Genes, gene function, metabolic function and transgenic.
1. Introduction
Climate changes and water availability cause an important impact in agriculture, food disposal and consequently in human health. According to the U.S. Census Bureau, the total population of the World is now over 7,032 billion, and all growth projections for developed and undeveloped countries show that a total of 9 million of inhabitants will be reached before 2050. As a result, the demand for food and fuel will increase significantly. How agriculture will move on to guarantee continuous provision of food for all inhabitants of the planet?
As a consequence of the population growth the scenario has changed and an increase of urban areas has occurred in the last decades. From the 50th´s urban population increased from 4 to 11% in Africa, 33 to 52% in Asia, 9 to13% in Latin America, and decreased from 38 to 15% in Europe, from 15 to 6% in Northern America. Growth forecasts for 2050 are 54, 32.5 and 6.8% increase in Asia, Africa and Latin America respectively. Increasing urban areas make less cropland available for fuel and food production. Croplands are not expanding in the same rate as population in the last half a century and salinity and desertification have also contributed to the fact that less useful areas remain proper for agriculture. According to FAO about 12% of globe´s land surface is used for crop production and most of remaining world agricultural land are covered by forest and protect by environmental laws. Brazil, Bolivia, Argentina, Colombia, Sudan and Democratic Republic of the Congo retain 90% of accessible agricultural land [1].
The climate changes in agriculture and human life can be considered under different aspects: the biological effects on crop yields; the resulting impacts on outcomes including prices, production and consumption and also the impact on per capita calorie consumption and child malnutrition [2]. In other words their effects on agriculture will induce changes in production and prices, altering economic system, crop mix, production, food demand and consumption. Unfortunately those changes are already occurring and the projections on annual mean temperature for the next 20 to 30 years point to great economic losses due to decline in productivity for cereals like maize, wheat and rice as well. It is well known that most of our important crops will decrease yield with temperature above 30°C, as they growth faster in high temperature they have less time to accumulate carbohydrates, proteins and oil. Increasing temperature will perhaps make some areas available for agriculture, but will it be enough to replace the areas that will certainly be lost?
Recently, it was discussed the physical and economic consequences of climate changes considering temperature rising in Europe over four different factors such as agriculture, river floods, coastal systems and tourism [3]. Considering four different temperature increases from 2.5 to 5.1°C and five Europe regions (Southern, Central South, Central North, British Isle and Northern). Yield change (%) would affect Southern Europe (Portugal, Spain, Italy, Greece and Bulgaria) more than any other region with temperature increase. Northern Europe (Sweden, Finland, Estonia, Latvia, and Lithuania) instead would benefit from positive yield changes. River floods are natural disasters anywhere it happens, resulting in very large economic losses due to properties and agriculture damage. An increase on river flood is expected with global warming [4]. As a consequence of increasing temperature river floods would affect 250,000-400,000 additional people in Europe in the 2080s, specially Western Europe, British Isle and Central Europe regions. All the costal systems across Europe would suffer with people flooded. Tourism in Europe would be impacted as well. According to bed night’s percentage measures the effects will be a decrease in Southern Europe and an increase in all other areas such as Central and Northern Europe. But not only temperature would have importance to agriculture, fluctuation in seasonal precipitation is also extremely relevant and as well as increasing evaporation rates [3].
The effects of climate change on rainfed and irrigated crops for developing and developed countries were also discussed [2]. Percentage change in yield for irrigated and rainfed crops like maize, rice and wheat were analyzed using Decision Support System for Agrotechnology Transfer (DSSAT) crop-simulation model with and without CO2 fertilization in 2050 scenario. The observed effects on rainfed were attributed to changes in temperature and precipitation index, while for irrigated areas the effects were only related to temperature variation. In general, yields in developed countries were less affected than those in developing countries, where for most crops without CO2 fertilization the yield declines. The stress imposed by climate changes on agriculture will certainly intensify the disparities among regions.
Nevertheless, prices for major grain crops like rice, wheat, maize and soybean will increase up to 60 to 70 %, over the next few years, even without climate changes. Bearing in mind the predicted weather changes an additional of 32 to 37% for rice, 52 to 55% for maize, 94 to 111% for wheat and 11 to 14% for soybean can be expected [2].
2. Physiological aspects of water stress
It is well known that plant growth and development can be affected by abiotic agents such as salinity, high temperatures, radiation, flood and water deficit. Exacerbate action of those environmental conditions can led to great losses in productivity due to crop stress. When subjected to water deficit plants go through a cascade of metabolic alterations started with reduction in photosynthetic pigments concentration. Physiological mechanisms of plant response to water stress are summarized in Figure 1. Facing a water deficit situation plant responses can be species/genotype specific, under rehydration after a mild water deficit almost every plant can return to normal growth, but if the stress intensity was moderated or severe some will not recover at all.
2.1. Photosynthetic responses
One of the significant alterations responsible for reduction in crop productivity is low photosynthetic ability. The water stress may cause decrease in CO2 assimilation in the leaves, the amount of ATP and the level of ribulose bisphosphate [5-8]. Stomatal closure limiting diffusion through stomata and mesophyll is one of the first events in plants response under water deficit situation with consequent increase of the Rubisco enzyme, responsible for CO2 fixation, e in order to overcome the low conductance [9-13]. However, some species (
The electron transport in thylakoids and the use of trioses phosphates are also reduced in the stress biochemical control therefore, the net photosynthetic rate tends to be lower. It has been proved that in plants subjected to water stress the photochemical efficiency of photosystem II (PSII) and quantum generation is reduced [6, 15-17]. Alterations in the level of photosynthetic pigment were also detected in water stressed plants; showing reduced or even no pigmentation. Both chlorophyll
2.2. Sugar and Reactive Oxygen Species (ROS) protection
Changes in the content of carbohydrates such as sucrose and raffinose, together with the unbalanced of plant hormones function as a signal that plant response to stress should be initiated [21]. Raffinose has been correlated to a plant tolerance to desiccation, possibly involved in the protection against ROS that are responsible for loss of membrane integrity and cellular death [22, 23]. Moreover, induction of sugar accumulation, i. e, sucrose, fructose, maltose and inositol is relevant for the osmoprotection process and has been associated to plant tolerance to water stress [22].
2.3. Hormonal regulation
It is well known that hormones play a special role in plant reaction to water stress conditions. The abscisic acid (ABA) is the main hormone correlated to water stress. Plants exposed to drought substantially increase the level of ABA in shoots and roots [24-26], and the ABA positive regulators induce plant response as G protein activation, ROS production, increase in cytosolic Ca2+, protein phosphorylation and dephosphorylation events and immediate stomatal closure [27, 28]. Actually the balance of positive and negative ABA regulators actions command the resistance or sensitivity to water scarcity situation. However, the regulation of stomatal closure occurs not only due the action of ABA, but by the integrated hormonal balance between ABA, Auxin (Ax) and Cytokinin (Ck) [21]. Along with Ck, ABA plays a role in controlling senescence [29, 30]. The high concentration of ABA possibly prevents excessive accumulation of ethylene (ET), thus indirectly maintaining the growth of roots and shoots [31, 32].
