Abstract
Closed soilless cultivation systems (SCS) support high productivity and optimized year-round production of standardized quality. Efficiency and precision in modulating nutrient solution composition, in addition to controlling temperature, light, and atmospheric composition, renders protected SCS instrumental for augmenting organoleptic and bioactive components of quality. Effective application of eustress (positive stress), such as moderate salinity or nutritional stress, can elicit tailored plant responses involving the activation of physiological and molecular mechanisms and the strategic accumulation of bioactive compounds necessary for adaptation to suboptimal environments. For instance, it has been demonstrated that the application of salinity eustress increases non-structural carbohydrates and health-promoting phytochemicals such as lycopene, β-carotene, vitamin C, and the overall phenolic content of tomato fruits. Salinity eustress can also reduce the concentration of anti-nutrient compounds such as nitrate due to antagonism between nitrate and chloride for the same anion channel. Furthermore, SCS can be instrumental for the biofortification of vegetables with micronutrients essential or beneficial to human health, such as iodine, iron, selenium, silicon, and zinc. Accurate control of microelement concentrations and constant exposure of roots to the fortified nutrient solution without soil interaction can maximize their uptake, translocation, and accumulation in the edible plant parts; however, biofortification remains highly dependent on microelement forms and concentrations present in the nutrient solution, the time of application and the accumulation capacity of the selected species. The present article provides an updated overview and future perspective on scientific advances in SCS aimed at enhancing the sensory and bioactive value of vegetables.
Soilless Means for Improving Sensory and Functional Quality of Vegetables
The productivity of agricultural production systems is unprecedentedly challenged by projections for global population increase, by climate change and by shortage of the fundamental natural resources of water and arable land. In the case of vegetable crops, which contribute significant nutritive and bioactive value to the human diet, maximal productivity is attained under controlled environments where production may expand vertically and temperature, light, nutrient supply, and atmospheric composition are controlled (Gruda, 2005, 2009). In particular, the technological advancement of closed soilless (hydroponic) cultivation systems (SCS; e.g., nutrient film, floating, and pot- and sacs-systems) based on recirculating nutrient solutions has maximized productivity per unit area and notably in terms of water use efficiency, by maximizing root contact with the nutrient source while minimizing evaporation and nutrient runoff (Treftz and Omaye, 2016). Despite the high capital investment and technological proficiency required for managing soilless systems, their expansion is propelled by the efficacy of optimized year-round production and standardized product quality irrespective of locality.
Besides the pressing issue of global food security, demand for high quality horticultural products is also on the rise, driven by the growing interest of society in fresh products of high organoleptic, nutritional, and functional quality. The quality of fresh horticultural commodities has been recently defined as “a dynamic composite of their physicochemical properties and evolving consumer perception, which embraces organoleptic, nutritional and bioactive components” (Kyriacou and Rouphael, 2018). Extrinsic characteristics of product quality are strongly influenced by socioeconomic and marketing factors which formulate consumer perception and generate quality prototypes. Despite the continued growth of the hydroponic industry consumers at large hold a negative bias toward SCS products which they consider artificial, less tasty, and of lower nutritional quality (Schnitzler and Gruda, 2002), just as organically grown fruits and vegetables are generally hailed as healthier and safer (Orsini et al., 2016). Nevertheless, it is apparent that key secondary metabolites which form the basis of functional quality in horticultural products can be modulated by appropriate management of SCS components. Exposure to biotic and abiotic stress underlies the superior nutritional quality often observed in organically grown products, since stress response entails the activation of physiological and molecular mechanisms necessary for adaptation to suboptimal environments, such as the biosynthesis of secondary metabolites (e.g., ascorbate, tocopherols, carotenoids, and glucosinolates; Orsini et al., 2016). Soilless systems can facilitate the precise application of an eustress (positive stress), such as moderate salinity or nutritional stress, through precise management of the concentration and composition (cationic and anionic proportions or single ions) of the nutrient solution, and thus may constitute a practical and effective means for improving the nutritional value of vegetables and for reducing the accumulation of anti-nutrient compounds, such as nitrates (Colla et al., 2018; Rouphael and Kyriacou, 2018; Rouphael et al., 2018a,b). Soilless culture can also be instrumental in the biofortification of edible plant portions with essential and/or beneficial micronutrients to human health. Biofortification with essential or beneficial micronutrients may constitute an effective means for supplying the human diet with iodine (I), selenium (Se), zinc (Zn), and silicon (Si) (White and Broadley, 2005). The present article provides an updated overview and future perspective on scientific advances in soilless cultivation aimed at enhancing the sensory and bioactive quality of vegetables through nutrient solution management and applications aimed at biofortification.
