Like many other plants, the first threat faced by ornamental plants in a saline environment is the lowered external water potential caused by the presence of salt ions. This prevents plant roots from taking up water from the soil, and can even cause water to drain out of the cells (Feng et al., 2014a), thus reducing plants’ ability to grow and survive. Accumulation of organic and inorganic solutes in the root cell cytoplasm (Feng et al., 2015) reduces the water potential of the cells and ensures water uptake under salt stress conditions (Han et al., 2012; Shao et al., 2014). In the process, some small organic molecules (compatible solutes), such as proline, will synthesize and accumulate in the cytosol of plant cells as the osmotic adjustment substances to cope with the osmotic stress (El-Shawa et al., 2020). These are also used to protect the structure of cells and macromolecular substances. In some cases, exogenous application of compatible solutes can increase plant salt tolerance. For example, increased antioxidant capacity was observed in plants to which exogenous glycine betaine (GB) was applied, compared with those without (Roychoudhury and Banerjee, 2016). At the same time, inorganic ion accumulation is also the way in which most salt-tolerant plants, such as halophytes, to reduce the osmotic potential. In this process, ions such as Na⁺ and Cl⁻ mainly accumulate in the vacuole so they can be used for osmotic adjustment of the plant cell (Chen and Jiang, 2010). Accumulation of inorganic ions as a strategy that consumes less energy than synthesize organic substances.

In addition, more Na⁺ and Cl⁻ accumulated in the roots than in the shoots of Dendrobium orchid under saline conditions. This high Na⁺/K⁺ ratio in the roots contributed to osmotic adjustment (Abdullakasim et al., 2018). More proline accumulated in seedlings of sweet osmanthus [Osmanthus fragrans (Thunb.) Lour.], germinated from gamma-irradiated seeds than those of controls, thus the salt tolerance of the seedlings was increased by improving osmotic adjustment (Geng et al., 2019). Salinity reduced the leaf area and flower weight of marigold (Calendula officinalis L.), but increased the proline content in these plants. This increased proline content conferred salt tolerance to marigolds in saline conditions below 150 mM NaCl (Adamipour et al., 2019). Despite decreased seedling biomass, proline accumulated and was the main osmolyte responsible for the osmotic adjustment of ornamental plants in response to saline conditions (El-Shawa et al., 2020). In the ornamental crop Hyacinthus orientalis L., proline in the leaves increased under saline conditions of 6.1–8.6 g L⁻¹. The ornamental qualities of these flowers also increased, indicating promise that this crop could be cultured in saline soils with concentrations of sodium chloride as was used in the laboratory culture (Ulczycka-Walorska et al., 2020).

Ionic homeostasis in plant cells is the basis for development and metabolism, especially the higher K⁺ and lower Na⁺ concentration in the cytosol of salt-tolerant plant cells (Blumwald, 2000). In salt sensitive plants under salt stress, ionic disturbance is very important, while salt-tolerant plants have a greater ability to maintain ionic balance (Guo et al., 2019a). With a similar charge and physiological characteristics, Na⁺ might compete with K⁺ for active sites of enzyme transporters. Thus, competition between the two ions leads to disruption of enzymatic function and biosynthesis (Zhu, 2003). For plants to grow and develop well under saline conditions, maintenance of a proper ratio of cytosolic K⁺/Na⁺ is required. This, along with the homeostasis of other ions, such as Ca²⁺, Mg²⁺ and Fe²⁺, is also a reliable indicator of the level of plants’ salt tolerance (Munns and Tester, 2008).

In salt-tolerant plants, ionic homeostasis might be maintained by excluding salt ions in soil through the roots by Salt Overly Sensitive 1 (SOS1) and apoplastic barriers (Hose et al., 2001; Meyer et al., 2009; Krishnamurthy et al., 2011; Song et al., 2012; Gao et al., 2016); thus fewer ions might be translocated to, or accumulate in, the aboveground parts of the plant, such as leaf cells, by compartmentalizing salt ions into the vacuole and reducing the ionic concentration in cytoplasm (Qiu et al., 2007). Therefore, restraining ionic transport to the shoots and compartmentalizing toxic ions in the vacuole are the important pathways to enhance plants’ salt tolerance in saline environments (Hasegawa, 2013). In the ornamental plant Eugenia myrtifolia L., more salt ions accumulated in roots than in leaves to perform normal physiological metabolism under salinity conditions (Acosta-Motos et al., 2017). In salt-tolerant chrysanthemum varieties, growth increased under saline conditions, together with increased K⁺, Ca²⁺ and Mg²⁺ content, and more efficient usage of N and P (Rahi and Singh, 2011). Results in marigold (Tegeta patula) indicated that salt tolerance could be improved by enhanced potassium application (Aboutalebi Jahromi and Hosseini Farahi, 2016).