ABA seems to be also involved in remobilize carbon to accelerate grains filling in rice and wheat [29, 30, 33]. The ABA increased level also induce ROS production and in order to prevent the oxidative stress, antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR) are immediately activated [34, 35]. The importance of regulating ABA contents as a stress signaling was also observed in rice leaves when, after a water stress period, plants were rehydrated; decreasing ABA content occurred a reduction on ROS, CAT and SOD [36].
Wheat and maize plants submitted to a moderate water deficit exhibit an increase in ET concentration [27, 37] that would be partly responsible for decreasing growth rates. In contrast for beans, cotton and miniature rose it has been shown that the rate of ethylene production is not affected during progressive drought [27]. ET is also involved in ROS production and antioxidant enzymes synthesis [23].
Cytokinins are generally involved in root and shoot development, but it has been shown an increased cytokinin concentration in leaves, from roots translocation, in plants submitted to water deficit [24, 29, 38]. Bentgrass transgenic plants expressing the enzyme adenine isopentenyl phosphotransferase for Ck synthesis ligated to a senescence-activated promoter (
The gibberellins (GA), Ax and brassinosteroids (BR) do not seem to have a direct involvement with water stress, however, the accumulation of GA in some dicots has been reported and also the BR along with ABA regulate the development and function of stomata [27]. In contrast in monocots such as maize, there is a decrease in the levels of GA in leaves [25, 27]. The Ax content in plants seems to decrease in roots and leaves under stress, but the importance of auxin in water stress response remains inconclusive [24, 25, 27, 40].
The JA instead seems to play a role in the biosynthesis of ABA in water stress. In citrus plants, for example, drought causes an increase of JA concentration in roots with subsequent increase in the concentration of ABA. One can conclude that JA is possibly the precursor in the signal transduction cascade in case of drought stress, providing increased levels of ABA which, in turn, induce later responses [41].
2.4. Morphological and anatomical modifications
All the known morphological changes that occur in plants under water deficit can be associated to hormone actions. Plants develop more roots in order to access more water, increasing the ratio root/shoot, reduce leaf number and leaf area to lower transpiration rates what leads, unfortunately, to a decrease in photosynthetic rates and biomass production [20, 26, 42] and develop the epinasty/hyponasty effects [43]. The increase of apoplastic pH in the elongation of leaf area could be the responsible for the foliar reduction [44]. The number of lateral seedling roots [17] as well as the stem length can also be affected [20].
The deformation of tracheids in the xylem due to the decrease in osmotic potential [45], the reduction of mitotic activity of mesophyll cells [46], the increase of starch granules in chloroplasts [17, 47] and trichome production, as well as the decrease in cell size and number of stomata per leaf, the thickness of palisade parenchyma are anatomical changes resulting from water stress [7].
2.5. C3 and C4 responses
The response to water deficit may vary from species C3 i.e.
3. Plant biochemical mechanisms to face water stress
Drought stress and its detrimental effects on plants in both natural and agricultural environments are receiving increasing attention in order to discover alternative solutions to enhance plant vigor and high tolerance; to maintaining crop yields under adverse or extreme climate conditions overcoming economic losses.
3.1. Drought effects: Two sides of the coin
Contrasting with the negative environmental aspects caused by water stress, the adverse effects on agriculture affecting plant growth and crop productivity can be mitigated by metabolic changes which invigorate the plant biosynthesis of natural products with widespread use by the pharmaceutical, energy and food industries.
3.2. Protective role of secondary metabolites in the plant response and tolerance to water stress
Plant defense response and tolerance to drought and salinity involves the perception of signal stress by receptors at the membrane level followed by signaling transduction in the cell, inducting a multiplicity of biochemical mechanisms involved in the protective role of secondary metabolites. Water stress reduces plant growth, so the carbon fixed during photosynthesis could be used to form secondary metabolites as established in several studies. Restrictions of water supply to plant bring about the production of a complex variety of secondary metabolites which level can be modulated through biochemical and genetic manipulation. Water stress induce the accumulation of reactive oxygen species (ROS), resulting in oxidative stress in the plant cells. Thus, antioxidant secondary metabolites, able to scavenger and detoxify ROS by the availability of –OH, –NH2, and –SH groupings, as well as aromatic nuclei and unsaturated aliphatic chains, can play important role in protecting plant species against oxidative stress caused by water deficit. It is well known that terpenoids possess antioxidative properties. Volatile isoprenoids accumulated in
Similarly, drought stress markedly enhanced the total concentrations of monoterpenes and resin acids in the main stem wood of Scots Pine and Norway Spruce Seedlings [52]. Results of investigations conducted on the effect of water deficit imposed to potted
Polyamines (PAs) are low molecular weight polycations that have been implicated in a wide range of biological processes in plant growth and development, including environmental stress. The major PAs occurring in plant cells are the diamine putrescine (PUT), triamine spermidine (SPD) and tetramine spermine (SPM). Among the important roles attributed to those plant polyamines are: membrane stabilization and free radicals scavenger action. Polyamine mediated regulation of the water deficit stress response of soybean seedlings was investigated using exogenous applications of polyamines and their biosynthetic inhibitors. The exogenous supply of PUT, SPD and SPM to soybean seedlings resulted in reduction of the stress injury in roots which showed increased length and water content over non-treated stressed controls. Moreover, up to 40% increase of shoot growth was observed in seedlings supplemented PUT, SPD and SPM in comparison with controls. In contrast, in the presence of polyamines inhibitors the stress injury intensified, growth was severely inhibited, and water content of roots was significantly decreased. Overall results suggested that polyamines are potentially useful to overcome the detrimental effects of drought [56].
Water stress is also known to increase the secondary metabolite production in a variety of medicinal plants. Increase of hypericin and betulinic acid levels upon
The main physiological and biochemical known mechanisms triggered by water stressed plants are illustrated in Figure 2.
3.3. Sustainable exploitation of cultured drought-resistant plants
3.3.1. Oilseed crops: Biofuel production
Recently, considerable attention has been given to biofuels as an alternative to fossil fuels and the challenge is to find oil bearing plants that produce non-edible oils as the feedstock for biodiesel production. Jatropha (
Besides the oil production, Jatropha species are source of jatrophone and jatropholone, macrocyclic diterpenoids, secondary metabolites that display varied pharmacological activities [64, 65].
3.3.2. Quinoa
Based on the high quality of the oil, and on the fact that some varieties show oil concentrations of up to 9.5%, quinoa could be considered as a potentially valuable new oil crop [66].
