus Pollack & Uecker and Rhizoctonia solani Kühn, which may attack the root system of plants separately or in association (Porto et al., 2016; Negreiros et al., 2019).

This disease has been occurring in different areas of cucurbit cultivation in arid and semi-arid regions around the world, causing significant economic losses (Negreiros et al., 2019; Castro et al., 2020). The management of these phytopathogens is difficult, since they have the ability to survive in the soil and in crop residues for long periods, even under unfavorable conditions, because they have resistance structures (Nascimento et al, 2018; Melo et al., 2021). Thus, using resistant cultivars is the best disease control strategy, but commercial melon cultivars resistant to root rot do not exist in Brazil (Linhares et al., 2020).

Currently, in Brazil there is no registered chemical for controlling soil-inhabiting root pathogens (Agrofit, 2023). One of the possible alternatives for the management of diseases caused by soil-inhabiting pathogens is the use of resistance-inducing products (Aleandri et al., 2010; Oliveira et al., 2016). These products, whether biotic or abiotic, activate plant defense mechanisms, stimulating the production of reactive oxygen species (ROS) and formation of phenolic compounds, promote lignification of tissues and favor the accumulation of pathogenesis-related (PR) proteins (Berger et al., 2016). The production of ROS leads to a hypersensitivity response (HR), through which rapid cell death occurs at the site of infection, aimed at delimiting the growth of the pathogen, after which the uninfected parts of the plant develop systemic resistance to the pathogen (Oliveira et al., 2016).

It is important to highlight that excess ROS cause oxidative damage to cells, and plants have a sophisticated antioxidant system against that (Berger et al., 2016). As part of this antioxidant system, the enzymes catalase (CAT), peroxidase (POX) and polyphenol oxidase (PPO) stand out (Chen et al., 2010). These enzymes, in addition to performing an antioxidant function, catalyze lignin formation, favoring the formation of defense barriers and strengthening the cell wall (Thilagavathi et al., 2007).

Positive results with the use of resistance inducers in the control of fungal diseases have already been reported for several crops of economic interest, such as bean (Berger et al., 2016), tomato (Ferraz et al., 2014), rice (Shasmita et al., 2019) and soybean (Lorenzetti et al., 2018). Thus, the objective of this study was to know the physiological and biochemical effects of resistance inducers on melon cultivated in an area with history of root rot.

2.1 Experimental Area Location and Characterization

During the study, three experiments were conducted, one preliminary in plant beds and two under field conditions. In the preliminary experiment, three abiotic elicitors (salicylic acid, Agro Mos® and Bion®) were applied alone and associated with a biotic elicitor (Compost Aid®). The treatments that promoted the lowest disease severity levels were selected (unpublished data), and the field experiments were conducted on a melon-producing farm (5°0’26.54” South, 37°23’53.16” West).

Before setting up the experiments, single soil samples from the 0–20 cm depth were collected in the experimental area of the farm to obtain a composite sample. The analysis of soil chemical components was performed based on the methodology proposed by Embrapa (Embrapa, 2017). The analysis showed the following values: pH = 7.0; OM = 15.9 g kg^− 1; Ca²⁺= 2.6; Mg²⁺= 0.9; Na⁺= 0.13; K⁺= 0.3; Al³⁺= 0.0 and H + Al = 0.0 cmol_c dm^− 3; P = 122.6; Cu = 1.5; Fe = 11.6; Mn = 53.6; Zn = 2.8 and B = 1.1 mg dm^− 3.

2.2 Experiment Conduction and Design

The experiments were conducted in an area with history of the disease located on a melon-producing farm in the municipality of Mossoró - RN. The melon hybrid used was ‘Goldmine’. Seedling transplanting and the other management practices were carried out as performed on the farm. Irrigation was applied through a fertigation line using the drip system.

The experimental design was randomized blocks (RBD), with five treatments and four replicates. Each plot was composed of one row with eight plants at spacing of 40 cm. The treatments were: standard, Bion®, Compost Aid®, Bion® + Compost Aid® (associated) and control (without application of products). The treatments were chosen based on the preliminary experiment, conducted in masonry beds, in which Bion® + Compost Aid® and Compost Aid® alone promoted the lowest values of disease severity. The standard treatment refers to the practices adopted by the farm, in addition to fertigation to maintain the appropriate nutritional aspects, based on soil analysis, with consolidated use of the fungus Trichoderma over the years of cultivation, to control root pathogens.

