The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties

Daniel Tomescu; Radu Şumălan; Lucian Copolovici; Dana Copolovici

doi:10.1515/biol-2017-0016

Article Open Access

The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties

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Published/Copyright: May 4, 2017

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From the journal Open Life Sciences Volume 12 Issue 1

Abstract

Soil salinity is one of the best known stress factors of plants that can lead to crop yield reduction. Therefore, it is important to identify new tolerance varieties of plants that can grow on saline soils. We have studied the influence of salt on five different tomato varieties from the Western region of Romania and compared them with a commercial hybrid and found that one of them (Rudna) is a very salt-tolerant variety (up to 200 mM NaCl). The assimilation rates and stomata conductance of water vapour are affected by salinity but some of the local varieties of tomato exhibit quite good tolerance. We found that all plants under salinity stress emit (Z)-3-hexenol (a C6, green leaf volatile) and the emission of all terpenes increased in proportion to the salt concentration. The emission of three terpenes, (Z)-beta-ocimene. 2-carene and beta-phellandrene, have been quantitatively correlated with salt concentration.

Keywords: salt stress; Solanum lycopersicum L.; terpenes; green leaf volatiles; photosynthetic parameters

1 Introduction

Soil salinity is an important abiotic stress which results in severe economic loss due to decreased crop productivity through the energy cost incurred by the plant [1]. Over 400 million hectares of soils are affected by salinity in which electrical conductivity of the root zone exceeds 4 dSm⁻¹ at 25 °C [2]. In addition, climate change could result in increased soil surface salinity due to long periods of drought [3]. Soil salinity is caused by the weathering of calcareous rocks, long periods of drought, high surface evaporation, irrigation with saline water and unsustainable agriculture.

Salinity affects plants’ ionic balance, mineral nutrition, stomatal closure, and assimilation rate [4-6]. High concentration of salt causes hyperosmotic stress in plants, reducing the ability of plants to utilise water and changes the plant’s metabolic processes [7].

Tomato (Solanum lycopersicum L.) is moderately sensitive to salinity at all stages of plant development including seed germination, plant growth and fruit quality and yield [8, 9]. Due to the fact that saline irrigation or natural soil salinity decreases tomato crop productivity, there is a continuous demand for new hybrids with high salinity tolerance. Previously, we have identified some tomato varieties from rural areas of Romania with very good salt tolerance even up to 300 mM NaCl [10, 11]. It has been shown that wild species within Lycopersicon represent a potential source of useful genes for agricultural breeding (see for review [8]). To cope with oxidative and saline stress, tomato accumulates a variety of different antioxidants, such as tocopherols and proline [12, 13]. In addition to these non-volatile metabolites a vast array of volatile compounds are also emitted from plants under different stresses including drought [14], flooding [15], cold and heat [16], and ozone [17]. These volatile organic compounds have been implicated in plant-plant and plant-insect communications (see for review [18]). Soil salinity has been shown to influence not only the fruit quality [19, 2] but also the biochemistry and physiological properties (such as respiration and assimilation rates or stomata conductance) [20]. The volatile compounds emitted from tomatoes have not been studies thoroughly. The green leaf volatile emission has been reported for tomato plants inoculated with necrotrophic fungus Botrytis cinerea [21], after feeding by cotton leaf worms, Spodoptera littoralis [22] and as a result of cold and heat stress [16]. The aim of this paper is to evaluate different tomato varieties (including wild species) for their tolerance to soil salinity and to find if some volatile organic compounds can be used for rapid screening of tomato varieties for salinity stress resistance.

2 Materials and methods

2.1 Plant material and stress application

Varieties of Solanum lycopersicum L. (Solanaceae family, genus Solanum), cultivated in Western Romania, were used in the present study: Cherestur, Cheglevici, Dolat, Rudna, Giera, and the commercially available F₁ hybrid ACE 55. These varieties were obtain from tomato germplast collection held at the Plant Physiology Laboratory, Banat University of Agricultural Sciences and Veterinary Medicine “King Michael 1^st of Romania”, Timisoara. The seeds were sown in 5 L pots filled with commercial soil and sand (2:1 w/w). Three pots from each variety were chosen as controls and four for stress application. Every pot contained five tomato plants. They were watered daily for one week with 1.0 L of saline solution of different concentrations: 100 mM, 200 mM, 300 mM, and 400 mM. The control plants were watered daily with 1.0 L of tap water.