For the ornamental plant gerbera (Gerbera jamesonii Bolus ex Hook. f., cv. “Forsa”), the presence of NaCl (such as 30 mM) could mitigate the phenotypes in leaves and flowers affected by boron (Gómez Bellot et al., 2018). A steady K⁺/Na⁺ ratio was maintained despite high Na⁺ accumulation in the leaves of daffodils [Narcissus sp. (L.) Amaryllidaceae] when treated with different salt concentrations—even under 150 mM NaCl conditions (Veatch-Blohm et al., 2014). While for the halophytic ornamental plant Lobularia maritima L., which growth was unaffected by 100 mM NaCl with the relative ionic balance in roots and leaves (Hsouna et al., 2020). Another halophytic ornamental plant Sesuvium portulacastrum displayed an optimal growth treated with moderate salinity with accumulating of large amounts of true halophyte and shows an optimal development under moderate salinity with a large amount of salt ions accumulating in the leaves (Nikalje et al., 2018; Ding et al., 2022). In Callistemon laevis treated with NaCl, little Na⁺ concentration was detected in the leaves, and more Na⁺ accumulated in the roots and stems, indicating that more salt ions were prevented from reaching the aboveground parts of the plant (Álvarez and Sanchez-Blanco, 2014). In ornamental grasses, such as Eragrostis spectabilis (Pursh) Steud., and Panicum virgatum L. “Northwind,” high visual quality was maintained when treated with NaCl, despite high concentrations of salt ions (Na⁺ and Cl⁻) accumulating in leaves (Wang et al., 2019c). In Lobelia erinus, plant growth and biomass were reduced with increased salinity, while salinity (30 or 50 mM NaCl) had no effect on flower production, and no toxic symptoms were observed on leaves, despite high accumulation of Na⁺ and Cl⁻ in leaf tissues. This indicates that L. erinus could be used for urban landscaping (Escalona et al., 2013). A similar result was observed in pansy (Viola x wittrockiana Gams.), which displayed salt tolerance at levels of 5 or 7 g L⁻¹ NaCl (Pušić et al., 2019). Under salt stress, uptake of Ca²⁺, Mg²⁺, and Na⁺ in the shoots of marigold (Tagetes erecta L.) increased, indicating an increase in salt tolerance (Koksal et al., 2016). When Callistemon citrinus plants were subjected to salt stress, greater Na⁺ storage was detected, which played a role in maintaining plant quality, and indicating that C. citrinus could be cultured with 4 dS m⁻¹ saline water (Álvarez and Sanchez-Blanco, 2014).

It is well known that high salinity decreases K⁺ content in plants. A saline environment reduced the growth of marigold, with decreased K⁺ content, while the Mg²⁺ content increased in the leaves under such conditions (Koksal et al., 2016). However, the K⁺ content, as well as the carotenoid content, in pelargonium (Pelargonium hortorum L.H. Bailey) leaves was not affected when plants were grown at salinities lower than 1.976 g L⁻¹. Meanwhile, the increased anthocyanin and proline content in leaves might be important in ameliorating the adverse effects caused by salt stress (Breś et al., 2016).

Salt-tolerant species can maintain ion homeostasis during growth, and this is inseparable from the roles of membrane-bound ion transporters, such as Na⁺/H⁺ antiporters. Under salt stress conditions, the plasma membrane-located Na⁺/H⁺ antiporter SOS1, and the NHX antiporters on tonoplast membranes are vital in maintaining the cellular ion homeostasis by transporting excess Na⁺ out of the cells and into the vacuole (Munns and Tester, 2008; Yue et al., 2012). In the working model of the SOS system pathway, cellular Ca²⁺ signals were identified as being involved. Firstly, salt stress induced an increased concentration of Ca²⁺ in the cytosol, which is sensed by, and causes the activation of SOS3. SOS2 is then activated by activated SOS3, forming an SOS2–SOS3 complex. Thirdly, SOS1 is activated, which mediates the transport of excess Na⁺ out of the cells and maintains a relatively low Na⁺ concentration in the cytoplasm (Tang et al., 2015). A significant reduction in Na⁺ content, and a favorable K⁺/Na⁺ ratio, was detected in transgenic plants—especially in the youngest leaves—in Chrysanthemum crassum overexpressing the CcSOS1 gene. Thus, the transgenic plants demonstrated higher salt tolerance, up to 200 mM NaCl (An et al., 2014).