2.3 Preparation and Application of Treatments

Bion® (a product whose active ingredient is acibenzolar-S-methyl) was applied at the concentration of 1.0 g/20 L of water, as recommended by the manufacturer. The first application was performed seven days after transplanting the seedlings, and subsequently, three more applications were performed with intervals of seven days. The first two applications were carried out via soil, due to the use of a non-woven fabric (TNT), which hinders foliar application at the beginning of the cycle. Both foliar applications were carried out using a manual sprayer, and the leaves were sprayed until they were completely wet, a process carried out from 16:00 hours.

Compost Aid® (a product based on Bacillus subtilis, Enterococcus faecium and Lactobacillus plantarum) was applied three times during the experiment, the first application at seven days after transplanting (3 kg/ha), and the other applications at intervals of seven days, at a dose of 2 kg/ha (manufacturer’s recommendation). All applications were carried out via soil, with a graduated cylinder, using 50 mL of the solution per plant.

2.4 Variables Analyzed

At 65 DAT, the roots of the eight plants of each plot were collected and taken to the Laboratory of Phytopathology and Microbiology of UFERSA for epidemiological analysis. To calculate the disease severity index (DSI), the roots of the eight plants of each plot were classified from 0 to 5 using the scale of scores described by Ambrósio et al., 2015. The DSI was normalized for each treatment using the following equation: DSI= [(X₁×0) + (X₂×1) + (X₃×2) + (X₄×3) + (X₅×4) + (X₆×5)]/(X₁ + X₂ + X₃ + X₄ + X₅), where X₁, X₂, X₃, X₄, X₅ and X₆ are the number of plants with disease severity scores of 0, 1, 2, 3, 4 and 5, respectively (Huo et al., 2021).

For the enzymatic analyses, samples of melon leaves (middle third) were collected 12 hours after the last application of the treatments. These samples were placed in a thermal box containing ice and transported to the Plant Biotechnology laboratory of the Federal Rural University of the Semi-Arid Region for weighing and processing, aiming at storage in a freezer (-80°C) for further analysis.

The leaf samples (0.5 g) were placed in mortar, where 25 mg of polyvinylpyrrolidone (PVP) and liquid nitrogen were added. Then, they were macerated with pistil and immediately after they received 2.5 mL of 100 mM sodium acetate buffer (pH 5.0) and 0.5 mL of EDTA (1 mM). The homogenate remained under 4 ºC in the centrifuge at 10,000 g for 10 minutes, and the obtained supernatant was considered as enzymatic extract (Bezerra Neto and Barreto, 2011). The enzymes analyzed were peroxidase (POX), polyphenol oxidase (PPO) and catalase (CAT), and hydrogen peroxide (H₂O₂) was quantified.

POX activity was estimated based on the difference in absorbance produced with guaiacol oxidation and together with the reduction of H₂O₂. For this, 25 µL of guaiacol (0.2 M) was mixed with 250 µL of hydrogen peroxide (0.38 M) and 1 mL of sodium phosphate buffer (0.2 M pH 6.0). The mixture was gently stirred, and the reaction was initiated with the addition of 25 µL of the protein extract. Readings were performed at 470 nm, every 10 seconds, for 1 minute. Enzymatic activity was estimated based on the difference of absorbance per minute and per weight of fresh sample. For the blank, the protein extract was replaced with distilled water (Bezerra Neto and Barreto, 2011).

For the spectrophotometric determination of PPO activity, 1.8 mL of the potassium phosphate buffer (0.05 M pH 6.0) was transferred to cryogenic vials. Then, 50 µL of protein extract and 50 µL of Catecol (0.1 M) were added. The mixture was stirred in vortex for 15 seconds and incubated for 30 minutes at 30 ºC. After incubation, the vials were transferred to ice bath, with addition of 100 µL of perchloric acid (1.4%), and the mixture was stirred again in vortex and left to rest for 10 minutes. For the blank, protein extract was replaced with distilled water. Readings were performed at 396 nm and the results were expressed in enzymatic unit (EU) per gram of fresh sample (Campos et al., 2007).

The spectrophotometric activity of CAT was determined according to the methodology proposed by Havir and Mchale (1987) with modifications by Azevedo et al. (1998). For this, 2.75 mL of potassium phosphate buffer (100 mM pH 7.5) and 100 µL of protein extract were added in cryogenic vials. Then, the reaction was initiated with the addition of 120 µL of H₂O₂, which was pipetted only at the time of readings. For the blank, potassium phosphate buffer was used. CAT activity was observed for 1 minute, with readings at time 0 and after 60 seconds at 240 nm wavelength, in quartz cuvettes. The results were expressed in µmol/min/mg protein. Protein concentration was analyzed by the Bradford method (Bradford, 1976). The results were expressed in enzymatic units min^− 1 mL^− 1.