Salinity Eustress and Macronutrient Management for Enhancing Nutritional Quality of Hydroponically Grown Vegetables
Excessive concentration of sodium chloride (NaCl) in irrigation water and agricultural soils disturbs physiological processes in vegetable crops, leading to stunted growth and yield decline (Rouphael et al., 2017, 2018b). However, recent scientific reviews have indicated that vegetable crops may exhibit tailored responses to the application of eustress, such as mild to moderate salinity, as a result of stress-induced reshuffling of plant metabolism and strategic accumulation of bioactive compounds against suboptimal conditions (Kyriacou and Rouphael, 2018). Vegetable crops can synthesize a broad range of secondary metabolites to counteract oxidative damage and to scavenge reactive oxygen species (ROS) elicited by environmental stressors (Orsini et al., 2016). These health-promoting phytochemicals, abundant in stressed plants, can enrich the functional quality of fresh vegetables to the benefit of human diet (Khanam et al., 2012; Kyriacou and Rouphael, 2018).
Multiple studies have reported increase in the bioactive content of vegetables triggered by mild to moderate NaCl concentrations in the nutrient solution (Tzortzakis, 2009, 2010; Rouphael et al., 2018a,b). Although under soil conditions this technique for improving product quality poses a high risk of plant overstress (Hidaka et al., 2008), soilless culture may be an effective tool for modulating secondary metabolites without curbing growth and yield, through proper management of the nutrient solution’s composition (Schwarz et al., 2009; Tomasi et al., 2015). Several studies have demonstrated that NaCl in the nutrient solution raises the levels of sugars, organic acids, and amino acids in several vegetable crops, like tomato (Zushi and Matsuzoe, 2015; Moya et al., 2017), pepper (Marin et al., 2009), melon (Rouphael et al., 2012b), watermelon (Colla et al., 2006), eggplant (Savvas and Lenz, 1996), lettuce (Sakamoto et al., 2014), and cauliflower (Giuffrida et al., 2017) thereby improving their organoleptic quality. The salt-induced osmoregulatory mechanism in hydroponically grown vegetables involves the biosynthesis of specific osmolytes (sugars, minerals, and amino acids such as proline and GABA) believed to function as osmoprotectants by counterbalancing the increase in vacuolar osmotic potential caused by the toxic accumulation of sodium and chloride ions (Hasegawa et al., 2000).
The application of salinity eustress may also affect health-promoting phytochemicals. For instance, increasing soilless nutrient solution electrical conductivity (EC) from 3 to 6.5 dS m-1 (Krauss et al., 2006), from 2.4 to 4.5 dS m-1 (Wu et al., 2004), and from 2.2 to 4.5 dS m-1(Moya et al., 2017) increased the lycopene, β-carotene, vitamin C, and total phenolic content of tomato. Giuffrida et al. (2017), showed that the functional quality of hydroponically grown cauliflower in response to moderate salt stress may depend on interactive variables, such as duration of exposure and plant phenological stage at the time of exposure (e.g., salinity stress applied constantly throughout the cultivation cycle or at the onset of flowering), with neoglucobrassicin concentration found two-fold higher in cauliflower heads supplied with saline nutrient solution (4 dS m-1) compared to the non-saline (EC 2 dS m-1) control treatment. Beneficial effects of mild to moderate salinity on nutritional and bioactive value was also reported for hydroponically grown leafy greens (Kim et al., 2008; Colla et al., 2013; Klados and Tzortzakis, 2014; Bonasia et al., 2017; Ntatsi et al., 2017; Petropoulos et al., 2017). For instance, Petropoulos and co-workers reported that increasing the EC from 1.8 to 6.0 dS m-1 increased ascorbic acid as well as α-tocopherol levels in spiny chicory. Similarly, Colla et al. (2013) and Bonasia et al. (2017) showed that raising the EC from 2.5 to 3.5 dS m-1 increased antioxidant compounds in wild rocket, and from 2.0 to 5.8 dS m-1 it improved the antioxidant activity, chlorogenic acid, cynarin, and luteolin levels in leaves of artichoke and cardoon grown in a floating system. However, response to NaCl is cultivar-dependent and the choice of the cultivar is critical for achieving the desired effects (Borghesi et al., 2011; Dominguez-Perles et al., 2011; Colla et al., 2013). Several workers have reported negative effects or no significant effects in response to NaCl application. Increasing the nutrient solution EC above 4.4 dS m-1 decreased lycopene and β-carotene content in tomato (De Pascale et al., 2001). Similarly, Petersen et al. (1998) and Bonasia et al. (2017) observed a decrease of ascorbic acid in tomato and wild rocket at EC 9.0 and 4.5 dS m-1, respectively. Presumably the antioxidant system of salt-stressed plants does not effectively support ROS scavenging after the stress threshold for maintaining growth is exceeded (Rouphael et al., 2018a,b), whereas leaf area reduction in salt-sensitive cultivars can also modify fruit temperature and halt the synthesis of bioactive compounds (Dorais et al., 2008). Finally, salinity eustress can reduce nitrate accumulation in SCS leafy vegetables due to antagonism between nitrate and chloride for the same anion channel (Rubinigg et al., 2003). Vegetable nitrate remains of high interest to regulators due to possible effects on human health, while it also imparts vegetables a bitter taste (Colla et al., 2018). Borgognone et al. (2016) reported that minimizing nitrate supply in floating raft culture by partial substitution of calcium nitrate with calcium chloride increased phenols and flavonoids and lowered nitrates in cardoon leaves without affecting yield.
