Understanding regulatory networks and engineering for enhanced drought tolerance in plants
Introduction
When plants experience environmental stresses such as drought, salinity, high and low temperature, intense light, and excessive ozone or CO2 they activate a diverse set of physiological, metabolic and defense systems to survive and to sustain growth. Tolerance and susceptibility to abiotic stresses are very complex. Abiotic stress is the primary cause of crop loss worldwide, causing average yield losses of more than 50% for major crops [1, 2]. Plant traits that are associated with resistance mechanisms are multigenic, and thus difficult to control and engineer. Transcriptomics, proteomics and gene expression studies have identified the activation and regulation of several stress-related transcripts and proteins, which are generally classified into two major groups. One group is involved in signaling cascades and in transcriptional control, whereas members of the other group function in membrane protection, as osmoprotectants, as antioxidants and as reactive oxygen species (ROS) scavengers. Manipulation of genes that protect and maintain cellular functions or that maintain the structure of cellular components has been the major target of attempts to produce plants that have enhanced stress tolerance.
Among the various abiotic stresses, drought is the major factor that limits crop productivity worldwide. Exposure of plants to a water-limiting environment during various developmental stages appears to activate various physiological and developmental changes. Understanding of the basic biochemical and molecular mechanisms for drought stress perception, transduction and tolerance is still a major challenge in biology. Plant modification for enhanced drought tolerance is mostly based on the manipulation of either transcription and/or signaling factors or genes that directly protect plant cells against water deficit.
Reviews on the molecular mechanisms of abiotic stress responses and the genetic regulatory networks of drought stress tolerance have been published recently [3, 4, 5•, 6, 7••]. This review focuses on the recent progress in understanding the mechanisms of gene regulation and the roles of protective metabolites in drought stress tolerance, and the progress in genetic or metabolic engineering for enhanced drought tolerance in crop plants. We have categorized these engineering efforts into two major groups: first, engineering cell signaling and gene regulation, and second, engineering for osmoprotectant accumulation.
Section snippets
Physiological and biochemical responses
Physiological and biochemical changes at the cellular level that are associated with drought stress include turgor loss, changes in membrane fluidity and composition, changes in solute concentration, and protein–protein and protein–lipid interactions [8]. Plant tissues can maintain turgor during drought by avoiding dehydration, tolerating dehydration or both [9]. These forms of stress resistance are controlled by developmental and morphological traits such as root thickness, the ability of
Engineering cell signaling and gene regulation
Gene expression profiling using cDNA or oligo microarray technology has advanced our basic understanding of gene regulatory networks that are active during the exposure of plants to various stresses [6, 17, 18•]. In Arabidopsis, numerous genes that respond to dehydration stress have been identified and categorized as responsive to dehydration (rd) and early response to dehydration (erd) genes [19]. There are at least four independent regulatory systems for gene expression in response to water
Engineering for osmoprotectant accumulation
Osmoprotectants are small neutral molecules that are non toxic to the cell at molar concentration and that stabilize proteins and cell membranes against the denaturing effect of stress conditions on cellular functions [44]. Many major crops lack the ability to synthesize the special osmoprotectants that are naturally accumulated by stress-tolerant organisms. It has been hypothesized, therefore, that engineering the introduction of osmoprotectant synthesis pathways is a potential strategy for
Mannitol
Mannitol is a major photosynthetic product in many algae and higher plants and enhances tolerance to water-deficit stress primarily through osmotic adjustment [47]. The introduction of a mannitol dehydrogenase (mtlD) gene into wheat [48] produced a considerable increase in water stress tolerance. There was, however, no significant difference in osmotic adjustment between the mtlD transgenic wheat and control plants, at either the callus or whole-plant level, suggesting that the beneficial
Raffinose, galactionol and fructan
Water deficit alters the synthesis and partitioning of metabolically important carbohydrates in plants. Some of these effects on carbohydrate metabolism might be required for the photosynthetic assimilation of carbon and/or its conversion to metabolically usable forms. Other stress-induced changes in carbon metabolism might reflect adaptations for stress tolerance [51]. For example, raffinose-family oligosaccharides, such as raffinose, stachyose and galactinol, play important roles in the
Trehalose
Trehalose (α-d-glucopyranosyl-1,1-α-d-glucopyranoside) is a non-reducing disaccharide that is present in many different organisms and that functions as reserve carbohydrate and stress protectant, stabilizing proteins and membranes and protecting them from denaturation [56]. In yeast, trehalose is synthesized from UDP-glucose and glucose-6-phosphate in two reactions, which are catalyzed by trehalose phosphate synthase (TPS) and trehalose-6-phoshate-phosphatase (TPP) [57]. A family of 11 TPS
Proline
Proline accumulation plays a highly protective role in plants that are exposed to abiotic stresses, conferring osmotic adjustment together with an increase in the levels of other osmolytes. Other suggested functions of proline are the detoxification of ROS and interaction with the hydrophobic residue of proteins. The proline biosynthetic pathway has been well characterized [63, 64].
The involvement of proline in the response to water deficits has been demonstrated in transgenic tobacco that
Conclusions and future perspectives
Transcriptomic, proteomic and metabolic analyses have identified and characterized several genes that are induced by drought stress and the associated signaling and regulatory pathways in plants. Recent efforts on dissecting the cross-talk between drought stress and other major abiotic stress signaling pathways also provide potential candidates for multiple stress tolerance. Most of these studies were conducted using model plants, and engineering for drought tolerance in crop plants is still in
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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