NHX family transporters are localized to the tonoplast, they are widely considered as the players to sequestrate sodium (Na⁺) into vacuoles and to avert the cytoplasmic ion accumulation when plants exposed to salinity. In Arabidopsis, the expressional levels of AtNHX1 and AtNHX2 genes were upregulated under osmotic stress or by abscisic acid (ABA; Jiang et al., 2011). Overexpression of HtNHX1 and HtNHX2 transporters from Helianthus tuberosus improved the salt tolerance of rice (Zeng et al., 2018). Salt or drought tolerance was enhanced in transgenic sweet potato [Ipomoea batatas (L.) Lam.] with overexpression of the IbNHX2 gene (Wang et al., 2016).

In view of this research on the ornamental flowering plants, salt-tolerant varieties seem to prefer to accumulate inorganic ions in the vacuole to lower cell water potential, and simultaneously synthesize some compatible solutes in the cytosol to balance the decline of vacuolar water potential. This strategy thereby ensures the growth of plants and their increasing salt tolerance. A reconstruction of osmotic and ion homeostasis pathways in a plant cell under saline stress is shown in Figure 1A.

Reactive oxygen species (ROS) are free radical molecules that are inevitably produced during plant metabolism. They have important roles in plant growth, development, and adaptation to stressors. Under normal conditions, ROS production and scavenging is kept in balance. However, when plants are subjected to adversity, such as salt or drought stress, more ROS are produced, and they will accumulate if production exceeds scavenging. Excess accumulation of ROS damages structural and metabolic plant processes (Pang et al., 2011). In salt-tolerant species, antioxidant capacity is enhanced to scavenge accumulated ROS, thus restoring the balance of ROS. Usually, ROS scavenging is implemented in two main ways: non-enzymatic and enzymatic mechanisms (Bowler et al., 1992; Mittler, 2002). Superoxide dismutase (SOD) and catalase (CAT) are usually considered the two most important antioxidant enzymes, but others, such as ascorbate peroxidase (APX), peroxidase (POD), and glutathione reductase (GR), are all employed to scavenge ROS in enzymatic reaction systems (Kozi, 1999). Furthermore, they work together to regulate the balance of ROS in plants.

When ROS levels are in equilibrium, membrane stability is maintained and normal metabolism occurs in plants (Li et al., 2012; Luo et al., 2013). Tolerance to other stresses, such as drought or heat, is also enhanced (Reddy et al., 2004). During ROS scavenging, enzymic amount and enzymic activity are strongly related to plants’ ROS scavenging ability. Overexpression of genes related to antioxidant enzymes could improve ROS scavenging, thus enhancing stress tolerance (Caverzan et al., 2016). In the ornamental plant Lavandula angustifoli Mill., antioxidant enzymes, including SOD and CAT, were activated under salt stress (even at 300 mM NaCl), with enhanced accumulation of flavonoids and phenolic substances, thus improving plants’ oxidation tolerance (Szekely-Varga et al., 2020). In salt-treated Echinacea species, E. purpurea displayed higher Na⁺ exclusion ability, and enhanced antioxidant activity of APX and SOD, but CAT activity was reduced and there was no change in GR activity (Sabra et al., 2012). The highly salt-tolerant ornamental plant, Parthenium hysterophorus could grow in a concentration as high as 160 mM NaCl. It also displayed increased proline, ascorbate, and glutathione contents, and elevated activity of enzymatic antioxidants, such as SOD, GR, and CAT (Ahmad et al., 2017). With the high salt tolerance (800 mM NaCl) of the ornamental plant Nerium oleander L., the activities of SOD and CAT were increased in the leaves and roots, even though more salt ions accumulated in these organs (Kumar et al., 2017). In tagetes (Tagetes patula L.), polyphenol and carotenoid contents, and antioxidant activities increased under 100 mM NaCl, and there was high accumulation of N, P, Zn, and Na in the flowers (Chrysargyris et al., 2018). In Eugenia myrtifolia L., SOD content and activity in the leaves increased despite reduced APX content and activity under saline conditions, and lower Na⁺ in the leaves than roots ensured normal photosynthesis (Acosta-Motos et al., 2015). The antioxidant ability of plants could also be enhanced by gene mutation. The activities of SOD, CAT, and POD were significantly increased in seedlings of sweet osmanthus germinated from gamma-irradiated seeds compared with controls; seedlings’ salt tolerance was improved by regulating ROS balance (Geng et al., 2019). When treated with 80 mM NaCl, growth and the activities of antioxidant enzymes of Catharanthus roseus plants were inhibited. However, the salt tolerance of the seedlings was enhanced, with increased plant weight, SOD, and POD activities when plants were grown with NaCl and propiconazole, except leaf area and stem length decreased (Jaleel et al., 2008).