Although most published articles concerning the positive effects of nutrient solution EC on nutritional, organoleptic, and functional quality of soilless vegetables were based on greenhouse experiments in which NaCl was the predominant salt, several studies have shed light on the effects of salinity induced by macronutrients. For instance, Fallovo et al. (2009) determined the effects of macronutrient solution concentration (2, 18, 34, 50, or 66 mequiv L-1, corresponding to an EC of 0.3, 1.2, 2.0, 2.8, and 3.6 dS m-1, respectively) during the spring and summer seasons on leafy lettuce (Lactuca sativa L. var. acephala) grown in a floating system. The authors reported a linear decrease in qualitative characteristics (glucose, fructose, proteins, total carbohydrates, and starch contents) in response to an increase in the nutrient solution concentration from 2 to 66 mequiv L-1. Similarly, Rouphael et al. (2012a) showed that raising the macronutrient solution concentration from 4 to 68 mequiv L-1 in floating raft culture increased biomass production but deteriorated leaf functional quality in both cardoon and artichoke by decreasing key polyphenols such as caffeic acid, chlorogenic acid, cynarin, and luteolin. Moreover, the management of the cationic proportions (K/Ca/Mg) in the nutrient solution facilitated by soilless culture has been also demonstrated as an effective tool for enhancing nutritional quality of fruit vegetables (Fanasca et al., 2006a). A high proportion of K in the nutrient solution caused a significant increase in tomato soluble solids and lycopene contents irrespective of cultivar (‘Corfu’ or ‘Lunarossa’ – standard or high-pigment cultivar), whereas high concentration of Mg improved the hydrophilic antioxidants (caffeic acid) and the total antioxidant capacity of the high-pigment ‘Lunarossa’ hybrid (Fanasca et al., 2006b). Synthesis and accumulation of the abovementioned antioxidant compounds in response to high Mg supply might relate to the increased activity of key enzymes such as glutamine synthetase that regulate ammonia assimilation and detoxification of plant tissues (Marschner, 2012).
Soilless Biofortification of Vegetables with Essential and Beneficial Micronutrients
Biofortification of vegetables with essential and non-essential beneficial micronutrients caters to the demand for healthier diet and the need to address human micronutrient deficiency, known as “hidden hunger” (White and Broadley, 2005; Carvalho and Vasconcelos, 2013). However, the window between biofortification and toxicity effect is often quite narrow. Applications aiming at the accumulation of health-supporting micronutrients must be adjusted to avoid detrimental effects on plant growth (Rouphael et al., 2018a). Moreover, biofortification may depend upon several interacting factors, such as genotype, chemical form, application rate, and environmental and growing conditions (Tomasi et al., 2015).