2.2 Gas exchange measurements and volatile organic compounds sampling

In order to perform the leaf gas exchange measurements and the volatile organic compound (VOC) sampling, we used a portable gas exchange system (GFS-3000, Heinz Walz GmbH, Effeltrich, Germany). The system has an environmental-controlled cuvette with 8 cm² window area and is equipped with full window leaf chamber for sample illumination measurements. All measurements were made at the ambient CO₂ concentration of 385 mmol mol⁻¹, light intensity of 1000 mmol m⁻² s⁻¹, leaf temperature of 25°C, and relative humidity > 65%. After enclosure of the leaf in the cuvette, light was switched on and the leaf was stabilized until stomata opened and steady state values for the assimilation rate (A) and stomatal conductance (gs) were determined. After gas exchange measurements, 3.0 L of the air exiting from the cuvette was sampled in a multibed stainless steel cartridge (10.5 cm length, 3 cm inner diameter, Supelco, Bellefonte, USA) filled with the following adsorbents (Supelco, Bellefonte, USA): Carbotrap C 20/40 mesh (0.1 g), Carbopack C 40/60 mesh (0.1 g), and Carbotrap X 20/40 mesh (0.1 g), that were optimized for green leaf volatiles (volatile C6 aldehydes and alcohols), and mono- and sesquiterpenes. The adsorption was done at a flow rate of 200 mL min⁻¹ for 15 min using a 1003-SKC constant flow sampling pump (SKC Inc., Houston, TX, USA). Samples were also taken from an empty leaf cuvette before and after each measurement. The cartridges filled with adsorbent were cleaned before VOC sampling by the passage of a stream of ultra pure helium at temperature of 250°C for 2 h.

The samples were analyzed for green leaf volatiles and terpene emissions by using a combined Shimadzu TD20 automated cartridge desorber and Shimadzu 2010 plus GC-MS instrument (Shimadzu Corporation, Kyoto, Japan). The chromatographic method used is detailed in [23]. The background (blank) VOC concentrations have been subtracted from emission samples of untreated plants. Compounds were identified using the NIST and Wiley libraries and the absolute concentrations of green leaf volatiles and terpenes were calculated based on an external authentic standard.

2.3 Data analyses

Means among the treatments were compared by one-way ANOVA follow by Tukey’s post hoc test. Statistical test results were considered significant at P < 0.05.

Ethical approval: The conducted research is not related to either human or animals use.

3 Results

3.1 Effect of soil salinity on photosynthetic characteristics

The effects of soil salinity on the assimilation rate and stomatal conductance to water vapor varied depending on the tomato variety. The assimilation rate for the control plants (plants which had been watered only with water) varied from 23.1 ± 0.9 μmol m⁻²s⁻¹ in Cheglevici to 19.01 ± 4.5 in Rudna (Figure 1a). In ACE 55 (commercial hybrid) and two landraces (Giera and Cheglevici) the assimilation rate decreased drastically after watering with the lowest salt concentration (100 mM NaCl). However, in the wild type Rudna the assimilation rate remained elevated (10.1 ± 1.7 μmol m⁻² s⁻¹) even after watering with 200 mM NaCl (no significant difference between treatments P = 0.202). This variety also exhibited the highest assimilation rates relative to the control and compared to the commercial hybrid. The value decreased significantly at 7.01 ± 1.7 μιmol m⁻² s⁻¹ only for plants treated with 300 mM NaCl (Figure 1a). In contrast, two varieties, Giera and Cheglevici, were affected by salinity in the same way as the commercial hybrid ACE 55. Generally, the local varieties have higher stomatal conductance than the commercial hybrid: 678 ± 34 μmol m⁻² s⁻¹ for Cheglevici compared with 359 ± 34 mmol m⁻² s⁻¹ for ACE 55 (Figure 2a). Rudna and Cherestur had the highest stomata conductance to water vapor relative to the control after treatment with 100 and 200 mM NaCl, respectively (Figure 2b). The other two varieties exhibited the same stomata water vapor conductance as that of the commercial hybrid (ACE 55). In the treatment with 400 mM NaCl, A and gs decreased significantly for all studied tomato varieties (P < 0.05). After this treatment, both parameters were reduced to 20% relative to the control.