Salt tolerance is different even in different varieties of the same species. In Amaranthus tricolor, ascorbate, carotenoids (non-enzymatic antioxidant), and SOD and APX (antioxidant enzymes) activities were increased in the salt-tolerant varieties compared with the salt-sensitive ones, indicating that increased ROS quenching ability conferred higher tolerance (Sarker and Oba, 2020). The activities of APX, SOD, POD and CAT in marigold were enhanced when plants were grown under conditions below 150 mM NaCl, then decreased at 200 mM NaCl (Adamipour et al., 2019), indicating that marigold could be developed for cultivation on saline lands.

In saline environments, large amounts of ROS accumulate in plants, resulting in ROS imbalance. Salt-tolerant ornamental varieties usually show improved ROS scavenging ability, both from enzymatic and non-enzymatic reaction processes, so this could be considered an indicator of high salt tolerance in ornamental flowering plants (Figure 1B).

Another measure that plants employ to reduce cellular ion content is to reduce the uptake of salt ions in the roots, or to excrete some absorbed salt ions out of the plant (Figure 1C). Thus, a relatively higher Na⁺ content will be detected in roots than in shoots (Abdullakasim et al., 2018). The same was found under cadmium stress (Qi et al., 2020). Salt tolerance was conferred by a special structure, such as thickened apoplastic barriers (Krishnamurthy et al., 2020). In some ornamental plants, such as Escallonia rubra, Cestrum fasciculatum, Viburnum lucidum (Cassaniti et al., 2009), and Aloe vera (L.; García-Caparrós et al., 2016), the mechanism employed to respond to salinity correlated with higher accumulation of ions in roots than in shoots. Na⁺ content in rhizomes of Iris germanica was usually lower than in leaves or roots under saline conditions, which may indicate a salt stress adaptation mechanism (Zhao et al., 2021). Perhaps, in such plants under saline conditions, the greater accumulation of salt ions in roots is associated with structural changes of roots related to the apoplastic exodermal barriers, such as the thickened endothelium, preformed suberin lamellae and Casparian bands (Andersen et al., 2015). In Opisthopappus taihangensis (Ling) Shih and Iris germanica (Meyer et al., 2009; Yang et al., 2020), salt ion uptake was reduced in root cells. Additionally, the absorbed ions in root cells could also be excreted out of the roots cells through antiporters such as SOS1 (Song et al., 2012; Gao et al., 2016; Mohammadi et al., 2019), resulting in increased ion accumulation in roots and reduced salt ion transport to shoots. However, the relationship between salt ion accumulation and apoplastic barriers remains to be investigated in ornamental flowering plants.

As well as reducing salt ion uptake through structural features, absorbed salt ions can also be removed from xylem. The HKT1 (high-affinity K⁺ transporters) gene plays vital roles in this process (Ali et al., 2016), and the HKT1 transporter can also restrict Na⁺ entry into plant roots (Rus et al., 2001). With the function of HKT1 localized in xylem parenchyma cells, Na⁺ flux to the shoot tip was actively reduced and excess Na⁺ accumulated in the root zone of plants. In Arabidopsis, AtHKT1 was proposed to recirculate Na⁺ in the phloem, reducing the allocation of Na⁺ in the shoot, and correspondingly increasing Na⁺ content in roots (Davenport et al., 2007).

Furthermore, absorbed Na⁺ can also be excreted from root cells through transporters such as SOS1, which are localized in the plasma membrane of root cells (Shi et al., 2000; Oh et al., 2009), like the CcSOS1 transporter in chrysanthemum (Song et al., 2012; Gao et al., 2016). Perhaps, in ornamental flowering plants, the SOS1 transporters also play a vital role in pumping Na⁺ out of root cells.