Quinoa is currently grown for its grain in the South American countries of Peru, Bolivia, Ecuador, Argentina, Chile and Colombia. Quinoa populations display a high degree of genetic distancing, and variable tolerance to salinity. Cultivars of quinoa can be adapted to growth from sea level to an altitude of 4,000 m, from 40°S to 2°N latitude, and from the cold highland climate to subtropical conditions, i.e. quinoa plant is cold and drought tolerant. The plasticity of quinoa biochemical response to a wide range of environmental conditions makes it possible to select, adapt, and breed cultivars [67]. Studies have shown that quinoa is a very good source of antioxidants and it can be a substitute for common cereals [68, 69]. The content of total phenolic compounds and the correlated radical scavenging activity of quinoa varieties have been analyzed. There were significant differences between the varieties and the content of total polyphenols [70]. Moreover, the saponins obtained as a by-product in the processing of quinoa grain can be utilized by the cosmetics and pharmaceutical industries.
3.3.3. Cotton
Polyphenols and carotenoids compounds with reactive oxygen species (ROS)-scavenging ability biosynthesized in drought tolerance Cotton genotypes were correlated to the drought tolerance of this important crop [71].
4. What have been done?
In order to cope with the major environmental problems that affect crops such as drought, salinity, cold and heat shock, genetic engineering and breeding techniques have become fundamental tools, as they have been for decades regarding biotic stresses, pests and diseases resistance. It is well known that very often an adversity results in another unfavorable condition for the development of a crop, for example high temperatures provoke water deficit reducing soil moisture resulting in salinity problems and desertification.
Biotechnological approaches focused on secondary metabolism pathways induction or repression at the transcriptional level are now being conducted to significantly improve plant tolerance to water deficit, extreme temperatures and ion imbalance.
4.1. Breeding crops
Considering all climate changes that the planet is going through it is vital the development of crops with high efficiency in water recovery and consequently tolerance to water stress, higher temperatures, salinity and desertification. Through conventional breeding methods and selection based in progeny tests it was possible to obtain stress resistant varieties [72], but it has to be considered that instability of genotypes in different environments may affect the cultivars agronomic performance.
Researchers consider that genetic improvement for stress tolerance can be achieved in two ways: directly, through the evaluation of primary features in the target environment, i.e. as productivity (empirical breeding); or indirectly (analytical breeding), through secondary characteristics related to stress adaptation observed in crops growing in limiting environment. Over the past 50 years genetic improvement have been carried out empirically, however, this type of traditional selection has not presented significant efficiency in terms of productivity, requiring the support of indirect selection [73]. The selection of genotypes with promising agronomic characteristics and tolerant to abiotic stresses demands successive seasonal evaluations of field cultures conducted in different locations, and under influence of stress agents, requesting arduous and extensive work.
Furthermore, it is important to highlight that the low heritability of complex traits have limited the development of tolerant cultivars due to significant G x E interaction and the QTL-by-environment interaction (QTL x E), and the trivial understanding of the physiological parameters related to the genetic yield potential in dry environments [73]. Biotechnology plays an important role for managing abiotic stress, allowing the exploitation of large germplasm collections with no need of experimental procedures under unfavorable environmental conditions [74].
4.2. Which genes are involved in plant responses?
Lately, much has been done to identify and isolate drought-induced genes in order to investigate the role those gene products play and the paths for induction of those genes [75, 76]. Gene expression in response to water stress can enhance the plant's ability to respond appropriately to the deleterious effect of drought, stimulating its aptitude to survive desertification [77]. In general, the stress-induced gene products can be classified in two ways: genes that directly protect the plant against stress and genes that regulate the expression of other genes [78, 79].
Through analysis of transcripts it was observed that the genes exhibit distinct expression profiles, being that stress-induced gene decrease mRNA levels when the plants are freed from stress conditions. However, the expression patterns of those genes are complex, with some genes responding very quickly to water deficit while others answer very slowly after the accumulation of ABA (abscisic acid) [80].
The differential gene expression analysis of two sugar cane cultivars, tolerant and sensitive to drought, showed that the number of genes expressed in the sensitive cultivar increased with the severity of the drought. Comparing the gene expression profiles 91 common genes were found among both cultivars, most of them drought-induced genes that are still unknown. Moreover, genes of important pathways related to drought stress were suppressed in sensitive plants. It was evidenced that plants submitted to the same water conditions responded differently to stress. Morphological changes occurred, but some genes may represent the difference between tolerance and sensitivity, as the S-adenosylmethionein decarboxylase (SAMDC) and induced cinnamoyl-CoA reductase (CCR) in resistant cultivars or lipid transfer protein that have been repressed, as well as other genes [81].
The expression of some sugarcane water-stress related genes and their association with sucrose accumulation was also investigated and a group of stress-induced genes that could be associated with sucrose accumulation were identified, showing that genes associated with the synthesis of proline are associated with stress and sucrose accumulation. Stress-related transcription factors and sugar transporter also play a role in sucrose accumulation [82].
For better understanding the processes and genes involved in water deficit tolerance it is required a full knowledge of the molecular principles that regulate plant responses to stress conditions. Thus, studies with model plants stand for and will continue to represent a relevant strategy for the elucidation of signaling and transcription processes using molecular genetics techniques [79, 83].
Genes isolated from several cultured species have been the focus of researches using gene expression in model plants with the objective of elucidating their direct effect on abiotic stress tolerance. Genetic transformation of plants in order to increase resistance is often based on the manipulation of genes to preserve the function and structure of cellular components [84]. In this context, the genetic engineering techniques for pest and herbicide resistance differ from the procedures for abiotic stress tolerance, since the first is a monogenic trait, more easily manipulated. In contrast, tolerance to environmental stresses may associate more than one of the genes involved in different signaling pathways.
The expression of
4.2.1. Signaling genes
Many of these genes encode proteins involved in signaling pathways, including protein kinases mitogen-activated (MAPKs), histidine kinases, protein kinase Ca2+ dependent (CDPKs), family SOS3 sensors Ca2+ as well as transcription factors [86, 87].
The association of three genes
Transgenic sugarcane plants overexpressing heterologous
In the same way, after detecting the up-regulated expression of two maize putatives PIS in response to drought, one of them, the
Remarkable results were observed with the
4.2.2. Transcriptional factors genes
Transcription factors (TFs) have been extensively studied and have shown to be important in the regulation of stress tolerance in plants. The TFs are proteins that play a role in physiological and biological processes such as growth, development and responses to environmental stresses acting as key regulators involved in early stages of expression, gene regulation, signal transduction [92].
The TF
In
The
Additionally, the soybean
It is evident the relevance of studying and elucidating the role of genes putatively related to water stress tolerance. In this context the molecular biology and the plant biotechnology comprise an efficient and helpful tool to achieve cultivars tolerant to environmental stresses that are gradually responsible for production losses all over the world.
