In the context of climate change and its effects, including increases in global temperature, scarcity of water resources for agriculture (lower rainfall, higher evaporation and evapotranspiration, reduced groundwater recharge) and salinisation of the soil in fields cultivated under irrigation, abiotic stress is already limiting food production through reduction of crop yields. This problem will become even more severe as the area affected by climate change-induced desertification extends. For example, long periods of intense droughts suffered in the Sahel region of Africa during the last decades have caused a substantial decrease in food production (1, 2). Crop yields were also significantly reduced by drought in the U.S. several times in the previous century, from 30% to more than 50%, mostly affecting maize production in the Midwestern States – in the so-called ‘corn belt’ – with the most severe droughts registered in the 1930s or in 1988 (3, 4, 5). Progressive ‘secondary’ salinisation of irrigated land, due to the continuous accumulation in the soil of toxic ions present in irrigation water, also limits agricultural production, contributing to the enormous challenge of feeding the world’s growing population in the next decades. At present, more than 800 million hectares of agricultural land worldwide is affected by salinity, to a greater or lesser degree (6) and it has been predicted that before 2050 salinity will seriously affect 30% of the available arable land area and about 50% by 2100 (7). Therefore, enhancing drought and salt stress tolerance of our major crops (for food supply and other applications) using both, traditional breeding and genetic engineering, should be a research priority in plant biotechnology in the coming years.
The vast majority of terrestrial plants, including all major crops, are glycophytes or salt-sensitive plants. Yet, a small percentage of angiosperm species (less than 1%) belonging to different genera and families, are adapted to saline environments and can complete their life cycle in habitats with soil salinity equivalent to 200 mM NaCl or more; these plants are defined as halophytes (8). Since plants show a continuous range of tolerance, from species extremely sensitive to salt to other highly tolerant, there are many taxa that, although cannot be considered as halophytes according to this definition, are nevertheless relatively resistant to salinity when compared to our present major crops; they may include some minor crops or potential crop species not cultivated commercially at present. Similarly, other species may be interesting as potential crops because of their relatively high tolerance to drought.
Plant adaptation and tolerance to abiotic stresses are regulated by complex molecular networks. Tolerance to water deficit, soil salinity and other environmental stress conditions involves responsive mechanisms to re-establish homeostasis, to maintain osmotic balance, to repair damaged proteins and membranes and to activate antioxidant systems – as all these stressful conditions cause oxidative stress as a secondary effect. While plant resistance to pathogens (biotic stress) is generally dependent on monogenic traits, the mechanisms of abiotic stress tolerance are multigenic and more complex, which makes them more difficult to investigate and, eventually, to control and manipulate (7). Paradoxically, most studies on the responses of plants to abiotic stresses and the mechanisms of tolerance have been performed using stress-sensitive species, especially the model plant Arabidopsis thaliana (9) or some crops such as Oryza sativa (10), Nicotiana tabacum (11), or Solanum lycopersicum (12). All plant species appear to have built-in capabilities for stress perception, signalling and response, although they clearly differ in their sensitivity and reaction to the decrease in water potential caused by drought, high salinity, low temperature or other abiotic stresses. Differences between sensitive and tolerant species seem to be of a quantitative rather than of a qualitative nature, resulting from changes in the expression patterns of a primary, conserved set of genes (9, 13, 14).
The domestication of wild halophytes (and other relatively salt-tolerant species) could be considered a substitute retrieval practice for plant breeders offering viable alternatives for saline agriculture. The sustainable use of salt-tolerant species has multiple purposes as food and feed crops, as a source of renewable energy (biofuels: bioethanol and biodiesel) (15), as raw material for different industrial uses and also for regeneration of degraded areas. Another advantage of saline agriculture is that commercial cultivation of halophytes might be combined with aquaculture of sea fishes, providing a broader range of products to the food market (16). A few scientific reports have been published emphasising the economic potential of salt-tolerant plants in agriculture as a source of food, oils, fibres (17), pharmaceuticals or with environmental potential for protection and biodiversity conservation. These include, for example, potential vegetable crops and grain crops such as: Salicornia europaea (18); Aster tripolium, Sesuvium portulacastrum (19); Inula crithmoides (20, 21); Chenopodium quinoa (22) and Distichlis palmeri (23); oilseeds such as Salicornia bigelovii (24) and Suaeda fruticosa (25) and medicinal plants: Helianthus tuberosus (26), Achillea mellifolium, Verbena officinalis (27).