Finally, absorbed salt ions (especially Na⁺) can be partitioned into the vacuole via transporters such as NHX1, which is localized in the tonoplast. On the one hand, vacuoles act as the ultimate Na⁺ sinks to reduce Na⁺ accumulation in cytoplasm. On the other hand, the water potential of root cells is also reduced to ensure water uptake in saline environments (Liang et al., 2015; Guo et al., 2020).

Under saline conditions, the response mechanisms triggered are different in different ornamental species. In some ornamental species with salt secreting structures like salt glands or salt bladders, especially Limonium species (Feng et al., 2014b; Leng et al., 2018; Lu et al., 2020; Mi et al., 2021), excess salt ions transported to aboveground parts of the plant are also excreted outside of the plant body through salt glands (García-Caparrós et al., 2016). Limonium species have remarkable salt tolerance thanks to their typical salt excreting salt glands in the leaves; they can grow and develop well in environments containing NaCl concentrations of more than 200 mM NaCl (Souid et al., 2016; Mi et al., 2021). Besides excreting excess salt ions out of the leaves, some of the absorbed salt ions are regionalized; they accumulate in vacuoles and regulate the osmotic potential of leaf cells (González-Orenga et al., 2021). Therefore, more ornamental flowering plants that possess these leaf structures, and which also have high value, should be exploited further.

Some ornamental plants, such as Portulaca (Borsai et al., 2020), as well as Aloe vera (L.), exhibit leaf succulence when they grow in saline or drought environments (García-Caparrós et al., 2016). In response to salt stress, large amounts of ions were accumulated in the vacuoles of leaf cells in such plants, and the leaf succulence was subsequently displayed higher ability to cope with the salt stress. And the specific anatomical adaptation to salinity in halophytic ornamental flowering plants is summarized in Supplementary Figure S1.

To respond to saline conditions, ornamental plants have evolved many other adaptations; for example, altering leaf function, reducing chlorophyll content, and reducing stomatal size and aperture (García-Caparrós and Lao, 2018). In carnation (Dianthus caryophyllus), salt tolerance was mainly associated with the reduction of water loss by reducing stomatal conductance and increasing epicuticular wax (Kwon et al., 2019). Chrysanthemum morifolium treated with different levels of salinity displayed salt tolerance, with increased photosynthetic pigments, and a better seedling growth (Vanlalruati et al., 2019). Photosynthetic pigments are vital in photosynthesis. Under stress, inhibited photosynthetic efficiency in plants was related to reduce chlorophyll content and damaged photosynthetic systems (Wu et al., 2016). Some plants showed higher tolerance to salinity in photosynthetic processes. For example, low energy dissipation rates and high light harvesting efficiencies were detected in Aster tripolium L. plants exposed to even 250 mM NaCl, with increased density of reaction centers (RC), enhanced electron transport ability, and lower energy dissipation rates (Duarte et al., 2017). In the ornamental plant Eugenia myrtifolia L., when treated with salinity, the normal photosynthetic system was protected by limiting salt ion accumulation in leaves, as well as by increasing chlorophyll content (Acosta-Motos et al., 2017). The salt tolerance of Aloe vera associated with high efficiency of photosystem II and ROS scavenging was enhanced by exogenous application of proline (Nakhaie et al., 2020). With the application of exogenous GB or proline, higher chlorophyll and K⁺ content was detected in Viburnum lucidum L. and Callistemon citrinus Stapf (Cirillo et al., 2016), as well as calendula (Calendula officinalis L.) plants (Soroori et al., 2021). Proline content and the stability of the cellular membrane were increased by exogenous application of ascorbic acid on calendula plants under salinity stress (Azizi et al., 2021).

The salt tolerance of ornamental flowering plants could also be enhanced, and the salt content reduced, by shedding old leaves. For example, older leaves are shed to reduce Na⁺ content in Kalanchoe blossfeldiana Poelln. In Gazania splendens Lem sp., multiple strategies are employed, such as accumulating the majority of Na⁺ and Cl⁻ in the roots, secreting salt ions out of leaves through salt glands, increasing the succulence index of living leaf tissue, and shedding old leaves (García-Caparrós et al., 2016). Thus, G. splendens is suitable for planting in saline environments. The adaptive strategies of shoots are summarized in Figure 1D.