Selenium and iodine have been particularly investigated since they are beneficial though non-essential microelements for human health. Uptake is higher when supplied in SCS nutrient solution where Se and I concentrations can be accurately controlled, as opposed to side-dressing of soil crops or foliar applications (Wiesner-Reinhold et al., 2017). Constant exposure of the root system to fortified nutrient solution and absence of micronutrient–soil interaction make SCS more efficient, thus maximizing uptake, translocation, and accumulation of these elements in the edible parts (Wiesner-Reinhold et al., 2017). However, micronutrient accumulation is highly dependent on the elemental concentration in the soilless solution, the time of application and the accumulation capacity of the selected species. For instance, Signore et al. (2018) reported that iodine biofortification of carrots at 50 mg L-1 through the hydroponic solution reached cumulative levels toxic on the plants compared to foliar applications both under open-field and greenhouse conditions at the same rate. On the other hand, low rates (0.5–1.5 mg L-1) of selenium in the nutrient solution increased Se concentration in several horticultural commodities such as spinach, lettuce, and basil without inducing toxic effects (Zhu et al., 2004; Malorgio et al., 2009; Ramos et al., 2011; Ferrarese et al., 2012; Puccinelli et al., 2017). Zhu et al. (2003), reported that biofortification with I in solution culture is easily feasible both with iodide (I-) and iodate (), as the application of I at rates from 0.13 to 12.7 mg L-1 effectively fortified spinach with iodine. Similarly, Blasco et al. (2008) showed that the most appropriate rate of I- in lettuce soilless culture is 5.1 mg L-1 or lower, whereas concentration of 1.3 to 30.5 mg L-1 achieved foliar accumulation of I without detriment to yield. Kiferle et al. (2013); Li et al. (2017), and Smoleń et al. (2018) indicated that also fruit vegetables and tuber crop such as tomato, pepper, and potato grown in soilless culture can be targeted for I and/or Se biofortification. Another important factor influencing Se and I accumulation in vegetables is their chemical forms. Vegetable species exposed to selenate (O4Se-2) rather than selenite (O3Se-2) and to I- rather to can accumulate more Se and I in leaf or fruit tissues. This is because selenate is taken up actively by the more efficient sulfate transporter compared to the passive phosphate transporter used for taking up selenite (Wiesner-Reinhold et al., 2017). Uptake of I- was much higher than since the latter form should be reduced to I- before uptake, thus reducing bioavailability to vegetable crops (Blasco et al., 2008).
According to White and Broadley (2005), concentrations of 0.1–0.7 mg Zn g-1 dry weight can be achieved in leafy vegetables with no detriment to yield, making Zn biofortification of leafy greens a potential tool for enhancing dietary Zn intake (White et al., 2018). Adequate Zn addition in the nutrient solution (5.2–6.5 mg L-1) allowed biofortification of Brassica oleracea coupled with significant synthesis and accumulation of amino acids (Arg, Asp, Glu, Gln, Hys, Lys, Phe, and Trp) while maintaining optimal growth (Barrameda-Medina et al., 2017). In addition, the production of Fe-enriched leafy vegetables such as lettuce using hydroponics is feasible, since the increase of Fe concentration in the nutrient solution 6 h before harvest resulted in significant increase of foliar Fe content without affecting yield (Inoue et al., 2000). Moreover, effective Si biofortification of soilless crops of basil, chicory, mizuna, purslane, Swiss chard, and tatsoi was demonstrated with SiO2 supplementation of the nutrient solution at 50–100 mg L-1 with no detrimental effect on crop productivity (D’Imperio et al., 2016).
Conclusion and the Challenges Ahead
The demand for global food security under increasing biotic and abiotic pressures exacerbated by climate change makes protected cultivation of vegetable crops an inevitable necessity. Technological progress in the management of SCS drives productivity and mitigates high initial infrastructural costs. Moreover, flexibility and precision in modulating nutrient solution composition, in addition to controlling temperature, light, and atmospheric composition, renders SCS systems instrumental in targeting organoleptic and bioactive components of quality thus addressing demand for improved vegetable quality. The effective application of eustress, such as mild to moderate salinity or nutritional stress, can elicit targeted plant responses through the activation of physiological and molecular mechanisms and the strategic accumulation of bioactive compounds necessary for adaptation to suboptimal environments. Salinity eustress has been demonstrated to augment organoleptic components of quality such as soluble carbohydrates, and health-promoting phytochemicals such as lycopene, β-carotene, vitamin C, and polyphenols in vegetables; moreover, it may curb anti-nutrients such as nitrate owing to nitrate-chloride antagonism for uptake. Understanding the molecular and physiological mechanisms elicited by controlled plant eustress and those facilitating micronutrient uptake in interaction with genotype and environmental conditions will usher horticultural science into the era of tailoring superior sensory and functional quality vegetables.