Cultivation of drought and/or salt-tolerant plants in marginal lands, arid zones or salinised cropland under rainfed conditions or using low-quality, salinised water for irrigation, will contribute to food production (apart from other economically interesting uses), through a more efficient use of limited resources such as fertile land and good-quality irrigation water, since they will not compete with conventional crops, which cannot grow under those conditions. These ‘new’ crops could include some species and cultivars of the genus Portulaca, which appear to have a relatively high resistance to drought and soil salinity, as compared to most standard crops (28).
This review attempts to give an overview of the most general responses of plants to abiotic stress, especially to drought and salinity, with focus on Portulaca taxa (but including also other examples), to summarise what is known for this genus. Although the information available is still limited, there are data indicating that Portulaca species and cultivars show variable levels of resistance to salinity and water deficit. For this reason, Portulaca can be considered as a suitable model to carry out comparative studies on their stress responses; this will, in turn, contribute to improving our knowledge on the general mechanisms of abiotic stress tolerance in plants.
The Genus Portulaca: Potential as Biological Model and Economic Interest
The genus Portulaca includes about 100 species, with a wide distribution, predominantly in tropical and subtropical regions, and a high morphological variability (29, 30, 31). Studies in different areas – taxonomy, ecology, physiology, biochemistry or genetics – have been performed on Portulaca species, including also the assessment of the genetic variability within the genus. Evolutionary relationships of Portulaca taxa were addressed through a BEAST [‘Bayesian evolutionary analysis by sampling trees’ (32)] analysis of a combined matrix of molecular markers (ITS) and several specific gene sequences; the obtained dendrogram was then correlated with the known taxonomy, morphology, biogeography, and chromosome number variation of the genus (33). Responses of Portulaca to abiotic stresses, such as elevated temperatures, water deficit or high salinity, have also been investigated by different authors (34, 35, 36). Even though most of these studies have been carried out in a single species, P. oleracea, it has been established that this and other taxa of the genus are relatively resistant to drought and/or salt stress, as compared to the major crops (35, 37).
The accumulated information on Portulaca species, together with the relatively easy handling of the plants, their size and short life cycle – eight to ten weeks under optimal conditions – would suggest that this genus can be used as a suitable research model in plant biology. In general terms, obviously, Portulaca cannot compete with other well-established model species, such as Arabidopsis thaliana and several major crops, for which many more data and resources are available. Yet, studies on abiotic stress tolerance in plants require the use of different models, as the responses to stress that are relevant for tolerance vary between species. Considering that Portulaca provides a large number of species and cultivars, with a common genetic background but – presumably – a wide range of tolerance degrees to water and/or salt stress, this genus represents an attractive model for these specific studies. Comparative analyses of the mechanisms activated in response to controlled stress treatments in different taxa, and correlation with their relative levels of stress resistance should allow identifying the responses that are most important for tolerance in this genus, thus complementing information obtained from studies in other genera.
In addition to their possible use for basic research, many Portulaca species are also interesting from an economic point of view, as potential ‘new’ crops for sustainable agriculture. Common purslane (P. oleracea) is a nutritious herb with a high content of ‘healthy’ antioxidant compounds and essential nutrients, such as α-linolenic acid, omega-3 and omega-6 fatty acids, ascorbic acid, glutathione, α-tocopherol and β-carotene (38). There are few vegetable sources rich in ω-3 fatty acids; this, together with the species’ relatively high salt tolerance, explains the growing interest to promote purslane as a new vegetable crop (35). In Chinese folklore, P. oleracea is known as ‘vegetable for a long life’ with a long history of use as both, an edible plant and traditional herbal medicine. It has been used for alleviating pain and swelling and has been attributed antibacterial, antiviral, antidiabetic or enhancing immunity properties (39). It has been recently suggested that P. oleracea may help to reduce the occurrence of cancer and cardiovascular diseases (40).