Fig. 1

Changes in assimilation rate (a) and assimilation rate relative to control (b) in different varieties of Solanum lycopersicum L. in response to soil salinity. The data are expressed per unit projected leaf area. Means were compared by Tukey’s multiple comparison post-hoc test (n = 4) and different letters indicate means that are statistically different at P < 0.05.

Fig. 2

Changes in stomatal conductance to water vapor (a) and stomatal conductance relative to control (b) in different varieties of Solanum lycopersicum L. in response to soil salinity. The data are expressed per unit projected leaf area. Each data point is the mean (±SE) of 4 independent replicate experiments, means were compared by Tukey’s multiple comparison post-hoc test (n = 4) and different letters indicate means that are statistically different at P < 0.05.

3.2 Emissions of volatiles from tomato under salinity stress

The green leaf volatiles detected as a result of the soil salinity stress was (Z)-3-hexenol (Figure 3). The emission from control plants had been very low at a level of 30 pmol m⁻² s⁻¹ that is close to the detection limit of the apparatus. Even at 100 mM soil salinity, all tomato varieties emitted (Z)-3-hexenol at a value between 0.17 ± 0.01 nmol m⁻²s⁻¹ for Cherestur and 0.38 ± 0.06 nmol m⁻² s⁻¹ for Cheglevici. The maximum value of (Z)-3-hexenol was 2.22 ± 0.29 nmol m⁻²s⁻¹ observed for Giera.

Fig. 3

Emissions of the green leaf volatiles from S. lycopersicum plants in response to soil salinity. Each data point is the mean (±SE) of 3 independent replicate experiments. Means were compared by Tukey’s multiple comparison post-hoc test (n = 3) and different letters indicate means that are statistically different at P < 0.05.

Tomato is a constitutive monoterpene emitter under physiological conditions, but the total emissions varied at a quite low level for control plants, between 0.03 and 0.20 nmol m⁻² s⁻¹. alpha-pinene, camphene, 2-carene, alpha-phellandrene, limonene, beta-phellandrene, (E)-beta-ocimene and terpinolene have been detected in the emission from all tomato varieties (Figure 4a-f). 2-carene and beta-phellandrene are the major compounds in the emission (Figure 4). The emission of monoterpenes from plants under osmotic stress increased even in low stress ones. Anyway, the fingerprint for all volatile organic compounds was the same at all stresses levels. The emission of alpha-pinene, alpha-phellandrene, limonene are not related with the strength of the stress. For example, the emission of alpha-pinene for Cheglevici variety increased from 0.10 ± 0.02 nmol m⁻² s⁻¹ in control plants to 0.19 ± 0.02 nmol m⁻² s⁻¹ for plants treated with 400 nM NaCl. In contrast, the (E)-beta-ocimene and beta-phellandrene emissions were proportional with the stress strength (Figure 5a and b).

Fig. 4

Emissions of monoterpenes from S. lycopersicum plants in response to soil salinity. Each data point is the mean (±SE) of 3 independent replicate experiments. Means were compared by Tukey’s multiple comparison post-hoc test (n = 3) and different letters indicate means that are statistically different at P < 0.05.

Fig. 5

Correlation of the emissions of induced monoterpenes (E)-beta-ocimene (a), beta-phellandrene (b), 2-carene (c) and 3-hexenol (d) with soil salinity.