Furthermore, SCS can facilitate the effective biofortification of vegetables with micronutrients essential or beneficial to human health, such as iodine, iron, selenium, silicon, and zinc. Accurate control of microelement concentrations and constant exposure of roots to the fortified nutrient solution without soil interaction can maximize their uptake, translocation, and accumulation in the edible plant parts. Biofortification remains, however, highly dependent on microelement forms and concentrations present in the nutrient solution, the duration of targeted applications, the developmental stage of plants, and the accumulation capacity of the selected species. These potentially interacting factors pose future challenges for research before SCS biofortification applications become effective tools for addressing nutrient deficiencies in human diet.
Statements
Author contributions
YR and MK had the original idea of eustress and biofortification of soilless vegetables and were both involved in writing the article.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
Barrameda-MedinaY.BlascoB.LentiniM.EspositoS.BenasN.MorenoD. A.et al (2017). Zinc biofortification improves phytochemicals and amino-acidic profile in Brassica oleracea cv. Bronco.Plant Sci.25845–51. 10.1016/j.plantsci.2017.02.004
2
BlascoB.RiosJ. J.CervillaL. M.Sanchez-RodriguezE.RuizJ. M.RomeroL. (2008). Iodine biofortification and antioxidant capacity of lettuce: potential benefits for cultivation and human health.Ann. Appl. Biol.152289–299. 10.1111/j.1744-7348.2008.00217.x
3
BonasiaA.LazzizeraC.EliaA.ConversaG. (2017). Nutritional, biophysical and physiological characteristics of wild rocket genotypes as affected by soilless cultivation system, salinity level of nutrient solution and growing period.Front. Plant Sci.8:300. 10.3389/fpls.2017.00300
4
BorghesiE.Gonzalez-MiretM. L.Escudero-GileteM. L.MalorgioF.HerediaF. J.Meléndez-MartínezA. J. (2011). Effects of salinity on carotenoids, anthocyanins, and color of diverse tomato genotypes.J. Agric. Food Chem.5911676–11682. 10.1021/jf2021623
5
BorgognoneD.RouphaelY.CardarelliM.LuciniL.CollaG. (2016). Changes in biomass, mineral composition, and quality of cardoon in response to NO3-:Cl- ratio and nitrate deprivation from the nutrient solution.Front. Plant Sci.7:978. 10.3389/fpls.2016.00978
6
CarvalhoS.VasconcelosM. (2013). Producing more with less: ‘omics’ at the service of plant-based food biofortification.Food Res. Intern.54961–971. 10.1016/j.foodres.2012.12.021
7
CollaG.KimH. J.KyriacouM. C.RouphaelY. (2018). Nitrate in fruits and vegetables.Sci. Hortic.237221–238. 10.1016/j.scienta.2018.04.016
8
CollaG.RouphaelY.CardarelliM.ReaE. (2006). Effect of salinity on yield, fruit quality, leaf gas exchange, and mineral composition of grafted watermelon plants.HortScience41622–627.
9
CollaG.RouphaelY.CardarelliM.SvecovaE.ReaE.LuciniL. (2013). Effects of saline stress on mineral composition, phenolics acids and flavonoids in leaves of artichoke and cardoon genotypes grown in floating system.J. Sci. Food Agric.931119–1127. 10.1002/jsfa.5861
10
De PascaleS.MaggioA.FoglianoV.AmbrosinoP.RitieniA. (2001). Irrigation with saline water improves carotenoids content and antioxidant activity of tomato.J. Hort. Sci. Biotechnol.76447–453. 10.1080/14620316.2001.11511392
11
D’ImperioM.RennaM.CardinaliA.ButtaroD.SantamariaP.SerioF. (2016). Silicon biofortification of leafy vegetables and its bioaccessibility in the edible parts.J. Sci. Food Agric.96751–756. 10.1002/jsfa.7142
12
Dominguez-PerlesR.Martinez-BallestaM. C.RiquelmeF.CarvajalM.Garcia-VigueraC.MorenoD. A. (2011). Novel varieties of broccoli for optimal bioactive components under saline stress.J. Sci. Food Agric.911638–1647. 10.1002/jsfa.4360
13
DoraisM.EhretD. L.PapadopoulosA. P. (2008). Tomato (Solanum lycopersicum) health components: from the seed to the consumer.Phytochem. Rev.7231–250. 10.1007/s11101-007-9085-x
14
FallovoC.RouphaelY.ReaE.BattistelliA.CollaG. (2009). Nutrient solution concentration and growing season affect yield and quality of Lactuca sativa L. var. acephala in floating raft culture.J. Sci. Food Agric.891682–1689. 10.1002/jsfa.3641
15
FanascaS.CollaG.MaianiG.VenneriaE.RouphaelY.AzziniE.et al (2006a). Changes in antioxidant content of tomato fruits in response to cultivar and nutrient solution composition.J. Agric. Food Chem.544319–4325. 10.1021/jf0602572
16
FanascaS.CollaG.RouphaelY.SaccardoF.MaianiG.VenneriaE.et al (2006b). Evolution of nutritional value of two tomato genotypes grown in soilless culture as affected by macrocation proportions.HortScience411584–1588.
