In higher plants, ethylene is produced from L-methionine via the intermediates, S-adenosyl-L-methionine (SAM) and 1-aminocyclopropane-1-carboxylic acid (ACC) . The enzymes involved in this metabolic sequence are SAM synthetase, which catalyzes the conversion of methionine to SAM ; ACC synthase, which is responsible for the hydrolysis of SAM to ACC and 5-methylthioadenosine ; and ACC oxidase, which metabolizes ACC to ethylene, carbon dioxide and cyanide .
In 1978, an enzyme capable of degrading ACC was isolated from Pseudomonas sp. strain ACP . Since then, ACC deaminase has been detected in several fungi and yeasts [17, 18] as well as in bacterial strains [1, 2, 19-26] This enzyme cleaves the plant ethylene precursor, ACC, to produce ammonia and a-ketobutyrate. It has been proposed  that microorganisms that contain the enzyme ACC deaminase can all promote plant growth since they act as a sink for ACC and thereby lower ethylene levels in a developing or stressed plant.
Ethylene is important for normal development in plants as well as for their response to stress . Ethylene is important during the early phase of plant growth; it is required by many plant species for seed germination, and the rate of ethylene production increases during germination and seedling growth . Ethylene also induces some plant defences including induced systemic resistance . However, high levels of ethylene can lead to inhibition of root elongation and the onset of senescence.
Strains of ACC deaminase-containing plant growth-promoting bacteria can reduce the amount of ACC within plant tissues that is detectable by HPLC, and hence the ethylene levels in plants are also lowered [5, 30]. As a consequence of this activity, ACC deaminase-containing plant growth-promoting bacteria promote root elongation in a variety of (ethylene sensitive) plants . In addition to lowering ethylene levels during plant development, ACC deaminase-containing plant growth-promoting bacteria decrease the levels of "stress ethylene" — the accelerated biosynthesis of ethylene associated with biological and environmental stresses and pathogen attack . Thus, the deleterious effects of flooding, high salt or drought on tomato plants [26, 33, 34] were decreased and the shelf life of the petals of ethylene sensitive cut flowers was prolonged, following treatment with ACC deaminase-containing plant growth promoting bacteria . Moreover, biocontrol strains of bacteria carrying ACC deaminase genes were better able to protect plants against various phytopathogens . In addition, canola seedlings grown in the presence of high levels of nickel, produced much less ethylene when the seeds were inoculated with an ACC deaminase-containing nickel-resistant plant growth-promoting strain that also produced indoleacetic acid and high levels of siderophores . In each of these situations, the ''stress ethylene'' produced and the damage caused by it, was reduced by the activity of ACC deaminase.
2. Plant growth-promoting bacteria and phytoremediation
While plants grown on metal contaminated soils might be able to withstand some of the inhibitory effects of high concentrations of metals within a plant, two features of most plants could result in a decrease in plant growth and viability. In the presence of plant inhibitory levels of metals, most plants (i) synthesize stress ethylene and (ii) become severely depleted in the amount of iron that they contain. Fortunately, ACC deaminase-containing plant growth-promoting bacteria may be used to relieve some of the toxicity of metals to plants. This can occur in two different ways (i) a decrease in the level of stress ethylene in plants growing in metal-contaminated soil and (ii) utilization by plants of complexes between bacterial siderophores and iron. Plant siderophores bind to iron with a much lower affinity than bacterial siderophores so that in metal-contaminated soils a plant is generally unable to accumulate a sufficient amount of iron (and often becomes chlorotic) unless bacterial siderophores are present.
In one study, in an effort to overcome the inhibition of plant growth by nickel, a bacterium was isolated from a nickel contaminated soil sample; the bacterium was (i) nickel-resistant, (ii) capable of synthesizing the auxin indoleacetic acid, (iii) able to grow at the cold temperatures (i.e., 5-10°C) that one expects to find in nickel contaminated soil environments in northern climes such as Canada, and (iv) an active producer of ACC deaminase . In order to isolate plant growth-promoting bacteria, all of the nickel-resistant bacterial isolates from a nickel-contaminated rhizosphere soil sample were tested for the ability to grow on minimal medium with ACC as the sole source of nitrogen . Nickel-resistant bacterial strains that were also able to grow on ACC were tested for the ability to produce siderophores and grow in cold temperatures. It was ascertained in laboratory tests, that the selected bacterium could promote plant growth (both roots and shoots) in the presence of high levels (1-6 mM) of nickel [22, 38].