Plants of the Portulacaceae family include also cash crop species that can tolerate moderate to high salt stress, producing profitable amounts of dry mass even at high salinities (41, 42). Moreover, they include as well several ornamental species, such as Portulaca grandiflora, P. umbraticola, P. villosa or P. halimoides, which are highly appreciated for their wide range of flower colours, type and size, and their potential use in garden design even in unfavourable environmental conditions. The availability of many commercial cultivars of these ornamental species increases the genetic variability of the genus as a whole and facilitate the comparative studies mentioned above.
Plant Responses to Salt and Water Stress
An unfavourable environment due to salinity, drought or other stressful conditions induces a complex set of responses in plants, which can sense the stress and react activating many different mechanisms, at the physiological, biochemical and molecular levels that may (or may not) enable their survival (43, 44, 45). Plants have even the capacity to ‘remember’ past exposure to abiotic stresses, modifying their responses when subjected again to the same stress so that the adverse conditions can be more easily overcome (46). The outcome of these responses depends on different factors, such as the type, intensity and duration of the applied stress, the combination of different stressful conditions, the tissue or organ of the plant affected and, obviously, the intrinsic level of tolerance of the species. It is also important the phase of the plant’s life cycle, with younger individuals being generally more sensitive to stress than older plants (e.g. 47). As mentioned above, all plants share the same basic responses to abiotic stress. However, information about the molecular mechanisms relevant for the tolerance to a specific type of stress of a given species – or group of related taxa – is still insufficient.
Salt and water stress responses during seed germination
Germination of seeds and early vegetative growth are in general the developmental stages most sensitive to abiotic stress and, therefore, a bottleneck in the plant life cycle under stress conditions. The responses to salt and water stress at this very early stage of development have been already investigated in different Portulaca taxa – although most studies have been carried out on common purslane (P. oleracea) – showing the progressive inhibition of seed germination as the intensity of the stress increases; high salt concentrations and lack of water both cause osmotic stress on germinating seeds and early seedlings but, in general, at the same osmotic potentials salinity has a more deleterious effect than water deficit, producing a stronger inhibition of germination, as reflected by lower final germination percentages and longer germination times (28,37,48, 49, 50, 51). Regarding the stress-induced inhibition of seed germination, Portulaca species are not different from most other plants, which show similar responses to water deficit or soil salinity, although with clear differences between species in their relative tolerance. This has been shown, for example, in Asparagus officinalis and Solanum lycopersicum (52). Likewise, in a study on the salt tolerance at the seed germination stage of Ocimum basilicum, Eruca sativa and Petroselinum hortense (53) it was found that parsley was the most sensitive of the three species, showing the strongest inhibition of germination with increasing salt concentrations.
In some ornamental plant species such as Ageratum mexicanum (54) and Tagetes patula (54, 55), increasing the substrate salinity led to the inhibition of plant growth at the highest salt concentration tested. Catharanthus roseus, when subjected to salt treatments showed delayed germination at low salinity levels and completed inhibition at high salt concentrations (56, 57). Similarly, seed germination in Limonium cossonianum was also largely affected under conditions of high salinity (58). Despite the examples above and many other reports on other species supporting this general behaviour, seed germination of some halophytes (salt-tolerant plants) is enhanced to different degrees at low or moderate salinity levels and inhibited only at higher salt concentrations (e.g. 59).
Growth inhibition as a general response to drought and salinity
The most widespread and rapid response of plants to any type of stress is inhibition of growth as they redirect their resources – assimilates, metabolic precursors, energy – from primary metabolism and biomass accumulation to the activation of specific defence mechanisms (60, 61, 62, 63). Therefore, the most straightforward and convenient way to assess the effects of drought and salt treatments on plants is based on the quantification of the degree of stress-induced growth inhibition. This can be done by determining different growth parameters (depending on the species), such as plant height or stem length, number of leaves, total leaf area, number of flowers or fresh and dry weight of the treated plants, in relation to the untreated controls.
This kind of measurements has been performed on seedlings of 12 common purslanes and cuttings of 13 ornamental purslane accessions treated with increasing NaCl concentrations, providing salinities of 0, 10, 20, 30 and 40 dS m−1 (57). It was found that the height of the salt-treated plants was slightly (but significantly) reduced in relation to the corresponding non-stressed controls, in a concentration-dependent manner, from 7% at the lowest salinity tested to about 20% at the highest. A similar pattern was observed regarding the relative changes in the number of leaves upon salt treatment of the plants; these numbers, which varied in the different purslane accessions, were generally reduced as compared to those of the corresponding controls in parallel with the increase in external salinity (64). According to the measured growth parameters, differences in their relative salt tolerance were detected among the selected purslane accessions.
