Tetragonia tetragonioides (Pallas) Kuntz. as promising salt-tolerant crop in a saline agricultural context
Introduction
Increasing population likely will result in an increase of the global food demand for at least another 40 years (Godfray et al., 2010). Lack of natural resources, especially high-quality cropland and renewable water resources, will reduce the food production potential in several regions (FAO, 2013). Moreover, the effects of climate change represent a further threat (Godfray et al., 2010), especially in marginal, already-stressed agroecosystems (Cheeseman, 2016). Today more than 34 MHa are salt-affected (FAO, 2011), either because they are coastal or because inappropriate irrigation practices have degraded soil and depleted or salinized groundwater (Cheeseman, 2016). Although significant advances have been made in the last 25 years in reducing hunger worldwide (FAO, 2013), the situation seems to be less optimistic in areas affected by both drought and salinity (Cheeseman, 2016). Given that the world's major crops have proven inadequate to supply people in these areas with sufficient amount of calories, proteins, fats and nutrients, new crops are needed that can specifically withstand such harsh ecological conditions (Cheeseman, 2016). New crops tolerant to saline conditions are likely to be found among edible halophytes. Halophytes are plants that can grow at salinity levels higher than 200 mM NaCl (Flowers and Colmer, 2008), roughly corresponding to half-strength seawater. Several morphological, physiological, and biochemical adaptations are adopted by halophytes to withstand or even to benefit from saline environments (Panta et al., 2014). Furthermore, favorable effects on yield and its quality can even be related to saline conditions (Flowers and Muscolo, 2015; Shannon and Grieve, 1998). The idea of growing salt-tolerant plants in agricultural systems irrigated with brackish and saline water is not new (Glenn et al., 1999; Rozema and Flowers, 2008; Rozema and Schat, 2013). However, advances in this direction have been slow, and in only a few cases has there been the goal of developing new crops (Cheeseman, 2016). According to Cheeseman (2016), this is due to the fact that there is little urgency for plant biologists, crop scientists, and politicians of the developed world. In the context of saline agriculture, the water requirements of salt-tolerant crops are met through brackish water and/or seawater, thus relieving pressure on fresh water resources. However, large-scale, sustainable agriculture involving pure seawater irrigation seems to be impractical for reasons mainly connected to the deterioration of soil structure (Breckle, 2009). Irrigating with seawater on fertile and well-structured soils would lead to a salt contamination through Ca2+/Na+ exchange and resulting clay dispersion (Ventura et al., 2015), with additional significant impacts on soil microbial properties (Chaudhary et al., 2016). On the other hand, there is growing interest in the possibility of recovering lost coastal soils while minimizing inputs, i.e. freshwater (Fedoroff et al., 2010); an ecologically-acceptable compromise to the using of saline waters for food production and the preservation of soil is represented by soilless cultivation (Atzori et al., 2019b).
Another benefit of complementary seawater irrigation relies on the fact that moderate saline stress has been often associated with an increase in plant-based compounds that demonstrate healthy properties for humans (Di Baccio et al., 2004; Sgherri et al., 2008). Plants cope with salinity by means of several strategies including selective accumulation or exclusion of ions, synthesis of osmotic solutes, induction of antioxidant compounds (Parida and Das, 2005) and secondary metabolite production (Ramakrishna and Ravishankar, 2011), most of which show positive effects on human health. Thus, halophytes under salinity condition could also become sources of biochemical compounds with the potential of additional nutritive value (Flowers and Muscolo, 2015). Tetragonia tetragonioides (Pallas) Kuntze, Aizoaceae, Caryophyllales -the common New Zealand spinach, and hereafter referred to as simply Tetragonia–is an annual herbaceous plant native to cool sandy and rocky seacoasts, notably in New Zealand, Japan, Argentina and Chile, now widely distributed throughout the world (Taylor, 1994). It is used as a vegetable, an ornamental ground and for medicinal purposes due to its anti-ulcerogenic and anti-inflammatory characteristics (Yousif et al., 2010a). Tetragonia is a salt-tolerant plant and several trials have shown that it may withstand an electrical conductivity (EC) of the growing medium as high as 10 dS m−1 (Neves et al., 2008; Wilson et al., 2000). One study identified a salt-induced growth response at salinity levels of 50–100 mM NaCl (EC 5–10 dS m−1) (Yousif et