Subsequently, a spontaneous siderophore overproducing mutant of this bacterium was selected. When the wild-type bacterium and the siderophore overproducing mutant were tested in the laboratory, both of them were observed to promote the growth of tomato, canola and Indian mustard plants in soil that contained otherwise inhibitory levels of nickel, lead or zinc. In addition, the siderophore overproducing mutant decreased the inhibitory effect of the added metal on plant growth significantly more than the wild-type bacterium. Metal contamination of soils is often associated with iron-deficiency of the plants grown in these soils . The low iron content of plants that are grown in the presence of high levels of metals generally results in these plants becoming chlorotic, since iron deficiency inhibits both chloroplast development and chlorophyll biosynthesis . Moreover, iron deficiency is a stress that causes the plant to synthesize stress ethylene. However, once they have bound iron, bacterial iron-siderophore complexes can be taken up by plants and thereby serve as an iron source for plants .
Thus, there is (at least) a dual role for bacteria that facilitate plant growth in metal-contaminated soils. On the one hand, the bacteria lower the level of stress ethylene in the plant thereby allowing it to develop longer roots and thus better establish itself during early stages of growth [11, 22]. On the other hand, the bacterium helps the plant to acquire sufficient iron for optimal plant growth, in the presence of levels of metals that might otherwise make the acquisition of iron difficult . When the siderophore overproducing mutant was tested in the field with nickel-contaminated soil, it was observed that both the number of seeds that germinated, and the size that the plants were able to attain was increased by 50-100% by the presence of the bacterium.
In another study, the common reed, Phragmites australis, a plant that has often been suggested for use in the phytoremediation of wetlands, was grown from seed in the laboratory in copper-contaminated soil. It was observed that the addition of a copper-resistant strain of Pseudomonas asplenii that had been genetically transformed to express a bacterial ACC deaminase gene significantly stimulated seed germination in the presence of high levels of copper where the native form of this bacterium had no stimulatory effect on seed germination (M.L.E Reed, B. Warner and B.R. Glick, submitted for publication). This is consistent with the notion that one reason that plant germination is often inhibited by the presence of high levels of soil contaminants is that a high level of ethylene is produced in seeds as a response to the contaminant. In this case, lowering seed ethylene levels so that they are no longer inhibitory should promote seed germination in the presence of a range of contaminants. Moreover, in these experiments, both the native and the transformed strain of Pseudomonas asplenii had a small but reproducible stimulatory effect on Phragmites australis root and shoot growth. This indicates that, at least for Phragmites australis, growth inhibition by copper is not solely a consequence of stress ethylene synthesis but rather likely mainly reflects copper inhibition of plant metabolic processes.
In a separate but similar study, the growth of canola roots and shoots in copper-contaminated soil was stimulated (significantly) but to the same extent by both native and ACC deaminase-transformed Pseudomonas asplenii (M.L.E. Reed and B.R. Glick, submitted for publication). In this case, the promotion of plant growth by both native and transformed Pseudomonas asplenii was attributed to the production of indoleactic acid by the added bacteria since this strain does not produce siderophores (and therefore could not be involved in providing iron to the plant). Only the transformed strain has ACC deaminase activity so that, as with Phragmites australis, decreasing ethylene levels is not a factor in growth promotion, and bacterial indoleacetic acid has previously been shown to be capable of directly promoting plant growth .
Given the extreme toxicity of arsenate to most plants and bacteria, the development of a phytoremediation scheme for the detoxification of arsenate-contaminated soils is not a simple matter. For example, unlike what has been observed with nickel, lead, copper and zinc, arsenate-resistant plant growth-promoting bacteria do not significantly protect plants from arsenate inhibition.
Polycyclic aromatic hydrocarbons (PAHs) are a particularly recalcitrant group of contaminants and are known to be highly persistent in the environment. In situ microbial remediation (i.e., bioremediation) has been attempted, but it is difficult to generate sufficient biomass in natural soils to achieve an acceptable rate of movement of hydrophobic PAHs (which are often tightly bound to soil particles) to the microbes where they can be degraded. In addition, relatively few microorganisms can use high molecular weight PAHs as a sole carbon source. More recently, there have been some improvements in the strategies for bacterial remediation of contaminated soil, including inoculation with bacteria that were selected from PAH contaminated sites, or supplementing contaminated soils with nutrients . However, there has only been limited success with these techniques. For bioremediation to be effective, the overall rate of PAH removal and degradation must be accelerated above current levels. One way to achieve this is to increase the amount of biomass in the contaminated soil. For this reason, the use of phytoremediation has received considerable attention [45-47].