4.2.3. Genetic modified crops using genetic engineering
Currently private companies have invested heavily in biotechnological programs for liberation of cultivars tolerant to insects, herbicides and drought. GMOs have been commercially cultivated since the 90’s, tolerance to herbicides and insects are the main features of GM crops, including maize, soybean, cotton, canola, rice, tomato, etc. Some crops that has been transformed using genetic engineering technology to receive genes which metabolic function are related to water stress response are listed in Table 1. Genes involved in osmoprotection, ABA responsive elements and Transcription factors have been used to generate more resistant plants. Soybean, maize, rice, cotton and tomato are the most denoted transgenic crops.
|
Arginine decarboxylase | Reduced chlorophyll loss under drought stress |
|
[96] |
|
Polyamine synthesis | Drought resistance |
|
[97] |
|
Betaine aldehyde dehydrogenase | Maintenance of osmotic potential |
|
[98] |
|
Betaine aldehyde dehydrogenase | Salinity tolerance |
|
[99] |
|
Choline dehydrogenase (glycinebetaine synthesis) | Drought resistance at seedling stage and high yield after drought |
|
[100] |
|
Choline oxidase (glycine betaine synthesis) | Tolerance to stress induced photo inhibition |
|
[101] |
|
Choline oxidase (glycine betaine synthesis) | Increased tolerance to salinity and cold |
|
[102] |
|
Choline oxidase (glycine betaine synthesis) | Recovery from a week long salt stress |
|
[103] |
|
Choline oxidase (glycine betaine synthesis) | Salt and stress tolerance |
|
[104] |
|
Chloroplastic glutamine synthetase | Increased salinity resistance and chilling tolerance |
|
[105] |
|
Mannitol-1-phosphate dehydrogenase & glucitol-6-phosphate dehydrogenase | High salt tolerance due to mannitol and glucitol accumulation |
|
[106] |
|
Mannitol-1-phosphate dehydrogenase (mannitol synthesis) |
Drought and salinity tolerance of calli and plants |
|
[107] |
|
Pyrroline carboxylate synthase (proline synthesis) | Osmotic adjustment and drought Resistance |
|
[108] |
|
Pyrroline carboxylate synthase (proline synthesis) | Salinity tolerance |
|
[109] |
|
Pyrroline carboxylate synthase (proline synthesis) | Increased biomass production under drought and salinity stress |
|
[110] |
|
Pyrroline carboxylate synthase (proline synthesis) | Reduced oxidative stress under osmotic stress |
|
[111] |
|
Pyrroline carboxylate synthase (proline synthesis) | Drought resistance, high RWC, high proline |
|
[112] |
|
Pyrroline carboxylate synthase (proline synthesis) | Drought resistance via antioxidant role of proline |
|
[89] |
|
Fructan accumulation | Reduced proline accumulation at low water status |
|
[113] |
|
Trehalose synthesis | Drought, salt and cold tolerance |
|
[114] |
|
Trehalose synthesis | Drought, salt and oxidative stress Tolerance |
|
[115] |
|
Group 3 LEA protein gene | Delayed wilting under drought stress |
|
[116] |
|
Group 3 LEA protein gene | Salinity tolerance in yield/plant |
|
[117] |
|
Group 3 LEA protein gene | Dehydration avoidance and cell membrane Stability |
|
[118] |
|
Group 3 LEA protein gene | Drought and salinity tolerance |
|
[119] |
|
Group 3 LEA protein gene | Increased biomass and WUE under stress |
|
[120] |
|
Group 3 LEA protein gene | Improved plant water status and yield under field drought conditions |
|
[121] |
|
Lea protein | Drought resistance for yield in the field |
|
[122] |
|
Aquaporin overexpression | Maintenance of leaf water potential and transpiration under 10 h PEG stress |
|
[123] |
|
Vacuolar Na+/H+ antiporter | Salt tolerance in photosynthesis and yield |
|
[124] |
|
Vacuolar Na+/H+ antiporter | Salt tolerance, growth, fruit yield |
|
[125] |
|
Vacuolar Na+/H+ antiporter | Salt tolerance for grain yield in the field |
|
[126] |
|
Potassium transporter | Salt tolerance in growth and improved K+/Na+ ratio |
|
[127] |
|
Transcription factor | Drought resistance |
|
[128] |
|
Arginine decarboxylase overexpression | Polyamine accumulation and salt resistance in biomass accumulation |
|
[129] |
|
Transcription factor | Drought, salt and cold tolerance with reduced growth under non-stress |
|
[130] |
|
Transcription factor | Delayed wilting under drought stress |
|
[131] |
|
ABA overproduction | High water-use efficiency, low transpiration and greater root hydraulic conductance |
|
[132] |
|
Increased ABA sensitivity | Hypersensitive to osmotic stress and exogenous ABA |
|
[133] |
|
Ethylene synthesis | Non-functional mutant expressed drought induced Senescence |
|
[134] |
|
putative papain-like cysteine protease | related to protein degradation for nutrient remobilization during leaf senescence |
|
[85] |
|
ABA signaling (ABA responsive element) | ABRE protein phosphorylation |
|
[88] |
|
Phosphatidylinositol synthesis | Membrane protection |
|
[90] |
|
Vacuolar pyrophosphatase gene | Proton pump activity |
|
[91] |
|
Transcription factor (R2R3 MYB family member) | ABA responses, salinity and drought conditions tolerance |
|
[83] |
|
Protein ERF (ethylene-responsive factor) | ABA responses , accumulation of proline and soluble sugars content, induction of genes related to responses to stress and photosynthesis |
|
[93] |
|
Sugarcane ERF transcription factors | Drought, osmotic stress, salt stress injuries and treatment with ABA |
|
[94] |
|
Soybean transcription factor family | Responses against biotic and abiotic stresses |
|
[95] |
5. Concluding remarks
The global warming is a reality that we have to face and in order to provide food to the growing population some actions have to be taken by government and researchers. The development of new cultivars more resistant to the environmental conditions, for every crop, must be a priority, in order to guarantee food demand security. To avoid yield reductions from floods, droughts and rising temperatures agribusiness will have to be reconsidered, investments have to be done, researchers will have to focus on ways to improve food quality, nutritional composition and increase yield using less land for farming. Crops will have to grow under a different scenario including less water and high temperature.
As it was discussed in this chapter changes in climate conditions will require several plant adaptations in order to minimize decreases in crop yield and to maintain food accessibility. Genetic breeding has been used over the last decades to improve yield and food quality. But how much can we still get from traditional plant breeding programs regarding to improve plants to face water scarcity? It is time to adopt new technologies as genetic engineering to help breeders in generating more adapted plants to survive water stress. For several years researchers have been spending time to understand how plants adapt to different situations, understanding the physiological parameters and their role in plants response to water stress specially hormones and transcriptional factors can help the development of new cultivars more resistant to stress conditions. All this knowledge allied to molecular biology techniques and genetic engineering can promote the development of transgenic plants with higher product quality, better storage conditions, easer processing, more efficient and more resistant to extreme conditions.