17
FerrareseM.MahmoodiS.QuattriniE.SchiaviM.FerranteA. (2012). Biofortification of spinach plants applying selenium in the nutrient solution of floating system.Veg. Crops Res. Bull.76127–136. 10.2478/v10032-012-0009-y
18
GiuffridaF.CassanitiC.MalvuccioA.LeonardiC. (2017). Effects of salt stress imposed during two growth phases on cauliflower production and quality.J. Sci. Food Agric.971552–1560. 10.1002/jsfa.7900
19
GrudaN. (2005). Impact of environmental factors on product quality of greenhouse vegetables for fresh consumption impact of environmental factors on product quality.Crit. Rev. Plant Sci.24227–247. 10.1080/07352680591008628
20
GrudaN. (2009). Do soilless culture systems have an influence on product quality of vegetables?J. Appl. Bot. Food Qual.147141–147.
21
HasegawaP. M.BressanR. A.ZhuJ. K.BohnertH. J. (2000). Plant cellular and molecular responses to high salinity.Annu. Rev. Plant Physiol. Mol. Biol.51463–499. 10.1146/annurev.arplant.51.1.463
22
HidakaK.YasutakeD.KitanoM.TakahashiT.SagoY.IshikawaK.et al (2008). Production of high quality vegetables by applying low temperature stress to roots.Acta Hortic.8011431–1436. 10.17660/actahortic.2008.801.176
23
InoueK.KondoS.AdachiA.YokotoH. (2000). Production of iron enriched vegetables: effect of feeding time on the rate of increase in foliar iron content and foliar injury.J. Hort. Sci. Biotechnol.75209–213. 10.1080/14620316.2000.11511225
24
KhanamU. K. S.ObaS.YanaseE.MurakamiY. (2012). Phenolic acids, flavonoids and total antioxidant capacity of selected leafy vegetables.J. Funct. Foods4979–987. 10.1016/j.jff.2012.07.006
25
KiferleC.GonzaliS.HolwerdaH. T.Real IbacetaR.PerataP. (2013). Tomato fruits: a good target for iodine biofortification.Front. Plant Sci.4:205. 10.3389/fpls.2013.00205
26
KimH. J.FonsecaJ. M.ChoiJ. H.KubotaC.DaeY. K. (2008). Salt in irrigation water affects the nutritional and visual properties of romaine lettuce (Lactuca sativa L.).J. Agric. Food Chem.563772–3776. 10.1021/jf0733719
27
KladosE.TzortzakisN. (2014). Effects of substrate and salinity in hydroponically grown Cichorium spinosum.J. Soil Sci. Plant Nutr.14211–222. 10.4067/s0718-95162014005000017
28
KraussS.SchnitzlerW. H.GrassmanJ.WoitkeM. (2006). The influence of different electrical conductivity values in a simplified recirculating soilless system on inner and outer fruit quality characteristics of tomato.J. Agric. Food Chem.54441–448. 10.1021/jf051930a
29
KyriacouM. C.RouphaelY. (2018). Towards a new definition of quality for fresh fruits and vegetables.Sci. Hortic.234463–469. 10.1016/j.scienta.2017.09.046
30
LiR.LiD. W.LiuH. P.HongC. L.SongM. Y.DaiZ. X.et al (2017). Enhancing iodine content and fruit quality of pepper (Capsicum annuum L.) through biofortification.Sci. Hort.214165–173. 10.1016/j.scienta.2016.11.030
31
MalorgioF.DiazK. E.FerranteA.Mensuali-SodiA.PezzarossaB. (2009). Effects of selenium on minimally processed leafy vegetables grown in a floating system.J. Sci. Food Agric.892243–2251. 10.1002/jsfa.3714
32
MarinA.RubioJ. S.MartinezV.GilM. I. (2009). Antioxidant compounds in green and red peppers as affected by irrigation frequency, salinity and nutrient solution composition.J. Sci. Food Agric.891352–1359. 10.1002/jsfa.3594
33
MarschnerP. (2012). Marschner’s Mineral Nutrition of Higher Plants.Cambridge, MA: Academic Press.