al., 2010b), though this salt-stimulated growth appeared to depend greatly on the age of the plant, which was further able to tolerate up to 17.4 dS m−1 in late-salinization treatments (Wilson et al., 2000). Similarly, in hydroponics conditions, Ahmed and Johnson (2000) set a salinity tolerance threshold for this species at an EC value around 12.5 dS m−1. Literature data on salinity tolerance refer solely to saline irrigation using NaCl solutions, whereas no information is available on the salinity tolerance of Tetragonia tetragonioides using seawater. Interestingly, for most species, salt stress tolerance seems to be higher when treated with seawater than with NaCl solutions treatments with the same EC (Boyko and Boyko, 1966). Further research is still needed to confirm such a statement, yet Sakamoto et al. (2014) suggest a similar assumption. In addition, this plant has been proposed as a salt-removing species, because of its high Na+ and Cl- uptake (Neves et al., 2014). Salt-removing species include grasses, shrubs and trees that can extract salts from contaminated soils. In contrast to costly desalination technologies such as thermal (distillation) processes, membrane-based processes, electro dialysis and reverse osmosis (Islam et al., 2019), phytodesalination is a cost-effective green technology for the remediation of salt-impacted sites (Hasanuzzaman et al., 2014). The same principle can also be tested in hydroponics, to assess a salt-removing species- capability of desalinating saline water (Islam et al., 2019). However, the salt removal potential of this plant has not been assessed in seawater-fed hydroponic systems. The current study thus had the aims of i) evaluating the effects of seawater irrigation on growth productivity of Tetragonia tetragonioides in hydroponic culture, ii) assessing the accumulation of ions and the production of osmotic solutes along with secondary metabolites related to physiological adaptation and to the nutritive value of the crop in response to different salinity levels, and iii) assessing the salt removal capability at increasing seawater concentrations in hydroponic conditions.
Section snippets
Experimental design, plant material and growth conditions
The trial was carried out in 2018 at the greenhouse facilities of the Department of Agricultural, Food, Environmental and Forestry Sciences and Technologies (DAGRI) at the University of Florence, Italy. A hydroponic system was set up with 18 plastic containers (4 l volume) that were continuously aerated. Seeds of Tetragonia tetragonioides (Pallas) Kuntze were obtained from the Tuttosemi company (www.tuttosemi.com) and germinated in a dark chamber at 18.5 °C starting from the 27th of July. Two
Growth
As reported in Fig. 1, no significant differences in growth were assessed throughout the trial between salt-treated plants and the control, even if a decreasing trend was observable for high seawater treated plants during the last three weeks of the experiment. Similar results were found for the RGR, where control plants showed a rate of 1.4 ± 0.4 g g−1 day-1 and medium and high seawater treated plants a rate of 1.2 ± 0.1 and 1.2 ± 0.2 g g−1 day−1 respectively. No significant differences among
Growth and morphological responses to increased salinity
The current trial shows that plant growth was not negatively affected by any seawater treatments even if a decreasing trend is observable in the last weeks of the experiment in 30% seawater treated plants. The results obtained in medium seawater treatment (EC 9.8 dS m−1) are in agreement with those found by other scientists Neves et al. (2008) and Wilson et al. (2000), who reported a salinity tolerance for Tetragonia at EC approx. 10 dS m-1. Similarly, Ahmed and Johnson (2000) found in
Conclusions
This species’ ability to achieve remarkable growth rates under saline conditions validates its potential in saline environments. The results of this study show that the production of the New Zealand spinach as a food can be obtained in hydroponic conditions characterized by salinity as high as 18 dS m−1. Plant water use dropped in saline conditions, yet thanks to an increased WUE the biomass production was not negatively affected, again validating the seawater irrigation of this species up to
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.
Acknowledgments
We gratefully acknowledge LINV and PNAT s.r.l. for inspiring and supporting this research. The study was also supported by the POR FSE 2014-2020 Program of the Regione Toscana with the "JFB - Jellyfish Barge: una serra galleggiante autosufficiente per coltivare il mare" Project (UNIFI_FSE2017). We wish to thank Dr. Emily Palm from DAGRI University of Florence for her linguistic support. We also gratefully acknowledge the participants of the Saline Futures conference (Leeuwarden, The
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