Nowadays, transgenic crops are cultivated all over the world, but there are some remains questions: How much are farmers dependent on biotechnology companies? Which economic and cultural losses transgenic cultures will bring about? These subjects are still extensively debated and researchers do not know for sure what is ahead. In the specific case of drought tolerance, much has been discussed about genetic engineering and experts consider the biotechnology relevant in developing higher genotypes.
Acknowledgments
The authors are grateful to: Fundação do Amparo à Pesquisa do Estado de São Paulo (FAPESP); Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq) and Universidade de Ribeirão Preto (UNAERP) for the constant financial support and also to Ms Rosane Castro França for her precious help during this chapter organization.
References
- 1.
FAO-Food and Agriculture Organization of the United Nations. Crop Prospects and Food Situation 2012. Rome, Italy. http://www.fao.org/docrep/015/i2490e/i2490e00.htm (accessed 6 July 2012). - 2.
Nelson GC., Rosegrant MW., Koo J, Robertson R, Sulser T, Zhu T, Ringler C, Msangi S, Palazzo A, Batka M, Magalhaes M, Valmonte-Santos R, Ewing M, LeeNelson DGC. Climate change: Impact on agriculture and costs of adaptation. In: Nelson GC., Rosegrant MW., Koo J, Robertson R, Sulser T, Zhu T, Ringler C, Msangi S, Palazzo A, Batka M, Magalhaes M, Valmonte-Santos R, Ewing M, LeeNelson DGC. Washington: International Food Policy Research Institute; 2009. 30p. - 3.
Ciscar JC, Iglesias A, Feyen L, Szabo L, Van Regemorter D, Amelung B, Nicholls R, Watkiss P, Christensen OB, Dankers R, Garrote L, Goodess C M, Hunt A, Moreno A, Richards J, Soria A. Physical and economic consequences of climate change in Europe. Proceedings of the National Academy of Sciences of the United States of America 2011;108(7)2378-2683. - 4.
Frei C, Scholl R, Fukutome S, Schmidli J, Vidale PL. Future change of precipitation extremes in Europe: Intercomparison of scenarios from regional climate models. Journal of Geophysical Research-Atmospheres 2006;111(D6)1-22. - 5.
Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW. Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 1999;401(6756)914-917. - 6.
Ribas-Carbo M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J. Effects of water stress on respiration in soybean leaves. Plant Physiology 2005;139(1)466-473. - 7.
Guerfel M, Baccouri O, Boujnah D, Chaibi W, Zarrouk M. Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive ( Olea europaea L.) cultivars. Scientia Horticulturae 2009;119(3)257-263. - 8.
Silva EN, Ribeiro RV, Ferreira-Silva SL, Viegas RA, Silveira JAG. Comparative effects of salinity and water stress on photosynthesis, water relations and growth of Jatropha curcas plants. Journal of Arid Environments 2010;74(10)1130-1137. - 9.
Sharkey TD, Seemann JR. Mild water-stress effects on carbon-reduction-cycle intermediates, ribulose bisphosphate carboxylase activity, and spatial homogeneity of photosynthesis in intact leaves. Plant Physiology 1989;89(4)1060-1065. - 10.
Vassey TL, Sharkey TD. Mild water-stress of Phaseolus vulgaris plants leads to reduced starch synthesis and extractable sucrose phosphate synthase activity. Plant Physiology 1989;89(4)1066-1070. - 11.
Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 2009;103(4)551-560. - 12.
Flexas J, Baron M, Bota J, Ducruet J-M, Galle A, Galmes J, Jimenez M, Pou A, Ribas-Carbo M, Sajnani C, Tomas M, Medrano H. Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri×V. rupestris). Journal of Experimental Botany 2009;60(8)2361-2377. - 13.
Yu J, Chen L, Xu M, Huang B. Effects of elevated CO2 on physiological responses of tall fescue to elevated temperature, drought stress, and the combined stresses. Crop Science 2012;52(4)1848-1858. - 14.
Galmes J, Ribas-Carbo M, Medrano H, Flexas J. Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress. Journal of Experimental Botany 2011;62(2)653-665. - 15.
Carmo-Silva AE, Gore MA, Andrade-Sanchez P, French AN, Hunsaker DJ, Salvucci ME. Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environmental and Experimental Botany 2012;83(1)1-11. - 16.
Rivero RM, Shulaev V, Blumwald E. Cytokinin-Dependent Photorespiration and the Protection of Photosynthesis during Water Deficit. Plant Physiology 2009;150(3)1530-1540. - 17.
Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo Y. Melatonin Promotes Water‐Stress Tolerance, Lateral Root Formation, and Seed Germination in Cucumber ( Cucumis sativus L.). Journal of Pineal Research 2012;1-9. http://onlinelibrary.wiley.com/doi/10.1111/j.1600-079X.2012.01015.x/pdf (accessed 16 July 2012). - 18.
Sanchez-Rodriguez E, del Mar Rubio-Wilhelmi M, Blasco B, Leyva R, Romero L, Manuel Ruiz J. Antioxidant response resides in the shoot in reciprocal grafts of drought-tolerant and drought-sensitive cultivars in tomato under water stress. Plant Science 2012;188-189(1)89-96. - 19.
Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R. Drought stress in plants: a review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology 2009;11(1)100-105. - 20.
Sangtarash MH, Qaderi MM, Chinnappa CC, Reid DM. Differential sensitivity of canola ( Brassica napus ) seedlings to ultraviolet-B radiation, water stress and abscisic acid. Environmental and Experimental Botany 2009;66(2)212-219. - 21.
Pinheiro C, Antonio C, Ortuno MF, Dobrev PI, Hartung W, Thomas-Oates J, Ricardo CP, Vanková R, Chaves M, Wilson JC. Initial water deficit effects on Lupinus albus photosynthetic performance, carbon metabolism, and hormonal balance: metabolic reorganization prior to early stress responses. Journal of Experimental Botany 2011;62(14)4965-4974. - 22.
Foito A, Byrne SL, Shepherd T, Stewart D, Barth S. Transcriptional and metabolic profiles of Lolium perenne L. genotypes in response to a PEG-induced water stress. Plant Biotechnology Journal 2009;7(8)719-732. - 23.
Smith DO. Abscisic acid: interactions with ethylene and reactive oxygen species in the regulation of root growth under water deficit. Msc thesis. University of Missouri; 2011. - 24.
Nan R, Carman JG, Salisbury FB. Water stress, CO2 and photoperiod influence hormone levels in wheat. Journal of Plant Physiology 2002;159(3)307-312. - 25.
Wang C, Yang A, Yin H, Zhang J. Influence of water stress on endogenous hormone contents and cell damage of maize seedlings. Journal of Integrative Plant Biology 2008;50(4)427-434. - 26.