As for the number of leaves, the number of flowers of the studied purslane taxa also differed from one accession to another in untreated plants and decreased in all of them with increasing salt concentrations although, here again, with quantitative differences between accessions. Among all the investigated morphological traits, flowering appeared to be the most affected by salinity: at 40 dS m−1, most accessions showed a reduction in flower number of more than 90% as compared to the corresponding controls or produced no flowers at all (64). Previous reports also revealed delayed flowering and fruiting as a response to stress in other ornamental and crop species, such as Iris hexagona (65), Cakile edentula (66) and Sporobolus virginicus (67).
Plant fresh weight and dry weight (or water content) are the parameters most often used to quantify the degree of stress-induced inhibition of growth. Their measurement, however, requires uprooting and killing the plant, contrary to merely determining the height of the plant or counting the number of leaves or flowers; both, fresh and dry weight are affected by drought and salinity (56). The plants of the tested Portulaca accessions differed in size (at the same developmental stage), and therefore in fresh and dry weight, before being submitted to the salt stress treatment; yet in all taxa biomass accumulation was reduced with respect to the corresponding controls at the end of the experiments, in a concentration-dependent manner; that is, the most substantial inhibition of growth was detected in the presence of the highest salt concentration tested (64).
The aforementioned changes observed in plants as a response to salt or water deficit treatments are partly due to the shedding of old leaves while maintaining the younger ones (37, 68), as well as to the reduction of the area of the leaves, which is accompanied by their decolouring, from green to yellowish (28, 69). Shedding of older leaves reduces water loss and can be considered as a recycling programme within the plant, which allows reallocating stored nutrients to the younger leaves. An additional, early response to salt and drought stress is stomata closure, which also protects the plants from extensive water loss; this might result in cell dehydration, runaway xylem cavitation and even death. (70, 71).
Physiological responses to stress
Many reports confirm the inhibitory effects of excess salt and drought on several basic physiological and biochemical processes, of which photosynthesis is paradigmatic. The stress effects on photosynthesis can be partly assessed measuring changes in the levels of photosynthetic pigments in the stressed plants. The results of specific studies (e.g. 72, 73, 74) indicate that salinity reduces the content of chlorophylls (a and b) and carotenoids. According to Gummuluru et al. (75), chlorophyll contents and photosynthetic activity are positively correlated; therefore, reduced chlorophyll levels must contribute to the inhibition of photosynthesis that has been generally detected under abiotic stress conditions (48, 62). Significant decreases in chlorophyll contents as a result of salt and drought stress treatments have also been observed in many plant species, including Paulownia imperialis (76), Phaseolus vulgaris (77) and Carthamus tinctorus (78) to give only a few examples.
Chlorophyll contents in purslane accessions subjected to salt stress treatments were also reduced in parallel to the increasing external salt concentrations, although the relative reductions with respect to the non-stressed controls were maintained below 40%, even at 32 dS m−1, the highest salinity tested (41). In plants kept under water deficit conditions, chlorophyll concentrations also declined, but only slightly (28, 79). This indicates that at least some Portulaca taxa are relatively resistant to drought and salt stress and could be promising candidates for commercial cultivation in arid and saline soils; they could also be used for ecosystem restoration in specific habitats affected by the effects of climate change.
Apart from affecting photosynthesis, salinity and water deficit cause profound changes in water relations in the plants, for example by reducing the osmotic potential of the leaf sap (80, 81, 82). Osmotic stress, or reduced turgor pressure, especially in root cells, due to the high concentration of ions in the soil or to scarcity of water, is a common effect of salinity and drought, which causes reduced water uptake, thus inducing a cascade of effects leading to inhibition of plant growth and, eventually, to plant death (83, 84).