4 Discussions

4.1 Effect of soil salinity on leaf photosynthesis

Salinity is one of the major stress factors of the plants which affects the yield and crop productivity drastically. This could be explained by the fact that that assimilation rate is lower in plants under osmotic stress, the carbon fixation is decreasing, therefore the investment of the plants in fruits is lower [24]. Indeed, in our experiment, the assimilation rates and stomatal conductance to water vapor decreased drastically even at 200 mM NaCl treatments. We identified two varieties, Rudna and Cherestur, which have very high assimilation rates and stomatal conductance to water vapor compared with the commercial hybrid. Overall, at 200 mM only one variety (Rudna) exhibited higher parameters compared with all other studied varieties. Probably this variety of tomato contains some resistance genes to salinity. Resistance to salinity stress is controlled by few genes [25] or by the complex interaction of several genes [26]. The gene overexpression confers lower cellular damage, improvement of root and shoot growth and maintenance of photosynthetic capacity [27]. At higher concentrations of sodium chloride in the soil, both parameters (assimilation rate and stomatal conductance to water vapor) decreased drastically for all varieties, suggesting that under high salinity the osmotic effect become important in CO₂ assimilation. Some papers pointed out that carbonic anhidrases and aquaporins are involved in regulation of stomatal conductance [28]. It was shown that Na⁺ at a concentration above 100 mM severely inhibits plants enzymes [29]. For Rudna variety we found that this threshold is increased to 200 mM. Indeed, in our previous studies based on genetic analysis we found out that this variety is the most tolerant to salinity [10].

4.2 The influence of soil salinity on volatile organic compounds emitted from tomato plants

Green leaf volatiles (C5 and C6 alcohols and ketones) originate from free fatty acids released by phospholipases from membranes in response to different abiotic and biotic stresses [30]. In our studies we found only (Z)-3-hexenol which is emitted from tomato under osmotic stress compared with the previous articles which reported four or even nine different C5 and C6 green leaf volatiles, respectively [21, 16]. The emission became significant even at 100 mM NaCl in soil but was very low for control plants. This observation rules out the mechanical damage of the leaves during experiments (see [31] for more details regarding to mechanical wounding).

Terpenes are stored in glandular trichomes of Solanum lycopersicum leaves and are released even in physiological conditions at a level of 0.5 nmol m⁻² s⁻¹ which is in accordance with data obtained by Schimiller et al. [32, 33]. The emissions consisted of α-pinene, camphene, 2-carene, α-phellandrene, limonene, β-phellandrene, (E)-β-ocimene and terpinolene as have been previously reported by Jensen et al. [21] and Copolovici et al. [16]. The composition was the same for stressed and control plants and could be due to cellular damage or enhanced permeability of barriers of terpene-containing structures. The same emissions have been described for B. cinerea infection of tomato which has been associated with inoculation damage [21] as well as for cold and heat stress [16]. It has been shown that the terpene emissions from storage pools scale exponentially with temperature due to the permeability changes of the glandular trichomes [16, 34]. In case of osmotic stress, the trichomes developed irregularly in Nicotiana tabacum L. [35] and even showed an overall density increase in Madia sativa [36, 37]. This observation can explain,, the increase of the emission of different terpenes with soil salinity in this study and we can speculate that increasing emission of terpenes can play an important role in stress tolerance. The emission of (E)-ß-ocimene, which is typically induced by abiotic stress, is increased proportionally with the soil salinity. (E)-beta-ocimene is synthesized in the plastid via the 2-C-methyl-d-erythritol-4-P pathway [38] and its emission could be due to changes in metabolite channeling. In the same way, the 2-carene and beta-phellandrene emissions increased with the concentration of soil salinity (Figure 5).

5 Conclusions

The photosynthetic parameters (assimilation rate and stomata water vapor conductance) decreased drastically for all plants watered with saline solution. One of the varieties (Rudna) showed better adaptation for growing in saline soil (high assimilation rates even at 200 mM NaCl) than the commercial hybrid. This study demonstrated that volatile organic compounds can be used as a very sensitive stress signal. One of the green leaf volatile (3-hexenol) emissions increased exponential with soil salinity and terpenes ((E)-beta-ocimene, beta-phellandrene and 2-carene) scale up with saline stress and can be used as markers of the stress.

Acknowledgements

This work was supported by a grant of the Romanian National Authority for Scientific Research, CNSI-UEFISCDI, project number PN-II-PT-PCCA-2011-3.1-0965 and by and the European Commission and the Romanian Government (project POSCCE 621/2014). The authors would also like to thank the Centre for Consultancy and Euro-regional Rural Cooperation for financial support.

Conflicts of interest: Authors state no conflict of interest

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Received: 2016-7-20

Accepted: 2017-2-20

Published Online: 2017-5-4

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