Leach KA, Hejlek LG, Hearne LB, Nguyen HT, Sharp RE, Davis GL. Primary root elongation rate and abscisic acid levels of maize in response to water stress. Crop Science 2011;51(1)157-172. - 27.
Acharya B, Assmann S. Hormone interactions in stomatal function. Plant Molecular Biology 2009; 69(4)451-62. - 28.
Zhang K, Xia X, Zhang Y, Gan S-S. An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis . Plant Journal 2012;69(4)667-678. - 29.
Yang JC, Zhang JH, Wang ZQ, Zhu QS, Liu LJ. Abscisic acid and cytokinins in the root exudates and leaves and their relationship to senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling. Planta 2002;215(4)645-652. - 30.
Yang JC, Zhang JH, Wang ZQ, Zhu QS, Liu LJ. Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell and Environment 2003;26(10)1621-1631. - 31.
Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE. Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiology 2000;122(3)967-976. - 32.
Sharp RE. Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell and Environment 2002;25(2)211-222. - 33.
Yang JC, Zhang JH, Wang ZQ, Zhu QS, Wang W. Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiology 2001;127(1)315-323. - 34.
Jiang MY, Zhang JH. Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 2002;215(6)1022-1030. - 35.
Jiang MY, Zhang JH. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany 2002;53(379)2401-2410. - 36.
Ye N, Zhu G, Liu Y, Li Y, Zhang J. ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant and Cell Physiology 2011;52(4)689-698. - 37.
Apelbaum A, Yang SF. Biosynthesis of stress ethylene induced by water deficit. Plant Physiology 1981;68(3)594-596. - 38.
Vaadia Y. Plant hormones and water stress. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 1976;273(927)513-522. - 39.
Merewitz EB, Gianfagna T, Huang B. Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis inAgrostis stolonifera . Journal of Experimental Botany 2011;62(1)383-395. - 40.
Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inzé D, Van Breusegem F. Perturbation of indole-3-butyric acid homeostasis by the UDP-Glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 2010;22(8)2660-2679. - 41.
De Ollas C, Hernando B, Arbona V, Gómez-Cadenas A. Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiologia Plantarum 2012;1-11. http://onlinelibrary.wiley.com/doi/10.1111/j.1399-3054.2012.01659.x/pdf (accessed 3 August 2012). - 42.
Maes WH, Achten WMJ, Reubens B, Raes D, Samson R, Muys B. Plant-water relationships and growth strategies of Jatropha curcas L. seedlings under different levels of drought stress. Journal of Arid Environments 2009;73(10)877-884. - 43.
O’Toole J, Cruz RT. Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiology 1980;65(3)428-432. - 44.
Ehlert C, Plassard C, Cookson SJ, Tardieu F, Simonneau T. Do pH changes in the leaf apoplast contribute to rapid inhibition of leaf elongation rate by water stress? Comparison of stress responses induced by polyethylene glycol and down-regulation of root hydraulic conductivity. Plant Cell and Environment 2011;34(8)1258-1266. - 45.
Brodribb TJ, Holbrook NM. Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology 2005;137(3)1139-1146. - 46.
Schuppler U, He PH, John PCL, Munns R. Effect of water stress on cell division and cell-division-cycle 2-like cell-cycle kinase activity in wheat leaves. Plant Physiology 1998;117(2)667-678. - 47.
Ackerson RC, Hebert RR. Osmoregulation in cotton in response to water stress: I. Alterations in photosynthesis, leaf conductance, translocation, and ultrastructure. Plant Physiology 1981;67(3): 484-488. - 48.
Nayyar H, Gupta D. Differential sensitivity of C3 and C4 plants to water deficit stress: Association with oxidative stress and antioxidants. Environmental and Experimental Botany 2006;58(1-3)106-113. - 49.
Ghannoum O. C4 photosynthesis and water stress. Annals of Botany 2009;103(1)635-644. - 50.
Alfonso SU, Brüggemann W. Photosynthetic responses of a C3 and three C4 species of the genus Panicum (s.l.) with different metabolic subtypes to drought stress. Photosynthesis Research 2012;1-17. http://www.springerlink.com/content/202130j47376816n/fulltext.pdf (accessed 3 August 2012). - 51.
Chen JW, Bai KD, Cao KF. Inhibition of monoterpene biosynthesis accelerates oxidative stress and leads to enhancement of antioxidant defenses in leaves of rubber tree ( Hevea brasiliensis ). Acta Physiologiae Plantarum 2009;31(1)95-101. - 52.
Turtola S, Manninen AM, Rikala R, Kainulainen P. Drought stress alters the concentration of wood terpenoids in Scots pine and Norway spruce seedlings. Journal of Chemical Ecology 2003;29(9)1981-1995. - 53.
Chen Y, Guo Q, Liu L, Liao L, Zhu Z. Influence of fertilization and drought stress on the growth and production of secondary metabolites in Prunella vulgaris L. Journal of Medicinal Plants Research 2011;5(9)1749-1755. - 54.
Hura T, Hura K, Grzesiak S. Possible contribution of cell-wall-bound ferulic acid in drought resistance and recovery in triticale seedlings. Journal of Plant Physiology 2009;166(16)1720-1733. - 55.
Azhar N, Hussain B, Ashraf MY, Abbasi KY. Water stress mediated changes in growth, physiology and. secondary metabolites of desi ajwain ( Trachyspermum ammi L.). Pakistan Journal of Botany 2011;43(SI)15-19. - 56.
Amooaghaie R. Role of polyamines in the tolerance of soybean to water deficit stress. World Academy of Science, Engineering and Technology 2011;(56)498-502. - 57.
Nacif de Abreu I, Mazzafera P. Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense Choisy. Plant Physiology and Biochemistry 2005;43(3)241-48. - 58.
Velloso MAL, Abreu IN, Mazzafera P. Indução de metabólitos secundários em plântulas de Hypericum brasiliense Choisy crescendoin vitro . Acta Amazonica 2009;39(2)267-72. - 59.
Marchese JA, Ferreira JFS, Rehder VLG, Rodrigues O. Water deficit effect on the accumulation of biomass and artemisinin in annual worm wood ( Artemisia annua L., Asteraceae). Brazilian Journal of Plant Physiology 2010;22(1)1-9. - 60.
Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R. Induction of drought stress tolerance by ketoconazole in Catharanthus roseus is mediated by enhanced antioxidant potentials and secondary metabolite accumulation. Colloids and Surfaces B-Biointerfaces 2007;60(2)201-206. - 61.
Bosswell MJ. Plant Oils: Wealth, health, energy and environment. In: Proceedings International Conference of Renewable Energy Technology for Rural Development; 2003. - 62.
Hanna M, Isom L, Campbell J. Biodiesel: current perspectives and future. Journal of Scientific and Industrial Research 2005;64(11)854-857. - 63.
