**1. Introduction**

The increased demands on fresh produce, fruits, vegetables, and herbs is challenged nowadays, with efforts focusing on the increasing yields and quality during the crop production. Moreover, efforts have also been targeted to decrease produce losses during the postharvest storage. As a consequence, the increased consumption of fresh produce has driven commercial desire for better storage and transportation conditions. There is an increased interest on effective sanitation means a decrease in postharvest losses due to decay, while maintaining fruit quality, including flavor, color, nutritional value, texture, and storability [1,2]. Non-single preservation means are efficient enough to be applied in a wide range of fresh produce, microorganisms, and environmental conditions, for each crop. Despite the fact that chemical applications in postharvest are of high effectiveness, there are significant challenges including current sanitation procedures and

**Citation:** Chrysargyris, A.; Rousos, C.; Xylia, P.; Tzortzakis, N. Vapour Application of Sage Essential Oil Maintain Tomato Fruit Quality in Breaker and Red Ripening Stages. *Plants* **2021**, *10*, 2645. https:// doi.org/10.3390/plants10122645

Academic Editors: Adriano Sofo, Laura De Martino and Hazem Salaheldin Elshafie

Received: 15 November 2021 Accepted: 30 November 2021 Published: 1 December 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

health and environmental concerns due to the possible generation of toxic by-products and residues [3–5]. Moreover, the use of chemicals as fungicides for postharvest sanitation is partially restricted in many countries [6]. Therefore, alternative, safe, eco-friendly but effective sanitizing agents are explored for the fresh produce preservation [7–11].

One candidate is the essential oils (EOs) derived from medicinal and aromatic plants (MAP) due to a wide range of biocidal activities, including antifungal [12–14], antibacterial [15–17], antioxidant [15,17], cytotoxic [18], and anti-inflammatory [19] activities, to name a few. Essential oils from a variety of plant species, including sage (*Salvia* spp.), have demonstrated bioactivity against a variety of plant diseases [7,20,21]. However, there has been not much research on the beneficial effects of the EOs application on the fruit quality of pears, tomatoes, eggplants, strawberries, and cherries [2,6,12,22,23], processed fresh produce [24] and cut flowers [25,26]. Although the strong aroma of EO can restrict the final product's organoleptic acceptability, it is known to have strong antioxidant and antimicrobial properties [7,27,28]. Recent research has revealed that EO (i.e., *Thymus capitatus*; thyme oil), can act as signaling compound. Therefore, EO application is triggering a signal to induce a defense mechanism in vegetables by increasing the activity of defense-related enzymes and increasing antioxidant ability [29]. Essentials oils can be both applied in aqueous and in vaporized phase, with the latter being an advantage for some commodities (i.e., strawberries and grapes) where aqueous sanitation is a limitation. The EO's antimicrobial activity is linked to its hydrophobic properties, which allow it to penetrate into microbial cells' phospholipid membranes, causing structural disorder and permeability [30]. However, the use of EOs in high levels is restricted due to probable unfavorable sensory effects, and as a result of that, the concentrations used need to be optimized for each commodity.

Tomatoes (*Solanum lycopersicum* Mill.) are harvested at different stages of ripeness to meet various consumption needs (e.g., fresh and processed). For red-fleshed tomatoes, six ripeness stages (i.e., green, breaker, turning, pink, light red, and red) are described based on the surface color [31]. Breaker-turning ripeness stage is used for longer fruit storage and transportation. Tomato is a climacteric fruit with a limited postharvest life due to the elevated levels of respiration, transpiration, ethylene emission and postharvest decay, resulting in an increased ripening process and senescence [32,33]. Tomato ripening is accompanied with chlorophyll break down, lycopene accumulation, tissue softening, and shifts in aroma and other compositional properties [34]. Following harvest, the fruit continues to have several biochemical changes on quality and deteriorates rapidly. In some cases, fruit deterioration can be during or after transport and marketing. Tomatoes are stored at comparably high temperatures (10–12.5 ◦C) depending on the maturity stage to prevent chilling injury which is evidenced at lower temperatures, below 7–10 ◦C [35].

Only fresh produce that meets the consumer's standards is suitable at the market interface. As a result, it is vital to assess the impact of potentially revolutionary applications on the sensory and organoleptic features of fruits and vegetables. Sage EO has been effective in fruit quality and observed antimicrobial activity [23,36]. The goal of this study was to examine if the vapor phase of essential oils obtained from sage (*Salvia trilova* L.) had any effect on tomato fruit quality attributes including: (i) physiological parameters (including weight loss, fruit firmness, and rates of respiration and ethylene production); (ii) fruit chemical composition (for example, vitamin C content, antioxidant capability, organic acid content (citrate), total soluble solids, carotenoids (lycopene, *β*-carotene) and total phenolic content) and damage index; and (iii) sensory qualities as determined by a consumer panel under controlled settings.