34
MoyaC.OyanedelE.VerdugoG.Fernanda FloresM.UrrestarazuM.AlvaroJ. E. (2017). Increased electrical conductivity in nutrient solution management enhances dietary and organoleptic qualities in soilless culture tomato.HortScience52868–872. 10.21273/hortsci12026-17
35
NtatsiG.AliferisK. A.RouphaelY.NapolitanoF.MakrisK.KalalaG.et al (2017). Salinity source alters mineral composition and metabolism of Cichorium spinosum.Environ. Exp. Bot.141113–123. 10.1016/j.envexpbot.2017.07.002
36
OrsiniF.MaggioA.RouphaelY.De PascaleS. (2016). ‘Physiological Quality’ of organically grown vegetables.Sci. Hortic.208131–139. 10.1016/j.scienta.2016.01.033
37
PetersenK. K.WillumsenJ.KaackK. (1998). Composition and taste of tomatoes as affected by increased salinity and different salinity sources.J. Hortic. Sci. Biotechnol.73205–215. 10.1080/14620316.1998.11510966
38
PetropoulosS. A.LevizouE.NtatsiG.FernandesA.PetrotosK.AkoumianakisK.et al (2017). Salinity effect on nutritional value, chemical composition and bioactive compounds content in Cichorium spinosum L.Food Chem.214129–136. 10.1016/j.foodchem.2016.07.080
39
PuccinelliM.MalorgioF.PezzarossaB. (2017). Selenium enrichment of horticultural crops.Molecules22:933. 10.3390/molecules22060933
40
RamosS. J.RutzkeM. A.HayesR. J.FaquinV.GuilhermeL. R. G.LiL. (2011). Selenium accumulation in lettuce germplasm.Planta233649–660. 10.1007/s00425-010-1323-6
41
RouphaelY.CardarelliM.BoniniP.CollaG. (2017). Synergistic action of a microbial-based biostimulant and a plant derived-protein hydrolysate enhances lettuce tolerance to alkalinity and salinity.Front. Plant Sci.8:131. 10.3389/fpls.2017.00131
42
RouphaelY.CardarelliM.LuciniL.ReaE.CollaG. (2012a). Nutrient solution concentration affects growth, mineral composition, phenolic acids, and flavonoids in leaves of artichoke and cardoon.HortScience471424–1429.
43
RouphaelY.CardarelliM.ReaE.CollaG. (2012b). Improving melon and cucumber photosynthetic activity, mineral composition, and growth performance under salinity stress by grafting onto Cucurbita hybrid rootstocks.Photosynthetica50180–188. 10.1007/s11099-012-0002-1
44
RouphaelY.KyriacouM. C. (2018). Quality and safety of fresh fruits and vegetables at harvest.Sci. Horti.23978–79. 10.1016/j.scienta.2018.05.006
45
RouphaelY.KyriacouM. C.PetropoulosS. A.De PascaleS.CollaG. (2018a). Improving vegetable quality in controlled environments.Sci. Hort.234275–289. 10.1016/j.scienta.2018.02.033
46
RouphaelY.PetropoulosS. A.CardarelliM.CollaG. (2018b). Salinity as eustressor for enhancing quality of vegetables.Sci. Hortic.234361–369. 10.1016/j.scienta.2018.02.048
47
RubiniggM.PosthumusF.FerschkeM.TheoJ.ElzengaM.StulenI. (2003). Effects of NaCl salinity on 15N-nitrate fluxes and specific root length in the halophyte Plantago maritima L.Plant Soil250201–213. 10.1023/A:1022849928781
48
SakamotoK.KogiM.YanagisawaT. (2014). Effects of salinity and nutrients in seawater on hydroponic culture of red leaf lettuce.Environ. Control Biol.52189–195. 10.2525/ecb.52.189
49
SavvasD.LenzF. (1996). Influence of NaCl concentration in the nutrient solution on mineral composition of eggplants grown in sand culture.Angew. Bot.70124–127.