Pousa GPAG, Santos ALF, Suarez PAZ. History and policy of biodiesel in Brazil. Energy Policy 2007;35(11)5393-5398. - 64.
Martini LH, Jung F, Soares FA, Rotta LN, Vendite DA, dos Santos Frizzo ME, Yunes RA, Calixto JB, Wofchuk S, Souza DO. Naturally occurring compounds affect glutamatergic neurotransmission in rat brain. Neurochemical Research 2007;32(11)1950-1956. - 65.
Theoduloz C, Rodriguez JA, Pertino M, Schmeda-Hirschmann G. Antiproliferative activity of the diterpenes jatrophone and jatropholone and their derivatives. Planta Medica 2009;75(14)1520-1522. - 66.
Koziol M. Chemical composition and nutritional evaluation of quinoa ( Chenopodium quinoa Willd.). Journal of food composition and analysis: an official publication of the United Nations University, International Network of Food Data Systems 1992;5(1)35-68. - 67.
Jacobsen SE. The worldwide potential for quinoa ( Chenopodium quinoa Willd.). Food Reviews International 2003;19(1-2)167-177. - 68.
Gorinstein S, Vargas OJM, Jaramillo NO, Salas IA, Ayala ALM, Arancibia-Avila P, Toledo F, Katrich E, Trakhtenberg S. The total polyphenols and the antioxidant potentials of some selected cereals and pseudocereals. European Food Research and Technology 2007;225(3-4)321-328. - 69.
Nsimba RY, Kikuzaki H, Konishi Y. Antioxidant activity of various extracts and fractions of Chenopodium quinoa andAmaranthus spp. seeds. Food Chemistry 2008;106(2)760-766. - 70.
Repo-Carrasco-Valencia RAM, Serna AL. Quinoa ( Chenopodium quinoa Willd.) as a source of dietary fiber and other functional components. Ciencia e Tecnologia de Alimentos 2011;31(1)225-230. - 71.
Yildiz-Aktas L, Dagnon S, Gurel A, Gesheva E, Edreva A. Drought tolerance in cotton: involvement of non-enzymatic ROS-Scavenging Compounds. Journal of Agronomy and Crop Science 2009;195(4)247–253. - 72.
Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA. Breeding for abiotic stresses for sustainable agriculture. Philosophical Transactions of the Royal Society B-Biological Sciences 2008;363(1492)703–716. - 73.
Peleg Z, Walia H, E. B. Integrating genomics and genetics to accelerate development of drought and salinity tolerant crops. In: Altman A, Hasegawa PM. (ed.) Plant Biotechnology and Agriculture – Prospects for the 21st century. London: Elsevier; 2012. p 271-281. - 74.
FAO- Food and Agriculture Organization of the United Nations. Biotechnologies for Agriculture Development. Current status and options for crop biotechnology in developing countries. Rome, Italy. http://www.fao.org/docrep/014/i2300e/i2300e00.htm (accessed 1 July 2012). - 75.
Bray EA. Molecular responses to water-deficit. Plant Physiology 1993;103(4)1035- 1040. - 76.
Rodrigues F, Da Graça J, De Laia M, Nhani-Jr A, Galbiati J, Ferro MIT, Ferro, J.; Zingaretti, S. Sugarcane genes differentially expressed during water deficit. Biologia Plantarum 2011;55(1)43-53. - 77.
Bray EA. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Journal of Experimental Botany 2004;55(407)2331–2341. - 78.
Bray EA. Plant responses to water deficit. Trends in Plant Science 1997;2(2)1035-1040. - 79.
Shao H-B, Guo Q-J, Chu L-Y, Zhao X-N, Su Z-L, Hu Y-C, Cheng JF. Understanding molecular mechanism of higher plant plasticity under abiotic stress. Colloids and Surfaces B-Biointerfaces 2007;54(1)37-45. - 80.
Shinozaki K, Yamaguchi-Shinozaki K. Molecular responses to drought and cold stress. Current Opinion in Biotechnology 1996;7(2)161-167. - 81.
Rodrigues FA, de Laia ML, Zingaretti SM. Analysis of gene expression profiles under water stress in tolerant and sensitive sugarcane plants. Plant Science 2009;176(2)286–302. - 82.
Iskandar HM, Casu RE, Fletcher AT, Schmidt S, Xu J, Maclean DJ, Manners JM, Bonnett GD. Identification of drought-response genes and a study of their expression during sucrose accumulation and water deficit in sugarcane culms. BMC Plant Biology 2011;11-12 http://www.biomedcentral.com(accessed 4 June 2012). - 83.
Ding Z, Li S, An X, Liu X, Qin H, Wang D. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. Journal of Genetics and Genomics 2009;36(1)17-29. - 84.
Wang WX, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003;218(1)2181-2184. - 85.
Chen H-J, Su C-T, Lin C-H, Huang G-J, Lin Y-H. Expression of sweet potato cysteine protease SPCP2 altered developmental characteristics and stress responses in transgenic Arabidopsis plants. Journal of Plant Physiology 2010;167(10)838–847. - 86.
Nogueira FTS, Schlogl PS, Camargo SR, Fernandez JH, De Rosa VE, Pompermayer P, Arruda P. SsNAC23 , a member of the NAC domain protein family, is associated with cold, herbivory and water stress in sugarcane. Plant Science 2005;169(1)93–106. - 87.
Agarwal PK, Agarwal P, Reddy MK, Sopory SK. Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Reports 2006;25(12)1263-1274. - 88.
Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis . Plant and Cell Physiology 2009;50(12)2123–2132. - 89.
Molinari HBC, Marur CJ, Daros E, de Campos MKF, de Carvalho JFRP, Bespalhok Filho JC, Pereira LFP, Vieira LGE. Evaluation of the stress-inducible production of proline in transgenic sugarcane ( Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum 2007;130(2)218–229. - 90.
Zhai S-M, Gao Q, Xue H-W, Sui Z-H, Yue G-D, Yang A-F, Zhang J-R. Overexpression of the phosphatidylinositol synthase gene from Zea mays in tobacco plants alters the membrane lipids composition and improves drought stress tolerance. Planta 2012;235(1)69–84. - 91.
Zhang H, Shen G, Kuppu S, Gaxiola R, Payton P. Creating drought-and salt-tolerant cotton by overexpressing a vacuolar pyrophosphatase gene. Plant signaling & behavior 2011;6(6)861-863. - 92.
Yu S, Liao F, Wang F, Wen W, Li J, Mei H, Luo L. Identification of Rice Transcription Factors Associated with Drought Tolerance Using the Ecotilling Method. Plos One 2012;7(2)1-9. - 93.
Quan R, Hu S, Zhang Z, Zhang H, Zhang Z, Huang R. Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnology Journal 2010;8(4)476–488. - 94.