For the quantification of H₂O₂, 75 µL of protein extract was added to Eppendorf® tubes and mixed with 75 µL of potassium phosphate buffer (10 mM pH 7.0) and 150 µL of potassium iodide (1 M). Then, the mixture was incubated for 30 minutes at ambient temperature and in the dark. For the blank, distilled water was used in place of protein extract. After that, readings were performed in a spectrophotometer at 390 nm (Quadros et al., 2019).

Physiological evaluations were performed at 50 DAT. Gas exchange was determined using an infrared gas analyzer - IRGA (Walz-Gfs-300), with airflow of 300 µmol s^− 1 and coupled light source of 1200 µmol m^− 2 s^− 1, with measurements between 8:00 a.m. and 10:00 a.m. The following variables were measured: photosynthetic rate (A) (µmol CO₂ m^− 2 s^− 1), stomatal conductance (gs) (mol m^− 2 s^− 1), internal CO₂ concentration (Ci) (µmol CO₂ m^− 2 s^− 1), transpiration (E) (mmol H₂O m^− 2 s^− 1), water use efficiency (WUE-A/E), instantaneous carboxylation efficiency (CEi = A/Ci) and leaf temperature (LT) (ºC). Chlorophyll A index, chlorophyll B index and chlorophyll A/B ratio were determined by the nondestructive method, using a portable chlorophyll meter (ClorofiLOG®, CFL 1030 model, Porto Alegre, RS), and the values were expressed in Falker chlorophyll index (FCI).

2.5 Statistical Analysis

Both experiments were conducted at the same time. A preliminary analysis of variance (ANOVA) was performed to determine whether there were significant differences between the two experiments, and whether the data could be combined. After finding that there was no difference between the experiments, another ANOVA was performed and the data were analyzed together, with the means compared by Tukey test at 5% probability level. The software program used was R (R-Core Team, 2020). The correlation plot was created in R using the corplot statistical package (Wei and Simko, 2017).

Under the field conditions, DSI was lower when the biotic (Compost Aid®) and abiotic (Bion®) elicitors were applied in association, not differing from Bion® applied alone (Fig. 1A). The association of elicitors promoted the highest concentration of H₂O₂, differing from the other treatments, except for Bion® applied alone (Fig. 1B). Following the same trend, the activity of the CAT enzyme was favored by the associated use of these resistance elicitors, with increments of 71.2 and 107.7% compared with the control and standard of the company, respectively (Fig. 1C). For POX, the associated use of elicitors promoted increments of 34.2 and 59.4% (Fig. 1D), while PPO activity increased by 15.2 and 14.9% compared to the control and standard of the company, respectively (Fig. 1E).

The associated use of Bion® and Compost Aid® elicitors favored the photosynthetic rate (A), not differing from Compost Aid® applied alone (Fig. 2A). Stomatal conductance (gs) was lower in the control compared to the other treatments, which did not differ from each other (Fig. 2B). The highest internal CO₂ concentration (Ci) was observed in the control treatment (Fig. 2C), which led to the lowest transpiration rate (E), differing from the other treatments (Fig. 2D).

The association of Bion® and Compost Aid® elicitors favored the carboxylation efficiency (CEi), promoting its highest value, differing only from the control treatment (Fig. 3A). For the water use efficiency (WUE) and leaf temperature (LT), there was no difference between treatments (Fig. 3B and 3C).

For chlorophyll A index, the lowest value was observed in the control, while the other treatments did not differ from each other (Fig. 4A). For chlorophyll B, there was no difference between treatments (Fig. 4B). Compost Aid® promoted the highest chlorophyll A/B ratio, differing only from the control (Fig. 4C).

There was a positive correlation between H₂O₂ and the defense enzymes CAT (0.48) and POX (0.33) (Fig. 5). CAT was positively correlated with A (0.44) and GS (0.31) (Fig. 5). The highest positive correlations for gas exchange occurred between A and CEi (0.77) and GS (0.71), and between GS and E (0.60) and CEi (0.51) (Fig. 5). CHLA was positively correlated with GS (0.67), A (0.61) and CEi (0.59) (Fig. 5). For DSI, the correlation was negative with H₂O₂ (0.58), CAT (0.51), A (0.41) and GS (0.32) (Fig. 5). Regarding gas exchange, the correlation was negative between Ci and CEi (0.86) and between A and Ci (0.59), while CHLA was negatively correlated with Ci (0.62) (Fig. 5).

The results of this study indicate that the biotic rhizobacteria-based elicitor (Compost Aid®) applied in association with the abiotic elicitor (Bion®), which has the active ingredient acibenzolar-S-methyl, promoted changes in H₂O₂ levels and oxidative metabolism, leading to reductions in the severity index of root system rot in melon. These reductions may be associated with the synergistic effect caused by the combination of the products, leading to an oxidative explosion, resulting in the formation of reactive oxygen species (ROS), including hydrogen peroxide (H₂O₂), superoxide anion (O₂⁻) and hydroxyl radicals (OH), which act as plant defense signaling molecules (Oliveira et al., 2016; Quadros et al., 2019; Jaiganesh and Kumar, 2018).