Biochemical responses to salt and drought stress
Sodium chloride is by far the most abundant salt in salinised soils worldwide. Na+ and Cl-, especially Na+, are toxic at relatively low concentrations; therefore, uptake of these ions by the plant can result in cytoplasmic toxicity. Accordingly, one of the essential mechanisms of defence against salt stress depends on the control of ion homeostasis, by regulating the cellular uptake and transport within the plant of Na+ and other toxic ions. Most plants, when growing in saline soils activate mechanisms to block transport of Na+ to the shoots; such plants are defined as ‘Na+ excluders’ (85). In contrast, some plant species accumulate high Na+ concentrations in the shoots and are thus considered Na+ ‘includers’ (or ‘accumulators’). The most salt-tolerant wild species, some dicotyledonous halophytes, belong to this group, as well as a few glycophytes such as barley, which is relatively resistant to salt, in comparison with other crops (86). P. oleracea also falls into this category, since salt treatments led to a significant increase of Na+ concentrations in roots and leaves, which was accompanied by a parallel reduction of K+ levels (79). A more recent study (87) also showed the accumulation of toxic ions (Na+ and Cl-) in the leaves of P. oleracea plants under high salinity conditions.
High soil salinity interferes with plant mineral nutrition, as Na+ and K+ show very similar uptake mechanisms, competing for the same membrane transport systems (88). Therefore, in general, salt stress leads to an imbalance on root and leaf K+ and Na+ levels; mechanisms that help to keep relatively high cellular K+/Na+ ratios appear to be relevant for salt tolerance (89). In addition to Na+, the ‘ion toxicity’ component of salt stress is partly due to Cl-, the most prevalent anion under saline conditions (85, 90). For example, it has been reported (91) that leaf injury was associated with a high concentration of Cl- in susceptible soybean varieties; also, salt-sensitive lines of barley contained higher leaf Cl- levels than more resistant cultivars (85).
Proline (Pro) accumulation has been attributed an essential role in the mechanisms of plant responses to abiotic stress, contributing in many cases to osmotic adjustment (as the only compatible solute or together with an increase in the levels of other osmolytes) and as an osmoprotectant. Free Pro is known to occur widely in higher plants, and it very often accumulates to high concentrations in response to environmental stresses (92, 93, 94, 95, 96, 97). In many cases, Pro accumulation has been positively correlated with stress tolerance; for example, transgenic tobacco plants over-expressing the P5CS gene – encoding the enzyme that controls the rate-limiting step of Pro biosynthesis from glutamate – show an increased Pro content and enhanced resistance to drought and salinity (98). Furthermore, Pro induces the expression of stress-responsive genes, bearing proline-responsive elements (e.g. PRE, ACTCAT) in their promoters (99, 100, 101). There are some reports describing Pro accumulation patterns in P. oleracea under different salinity and drought conditions, and it was found that free Pro content in leaves of purslane plants increased in response to stress, up to three-fold over control levels (42, 48, 102).
Proline accumulation does not always correlate positively with stress tolerance in higher plants. For example, in rice plants grown under high salinity conditions, the accumulation of Pro seemed to be a symptom of injury of the leaves caused by salt rather than being a direct indicator of salt stress (103). Likewise, salt-induced increase in Pro content was not associated with tolerance in two sorghum genotypes differing in the sensitivity to salt (104). In other species, Pro accumulation correlates negatively with tolerance, with higher concentrations measured in the most sensitive genotypes, for example in different bean cultivars (105); in these cases, Pro can be considered as a reliable stress marker but is not involved in stress tolerance mechanisms.
Among the many quaternary ammonium compounds (QACs) with a functional role as compatible osmolytes in plants subjected to abiotic stress, glycine betaine (GB) occurs most abundantly in response to dehydration (106, 107, 108) and there is generally a good correlation between relative GB contents and the degree of tolerance (109). GB effectively stabilises different macromolecular structures under stress conditions, including the highly ordered cellular membranes or the quaternary structures of enzymes and other complex proteins (110). Many crop plants accumulate GB in response to stress, including sugar beet (111), spinach (112), barley (113) and sorghum (114). In these species, GB reaches typically higher concentrations in tolerant genotypes than in sensitive ones, in response to the same level of stress. However, this is not a general phenomenon, as reported for other species of Triticum, Agropyron and Elymus (90). Similarly, referring to Portulaca species, no significant differences were recorded between P. oleracea and P. grandiflora regarding salt-induced GB accumulation (115).