Trujillo LE, Sotolongo M, Menendez C, Ochogavia ME, Coll Y, Hernandez I, Borrás-Hidalgo O, Thomma BPHJ, Vera P, Hernández L. SodERF3 , a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant and Cell Physiology 2008;49(4)512–525. - 95.
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y. Overexpression of the soybean GmERF3 gene, anAP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. Journal of Experimental Botany 2009;60(13)3781–3796. - 96.
Capell T, Escobar C, Liu H, Burtin D, Lepri O, Christou P. Over-expression of the oat arginine decarboxylase cDNA in transgenic rice ( Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theoretical and Applied Genetics 1998;97(1-2)246-254. - 97.
Capell T, Bassie L, Christou P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences of the United States of America 2004;101(26)9909–9914. - 98.
Moghaieb REA, Tanaka N, Saneoka H, Hussein HA, Yousef SS, Ewada MAF, Aly MAM, Fujita K. Expression of betaine aldehyde dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. Soil Science and Plant Nutrition 2000;46(4)873-883. - 99.
Kumar S, Dhingra A, Daniell H. Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology 2004;136(1)2843-2854. - 100.
Quan R, Shang M, Zhang H, Zhao Y, Zhang J. Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol Journal 2004;2(6)477-486. - 101.
Prasad K, Saradhi PP. Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Science 2004;166(5)1197-1212. - 102.
Sakamoto A, Murata A, Murata N. Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Molecular Biology 1998;38(6)1011-1019. - 103.
Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK. Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theoretical and Applied Genetics 2002;106(1)51-57. - 104.
Su J, Hirji R, Zhang L, He CK, Selvaraj G, Wu R. Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. Journal of Experimental Botany 2006;57(5)1129-1135. - 105.
Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T. Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Molecular Biology 2000;43(1)103-111. - 106.
Tang W, Peng XX, Newton RJ. Enhanced tolerance to salt stress in transgenic loblolly pine simultaneously expressing two genes encoding mannitol-1-phosphate dehydrogenase and glucitol-6-phosphate dehydrogenase. Plant Physiology and Biochemistry 2005;43(2)139-146. - 107.
Abebe T, Guenzi AC, Martin B, Cushman JC. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiology 2003;131(4)1748-1755. - 108.
Molinari HBC, Marur CJ, Kobayashi AK, Pileggi M, Júnior RPL, Pereira LFP, Vieira LGE. Osmotic adjustment in transgenic citrus root stock Carrizo citrange ( Citrus sinensis Osb. xPoncirus trifoliata L. Raf.) overproducing proline. Plant Science 2004;167(6)1375-81. - 109.
Hmida-Sayari A, Gargouri-Bouzid R, Bidani A, Jaoua L, Savoure A, Jaoua S. Overexpression of Delta(1)-pyrroline-5-carboxylate synthetase increases proline production and confers salt tolerance in transgenic potato plants. Plant Science 2005;169(4)746-752. - 110.
Zhu B, Su J, Chang M, Verma DPS, Fan YL, Wu R. Overexpression of a [delta] 1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Science 1998;139(1)41-48. - 111.
Hong ZL, Lakkineni K, Zhang ZM, Verma DPS. Removal of feedback inhibition of Delta (1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology 2000; 122(4)1129-1136. - 112.
De Ronde J, Cress W, Krüger G, Strasser R, Van Staden J. Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. Journal of Plant Physiology 2004;161(11)1211-24. - 113.
Knipp G, Honermeier B. Effect of water stress on proline accumulation of genetically modified potatoes ( Solanum tuberosum L.) generating fructans. Journal of Plant Physiology 2006;163(4)392-397. - 114.
Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, et al. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiology 2003;131(2)516-524. - 115.
Cortina C, Culianez-Macia FA. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Science 2005;169(1)75–82. - 116.
Maqbool B, Zhong H, El-Maghraby Y, Ahmad A, Chai B, Wang W, Sabzikar R, Sticklen B. Competence of oat ( Avena sativa L.) shoot apical meristems for integrative transformation, inherited expression, and osmotic tolerance of transgenic lines containing hva1. Theoretical and Applied Genetics 2002;105(2-3)201-208. - 117.
Oraby HF, Ransom CB, Kravchenko AN, Sticklen MB. Barley HVA1 gene confers salt tolerance in R3 transgenic oat. Crop Science 2005;45(6)2218-2227. - 118.
Babu RC, Zhang JX, Blum A, Ho THD, Wu R, Nguyen HT. HVA1 , a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Science 2004;166(4)855-862. - 119.
Rohila JS, Jain RK, Wu R. Genetic improvement of Basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Science 2002;163(3)525-532. - 120.
Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho THD, Qu RD. Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Science 2000;155(1)1-9. - 121.
Bahieldin A, Mahfouz HT, Eissa HF, Saleh OM, Ramadan AM, Ahmed IA, Dyer WE, El-Itriby HA, Madkour MA. Field evaluation of transgenic wheat plants stably expressing the HVA1 gene for drought tolerance. Physiologia Plantarum 2005;123(4)421-427. - 122.
Xiao B, Huang Y, Tang N, Xiong L. Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theoretical and Applied Genetics 2007;115(1)35-46. - 123.
Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su W-A, Tang Z-C. The role of aquaporin RWC3 in drought avoidance in rice. Plant and Cell Physiology 2004;45(4)481-489. - 124.
He C, Yan J, Shen G, Fu L, Holaday AS, Auld D, Blumwald E, Zhang H. Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant and cell physiology 2005;46(11)1848-1854. - 125.
Apse MP, Aharon GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis . Science 1999;285(5431)1256–1258. - 126.
Xue ZY, Zhi DY, Xue GP, Zhang H, Zhao YX, Xia GM. Enhanced salt tolerance of transgenic wheat ( Triticum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Science 2004;167(4)849-859. - 127.
Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA. A role for HKT1 in sodium uptake by wheat roots. Plant Journal 2002;32(2)139-149. - 128.
Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Nahm BH, Ju- Kim K. Arabidopsis CBF3/DREB1A andABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiology 2005;138(1)341-351. - 129.
Roy M, Wu R. Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Science 2001;160(5)869-875. - 130.
Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Kazuko Y-S. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant and Cell Physiology 2006;47(1)141-153. - 131.
Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D. Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 2004;47(3)493-500. - 132.
Thompson AJ, Andrews J, Mulholland BJ, McKee JMT, Hilton HW, Horridge JS, Farquhar GD, Smeeton RC, Smillie IRA, Black CR, Taylor IB. Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiology 2007;143(4)1905-1917. - 133.
Borsani O, Cuartero J, Valpuesta V, Botella MA. Tomato tos1 mutation identifies a gene essential for osmotic tolerance and abscisic acid sensitivity. Plant Journal 2002;32(6)905-914. - 134.
Young TE, Meeley RB, Gallie DR. ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant Journal 2004;40(5):813-825.