This increase in ROS production is necessary for a hypersensitivity response to occur, a process that involves the programmed death of cells adjacent to the infection, limiting the pathogen’s access to water and nutrients (Thakar and Sohal, 2013). However, ROS accumulation is highly toxic to plant cells, causing lipid peroxidation and cell death (Gupta et al., 2013). To combat this, plants have a sophisticated antioxidant system, composed of enzymes such as CAT, POX and PPO, which protect tissues against oxidative damage (Quadros et al., 2019). This behavior was evident with the results obtained in the present study.

In addition to performing antioxidant function, POX is also involved in the process of lignification of the cell wall, catalyzing the biosynthesis of metabolites such as phytoalexins and phenols for lignin formation (Berger et al., 2016; Li et al., 2015). CAT catalyzes the rapid decomposition of H₂O₂ into H₂O and O₂, a less reactive gas molecule, while PPO, besides being involved in plant defense mechanisms, catalyzes the oxidation of phenols into quinines anoxygenically (Shasmita et al., 2019).

Pearson’s correlation values show that the increase in the production of ROS, specifically H₂O₂, favors the synthesis of CAT, POX and PPO enzymes, promoting greater resistance of melon plants to root rot, reducing the disease severity index. The increase in the synthesis of these antioxidant enzymes makes plants withstand stress-induced restrictions, protecting cellular functioning, favoring their growth and development (Ahanger et al., 2020).

In relation to the physiological aspects, the treatments that had the lowest DSI were the ones that promoted the best results for gas exchange and chlorophyll indices. Naturally, in treatments with higher DSI, there was greater invasion of the vascular system by fungal pathogens, leading to the dissolution of the xylem cell walls, formation of tyloses and consequent reduction in the transport of water and nutrients (Argaez et al., 2020). Therefore, one of the ways plants react to the attack of a root pathogen is through stomatal closure, aiming at avoiding or reducing water loss (Li et al., 2015), causing decreases in gs, E and A, as observed in the present study.

As a result, there was a higher accumulation of Ci due to the higher DSI, which can be explained by the reduction of A, inhibiting carboxylation and biochemical fixation of carbon (Taiz et al., 2017). In addition, water limitation leads to nutritional deficiency, reducing the absorption of some nutrients, such as nitrogen and magnesium, resulting in leaf senescence (Argaez et al., 2020), with limitation to chlorophyll synthesis. The results of this study corroborate those mentioned above.

The association of Bion® + Compost Aid® and Compost Aid® alone reduce the disease severity index and positively influence gas exchange and chlorophyll indices. The elicitors Bion® + Compost Aid® applied in association activate plant defense through increments in peroxidase, catalase and polyphenol oxidase enzymes.

Availability of data and material

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

Statement of the authors

This statement acknowledges that each author has madea sub-stantial contribution to the manuscript and is willing to take public responsibility forits contents. Author(s) attest that all persons desig-nated as authors qualify for authorship and all those who qualify are listed. The corresponding author takes responsibility for the integrity of the work as a whole, from inception to published article.

Acknowledgments

The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their scholarships.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

CRediT authorship contribution statement

Francisco R. A. Figueiredo: Conceptualization, Investigation, Formal analysis, Writing – original draft. Afonso L. A. Freires: Investigation, Formal analysis. Igor V. P. da Silva: Investigation, Formal analysis. Jarlan L. S. Santos: Investigation, Formal analysis. José Janderson F. de Souza: Investigation, Formal analysis. Ana P. de Moura: Investigation, Formal analysis. Leonardo V. de Sousa: Formal analysis. Rui S. Júnior: Supervision, Writing – original draf. Andreia M. P. Negreiros: Supervision, Formal analysis, Writing – original draf. Márcia M. Q. Ambrósio: Supervision, Formal analysis, Writing – original draf.

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Reviewers agreed at journal
28 Aug, 2024
Reviewers invited by journal
24 Jul, 2024
Editor assigned by journal
23 Jul, 2024
First submitted to journal
18 Jul, 2024

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Physiological and biochemical effects elicitors on melon cultivated in area with root rot history

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Abstract

Figures

1. Introduction

2. Material and Methods

2.1 Experimental Area Location and Characterization

2.2 Experiment Conduction and Design

2.3 Preparation and Application of Treatments

2.4 Variables Analyzed

2.5 Statistical Analysis

3. Results

4. Discussion

5. Conclusions

Declarations

References

Status:

Version 1