Soluble sugars can also act as physiological osmolytes in higher plants (116). According to Cram (117), in glycophytes soluble carbohydrates are the major compounds responsible for maintaining cellular osmotic balance under stress conditions, contributing up to 50% of the total osmotic potential. Soluble sugars have often been reported to accumulate in response to salinity or water deficit, even though these stresses may significantly decrease the net CO2 assimilation rate (118, 119). Several studies have focused on correlating changes in soluble sugar contents with the relative degree of stress tolerance. For example, soluble sugar contents increased significantly with increasing salinity in five sunflower lines differing in salt tolerance but reaching relatively higher levels in the salt-tolerant genotypes than the salt-sensitive ones (120). In contrast, this clear correlation could not be established in safflower, which showed significant differences in sugar contents between salt tolerant genotypes, while no differences were observed between some tolerant and sensitive lines (121).
Oxidative stress and activation of antioxidant systems
Many different stressful environmental conditions, including drought, high salinity, too low or too high temperatures, or heavy metals in the soil, induce, as a secondary effect, oxidative stress in plants due to the increase in the levels of ‘reactive oxygen species’ (ROS). ROS have multiple deleterious cellular effects, mediated by the oxidation of membrane lipids, amino acid residues in proteins and the bases in DNA (122, 123).
Malondialdehyde (MDA) is a product of lipid peroxidation, generated by oxidation of membrane lipids and considered as a reliable oxidative stress marker in plants. There are many publications reporting an increase in MDA contents in response to abiotic stresses in different plant species such as turfgrass (124), sesame (125), Inula sp. (21), bitter gourd (126) or Juncus sp. (127). In salt-treated P. oleracea plants, a slight (14%) increase in leaf MDA concentrations, as compared to the controls, was detected after 30 days of exposure to 140 mM NaCl, whereas no significant differences between stressed and non-stressed plants were observed with shorter treatments (18 days) or lower salt concentrations (70 mM NaCl) (95). On the other hand, no increase in MDA levels was detected under water deficit conditions (48). These data are in agreement with the notion that common purslane is relatively resistant to drought and salinity.
Since different environmental stresses cause secondary oxidative stress in plants, a general reaction to salt and water deficit is the activation of antioxidant compounds and enzymes. Among non-enzymatic antioxidants, the complex group of phenolic compounds and, mainly, the subgroup of flavonoids, include many secondary metabolites that are apparently highly relevant for these antioxidant responses.
Phenolic compounds play multiple functional roles in plants; some are structural components of the cell walls, others are involved in the regulation of growth and different developmental processes or participate in defence reactions against herbivores and pathogens. Furthermore, many phenolics are also involved in plant responses to abiotic stresses: UV radiation, high temperature, heavy metals, herbicides, salt stress or drought, among others (128). There is evidence that these responses are mediated by the antioxidant properties of many phenolic compounds, thus explaining the increase in total phenolics contents generally observed in plants under high salinity and water deficit conditions (129, 130).
Flavonoids, the most complex subclass of phenolic compounds, include more than 10,000 different molecules (131) and have long been reported to be involved in a wide range of plant-environment interactions (132, 133). Flavonols are the most ancient and widespread subgroup of flavonoids (134); it has been proposed that they played key functions during the evolution of early terrestrial plants, as antioxidant and regulatory molecules (135, 136). The biosynthesis of flavonoids is upregulated not only by UV-radiation but also in response to a wide range of other abiotic (and biotic) stresses, ranging from depletion of mineral nutrients to salinity, cold or drought stress (137, 138, 139). Several studies show that flavonoid contents increase in plants upon different abiotic stress treatment, and that accumulation of these compounds correlates with the intensity of the applied stress (e.g. 140).
A study carried out on 12 different purslane accessions, including 10 ornamentals and two common purslanes (35) at increasing salinity levels (0, 8, 16, 24 and 32 dS m-1) showed that salt treatments had significant impact on total phenolics and flavonoid contents, leading to concentration-dependent increases of up to 35% over the non-stressed controls.
