The genus Portulaca as a suitable model to study the mechanisms of plant tolerance to drought and salinity
Article Category: Review
Published Online: Apr 25, 2018
Page range: 104 - 113
DOI: https://doi.org/10.2478/ebtj-2018-0014
Keywords
© 2018 Orsolya Borsai, Mohamad Al Hassan, Monica Boscaiu, Radu E. Sestras, Oscar Vicente, published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.
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
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:
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
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
The genus
The accumulated information on
In addition to their possible use for basic research, many
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
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.
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
In some ornamental plant species such as
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
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
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).
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
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
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).
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).
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 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
Among the many quaternary ammonium compounds (QACs) with a functional role as compatible osmolytes in plants subjected to abiotic stress,
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).
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.
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
A brief summary of some of the responses to salt treatments observed in three
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
| Species | 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