50
SchnitzlerW. H.GrudaN. (2002). Quality issues of greenhouse production.Acta Hortic.614663–674. 10.17660/actahortic.2003.614.99
51
SchwarzD.FrankenP.KrumbeinA.KläringH. P.Bar-YosefB. (2009). Nutrient management in soilless culture in the conflict of plant, microorganism, consumer and environmental demands.Acta Hort.84327–34. 10.17660/actahortic.2009.843.1
52
SignoreA.RennaM.D’ImperioM.SerioF.SantamariaP. (2018). Preliminary evidences of biofortification with iodine of “Carota di Polignano”, an italian carrot landrace.Front. Plant Sci.9:170. 10.3389/fpls.2018.00170
53
SmoleńS.KowalskaI.SkoczylasL.Liszka-SkoczylasM.GrzankaM.HalkaM.et al (2018). The effect of salicylic acid on biofortification with iodine and selenium and the quality of potato cultivated in the NFT system.Sci. Hort.240530–543. 10.1016/j.scienta.2018.06.060
54
TomasiN.PintonR.Dalla CostaL.CortellaG.TerzanoR.MimmoT.et al (2015). New solutions for floating cultivation system of ready-to-eat salad: a review.Trends Food Sci. Technol.46267–276. 10.1016/j.tifs.2015.08.004
55
TreftzC.OmayeS. T. (2016). Hydroponics: potential for augmenting sustainable food production in non-arable regions.Nutr. Food Sci.46672–684. 10.1108/NFS-10-2015-0118
56
TzortzakisN. G. (2009). Influence of NaCl and calcium nitrate on lettuce and endive growth using nutrient film technique.Intern. J. Veg. Sci.1544–56. 10.1080/19315260802446419
57
TzortzakisN. G. (2010). Potassium and calcium enrichment alleviate salinity-induced stress in hydroponically grown endives.Hortic. Sci.37155–162. 10.17221/1/2010-hortsci
58
WhiteP. J.BroadleyM. R. (2005). Biofortifying crops with essential mineral elements.Trends Plant Sci.10586–593. 10.1016/j.tplants.2005.10.001
59
WhiteP. J.PongracP.SneddonC. C.ThompsonJ. A.WrightG. (2018). Limits to the biofortification of leafy brassicas with zinc.Agriculture8:3. 10.3390/agriculture8030032
60
Wiesner-ReinholdM.SchreinerM.BaldermannS.SchwarzD.HanschenF. S.KippA. P.et al (2017). Mechanisms of selenium enrichment and measurement in brassicaceous vegetables, and their application to human health.Front. Plant Sci.8:1365. 10.3389/fpls.2017.01365
61
WuM.BuckJ. S.KubotaC. (2004). Effects of nutrient solution EC, plant microclimate and cultivars on fruit quality and yield of hydroponic tomatoes (Lycopersicum esculentum L.).Acta Hort.659541–547. 10.17660/actahortic.2004.659.70
62
ZhuY. G.HuangY.HuY.LiuY.ChristieP. (2004). Interactions between selenium and iodine uptake by spinach (Spinacia oleracea L.) in solution culture.Plant Soil26199–105. 10.1023/b:plso.0000035539.58054.e1
63
ZhuY. G.HuangY. Z.HuY.LiuY. X. (2003). Iodine uptake by spinach (Spinacia oleracea L.) plants grown in solution culture: effects of iodine species and solution concentrations.Environ. Int.2933–37. 10.1016/s0160-4120(02)00129-0
64
ZushiK.MatsuzoeN. (2015). Metabolic profile of organoleptic and health-promoting qualities in two tomato cultivars subjected to salt stress and their interactions using correlation network analysis.Sci. Hort.1848–17. 10.1016/j.scienta.2014.12.030
Summary
Keywords
anti-nutrients, chemical eustressor, functional quality, floating system, micronutrients, mild salt stress, nutrient solution management, stress response
Citation
Rouphael Y and Kyriacou MC (2018) Enhancing Quality of Fresh Vegetables Through Salinity Eustress and Biofortification Applications Facilitated by Soilless Cultivation. Front. Plant Sci. 9:1254. doi: 10.3389/fpls.2018.01254
Received
25 May 2018
Accepted
07 August 2018
Published
22 August 2018
Volume
9 - 2018
Edited by
Dimitrios Savvas, Agricultural University of Athens, Greece
Reviewed by
Giancarlo Fascella, Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria (CREA), Italy; Smiljana Goreta Ban, Institute of Agriculture and Tourism, Croatia
Updates
Copyright
© 2018 Rouphael and Kyriacou.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Youssef Rouphael, youssef.rouphael@unina.it Marios C. Kyriacou, m.kyriacou@ari.gov.cy
This article was submitted to Crop and Product Physiology, a section of the journal Frontiers in Plant Science
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.