Plants have developed a series of detoxification systems to maintain growth, development, metabolism and overall productivity under stress, avoiding or minimising the potential damage caused by ROS on cellular components (141, 142). Antioxidant enzymes play crucial roles as ROS scavengers in the mechanisms of defence against abiotic stress; superoxide dismutase (SOD), several peroxidases (POD), catalase (CAT) and glutathione reductase (GR) are amongst the most important antioxidant enzymatic systems, responsible for maintaining the appropriate redox equilibrium in the cell (143).
These enzymatic activities have been determined in leaves of salt-treated P. oleracea plants (102). In general, salt stress increased POD, CAT and GR specific activities, while no significant change in SOD activity was observed; however, under the strongest stress conditions tested – higher NaCl concentration and/or longer treatment time – some reduction of the activity with respect to the control was detected for all enzymes but GR, probably due to their inactivation. In an independent study, it was found that SOD and POD activities increased significantly in purslane plants upon drought or heat treatments, especially when both stresses were applied simultaneously (144).
A brief summary of some of the responses to salt treatments observed in three Portulaca species (P. oleracea, P. halimoides and P. grandiflora), regarding inhibition of seed germination and plant growth, and changes in the levels several physiological and biochemical stress markers (chlorophylls, proline, ion contents, MDA) is shown in Table 1. For comparison, similar responses are shown for tomato, a crop that is not amongst the cultivated species most sensitive to salt.
Inhibition of seed and plant growth, and changes in the levels of stress biomarkers in response to salt treatments at the indicated NaCl concentrations (mM), in three Portulaca species and in Solanum lycopersicum. Data for the Portulaca taxa are taken from references cited in the text; those for tomato from (145, 146, 147)
Seed germination inhibition / NaCl (mM)
Growth inhibition / NaCl (mM)
Decrease of chlorophyll content / NaCl (mM)
Increase of Pro content / NaCl (mM)
Increase of ion contents
Change in MDA levels / NaCl (mM)
Na+ / NaCl (mM)
Cl- / NaCl (mM)
50% / 100
37% / 400
30% / 400
196% / 400
1,811% / 400
1,686% / 400
- 17% / 400
33% / 100
19% / 400
14% / 400
466% / 400
539% / 400
373% / 400
- 6% / 400
14% / 100
12% / 400
24% / 400
263% / 400
245% / 400
141% / 400
+ 14% / 400
43% / 100
55% / 200
13% / 200
88% / 150
98% / 160
Although information on Portulaca species, regarding their responses to abiotic stress, is still limited – most studies on the genus have been focused on P. oleracea, common purslane – there are data indicating that some of these species are relatively resistant to drought and/or salinity. Comparative analyses of the responses to salt and water stress of closely related taxa, but with different degrees of stress resistance, represent a useful approach to investigate the mechanisms of tolerance to stress. Correlation of the activation of specific defence responses with the relative tolerance of the studied species – estimated from the relative inhibition of growth observed under controlled stress conditions and/or from the characteristics of the plants’ natural habitats – will allow distinguishing the responses that are relevant for tolerance from those which are not. We propose the Portulaca genus as a suitable model to carry out this kind of studies, which can provide complementary information to that obtained from other, more common model species, thus contributing to our knowledge on the general mechanisms of abiotic stress tolerance in plants.
Portulaca oleracea has been used since ancient times as a traditional Chinese medicinal plant and is a highly nutritious vegetable, very rich in antioxidant compounds and ω-3 and ω-6 fatty acids. On the other hand, several Portulaca species and cultivars are grown as ornamentals, mostly because of the beauty of their flowers. Due to their relative tolerance to drought and soil salinity – in comparison to our major crops – these species could be developed as ‘new’ crops for sustainable agriculture, to be cultivated in salinised farmland, in marginal lands or arid zones, unsuitable for standard crops. They could be grown without irrigation, or using low-quality, brackish water for irrigation, and thus will (modestly) contribute to food production, apart from other economically interesting uses as medicinal plants or ornamentals. Most important, they will not compete with conventional crops for limited resources such as fertile land and good-quality irrigation water.
Inhibition of seed and plant growth, and changes in the levels of stress biomarkers in response to salt treatments at the indicated NaCl concentrations (mM), in three Portulaca species and in Solanum lycopersicum. Data for the Portulaca taxa are taken from references cited in the text; those for tomato from (145, 146, 147)
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