#### **2. Results**

The experimental lay out is presented in Figure 1, with tomato fruits exposed to sage EO (50 or 500 μL L<sup>−</sup>1) during storage for up to 2, 7, and 14 days or exposed to EO for 7 days and then stored to chilled conditions for an additional 7 days.

**Figure 1.** Layout of experiments: Tomato fruit were exposed to ambient air or essential oil (EO: 50 or 500 μL L<sup>−</sup>1) in the dark at 11 ◦C and 90% RH. Experiment 1: Tomato fruit were exposed to air or EO for 2, 7, and 14 days and sampling took place during exposure (sustain effect—SE) to air or EO. Experiment 2: Tomato fruit were exposed to air or EO for seven days, and then transferred for additional seven days to air. Sampling took place following EO exposure (memory effect—ME) at 14 days of storage. Air ( ), EO exposure (→). Tomato exposed to air , tomato exposed to EOs .

### *2.1. Fruit Decay*

Neither the EO-treated nor the control fruit showed signs of degradation until day 7 of the storage period. At the end of the trial (day 14), control fruit showed evidence of deterioration (assessed as 2.05 and 2.75 on a 1–5 scale, for breaker and red fruit, respectively) [principally symptoms of anthracnose rot (caused by *Colletotrichum coccodes*) and secondary symptoms of black spot] (caused by *Alternaria alternata*)] as shown in Table 1.

**Table 1.** Effect of sage essential oil (EO) of tomato fruit decay at breaker and red ripening stage, exposed to ambient air (control) or EO (50 or 500 μL L<sup>−</sup>1) for 14 days (Sustain effect—S) or up to 7 days and then transferred to ambient air for an additional 7 days (memory effect—M). Fruit were maintained throughout at 11 ◦C and 90% RH. The degree of infection on fruit was rated using a scale of 1 to 5 (1-clean, no infection; 2-trace infection; 3-slight infection; 4-moderate infection; 5-severe infection).


Values represent the mean (±SE) of evaluation made on eight independent fruit per treatment per storage period. Values followed by the same letter in each column do not differ significantly (*p* < 0.05). Symbols of \* indicating significance among controls through storage period.

### *2.2. Fruit Weight Loss, Firmness and Colour*

Fruit weight loss increased when storage time was extended, reaching 1.65% in control and in 1.32% in 500 μL L−<sup>1</sup> EO-treated breaker fruit after 14 days at 11 ◦C (Figure 2A) while the relevant values in red fruits were 1.61% and 1.17%, respectively (Figure 2B). Fruit weight loss (%) was at similar levels for both breaker and red tomatoes during 2 days of storage. However, fruit weight loss was significantly decreased (up to 45%) in EO-treated tomatoes after 7 and 14 days, comparing with fruits maintained throughout in ambient air at 11 ◦C (Figure 2A,B). Interestingly, the effects were persisted when fruit removed

from 50 μL L−<sup>1</sup> of EO exposure (including 500 μL L−<sup>1</sup> of EO for red tomatoes), and stored additionally for seven days (memory effect).

**Figure 2.** Impacts of sage essential oil (EO) on weight loss (%) and firmness (expressed in Newtons) of tomato fruit at breaker (**A**,**C**) and red (**B**,**D**) ripening stage, exposed to ambient air (control) or EO (50 or 500 μL L<sup>−</sup>1) for 2, 7, and 14 days (sustain effect—S) or up to 7 days and then transferred to ambient air for an additional 7 days (memory effect—M). Fruits were maintained throughout at 11 ◦C and 90% RH. Values represent mean (±SE) of measurements made on eight independent fruit per treatment and storage period. Means followed by different Latin letters significantly differ according to Duncan's MRT (*p* = 0.05).

The effect of EO and fruit ripening stage on the tomato firmness is presented in Figure 2C,D. Two days' storage in an EO-enriched atmosphere revealed no changes in the tomato firmness for breaker stage fruits, but maintained in red tomatoes. Tomatoesenriched with 50 μL L−<sup>1</sup> EOs maintained fruit firmness up to 14 days comparing with higher concentration (500 μL L−1) in both red and breaker fruits. However, when treated fruit was transferred to ambient air, breaker and red fruit previously exposed to 50 μL L−<sup>1</sup> EO remained substantially (*p* = 0.01) firmer than fruit subjected to 500 mg L−<sup>1</sup> EO storage conditions throughout.

Fruit colour was mainly affected by the storage and ripening stage of tomatoes rather than the EO application (Figure S1). At breaker stage, *L\** value was greater in 500 μL L−<sup>1</sup> EO application at 14 days of storage for both sustain and memory treatments (Figure S1A). Moreover, breaker-tomatoes revealed decreased chroma and *a\** value but increased *b\** value in 500 μL L−<sup>1</sup> EO application at 14 days of storage (Figure S1C,G). Red tomatoes revealed increased *L\** value at 2 and 7 days but decreased Chroma and *a\** value at high EO (500 μL L<sup>−</sup>1) application at 14 days of storage (Figure S1B,D,H).