Although using plants for remediation of persistent contaminants may have advantages over other methods, many limitations exist for the large-scale application of this technology. For example, many plant species are sensitive to contaminants including PAHs so that they grow slowly, and it is time consuming to establish sufficient biomass for meaningful soil remediation. In addition, in most contaminated soils, the number of microorganisms is depressed so that there are not enough bacteria either to facilitate contaminant degradation or to support plant growth. To remedy this situation, both degradative and plant growth-promoting bacteria may be added to the plant rhizosphere. Phytoremediation (where contaminant degradation is dependent solely on plants) is not significantly faster than bioremediation (where biodegradation of the organics is by microorganisms independent of plants) for removal of PAHs or TPHs (Total Petroleum Hydrocarbons) [48-50]. However, cultivating plants together with plant growth-promoting bacteria allows the plants to germinate in the presence of soil contaminants to a much greater extent than they would otherwise, and then to grow well under stressful conditions and accumulate a larger amount of biomass than plants grown in the absence of plant growth-promoting bacteria. In addition, the plant growth-promoting bacteria in these experiments significantly increase the amount of PAH or TPH that is removed from the soil. In heavily contaminated soils, plant growth-promoting bacteria increased seed germination and plant survival, increased the plant water content, helped plants to maintain their chlorophyll contents and chlorophyll a/b ratio, and promoted plant root and shoot growth. In the case of PAHs, this is most likely due to a combination of the direct promotion of plant growth by bacterial indoleacetic acid and a lowering of the concentration of stress ethylene by bacterial ACC deaminase (MLE Reed and BR Glick, submitted for publication). As a consequence of the treatment of plants with plant growth-promoting bacteria, the plants provide a greater sink for the contaminants since they are better able to survive and proliferate.
3. Phytoremediation with plants engineered to produce less ethylene
If ACC deaminase-containing plant growth-promoting bacteria, bound to plant roots, can act as a sink for some of the excess ACC produced as a consequence of environmental stress, then transgenic plants expressing a bacterial ACC deaminase gene should behave similarly and have a level of stress ethylene lower than non-transformed plants and consequently be less susceptible to the deleterious effects of the stress. In fact, in two separate studies transgenic plants expressing ACC deaminase were shown to proliferate to a much greater extent than the comparable non-transformed plants in the presence of metals [51, 52]. In one study, transgenic tomato plants expressing a bacterial ACC deaminase gene under the transcriptional control of two tandem 35S cauliflower mosaic virus promoters (constitutive expression), the rolD promoter from Agrobacterium rhizogenes (root specific expression) or the pathogenesis related PRB-1b promoter from tobacco, were compared to non-transgenic tomato plants in their ability to grow in the presence of cadmium, cobalt, copper, magnesium, nickel, lead or zinc and to accumulate these metals . These transgenic tomato plants acquired a greater amount of metal within the plant tissues, and were less subject to the inhibitory effects of the metals on plant growth than were non-transformed plants. Moreover, plants in which the ACC deaminase gene was under the transcriptional control of the rolD promoter were more resistant to the various metals than were the other transgenic plants.
Of course, there is no expectation that transgenic tomato plants will ever become part of a phytoremediation strategy. Nevertheless, the results that were obtained with tomato plants were intriguing and served as a starting point for the development of other transgenic plants with lowered ethylene concentrations that could be used as a component of a phytoremediation scheme. Thus, both transgenic tobacco (because of its potentially large leaf biomass) and canola (because of its previously demonstrated ability to be a moderate accumulator of numerous metals) were transformed with bacterial ACC deaminase genes under the transcriptional control of either the 35S or rolD promoters (Li, Q, Shah, S, Saleh-Lakh, S and GLick, BR, submitted for publication; Stearns, JC, Shah, S, Dixon, DG, Greenberg BM and Glick, BR, submitted for publication). When they were tested, in laboratory and greenhouse experiments, the transgenic tobacco and canola plants responded similarly to the presence of nickel in the soil to the previously constructed transgenic tomatoes. In all instances, transgenic plants in which the exogenous ACC deaminase gene was controlled by the rolD promoter demonstrated the highest level of resistance to growth inhibition by nickel. Moreover, rolD canola plants were also resistant to growth inhibition by high levels of salt in the soil (Sergeeva, E, Shah, S and Glick, BR, submitted for publication). Reminiscent of the protection from salt stress that is afforded by a salt-resistant plant growth-promoting bacterium . From these and other data, it appears that the behaviour of plants to a variety of stresses (metals, salt, flooding and pathogens), transformed with an exogenous ACC deaminase gene controlled by the rolD promoter, is similar to the way in which these plants respond when ACC deaminase-containing plant growth-promoting bacteria have colonized the plant roots. In both cases, root-associated ACC deaminase acts as a sink for ACC and thereby prevents the formation of growth inhibitory levels of stress ethylene. The major difference between these two scenarios is that, in addition to lowering ethylene levels, the bacteria can directly promote plant growth by providing the hormone indoleacetic acid or siderophores that help the plant to obtain a sufficient amount of iron. In fact, in laboratory and greenhouse experiments, ACC deaminase-containing plant growth-promoting bacteria generally are a greater stimulus to plant growth under a range of stressful and potentially inhibitory conditions than are ACC deaminase transgenes expressed exclusively in the roots. Unfortunately, as a consequence of a number of environmental factors (such as weather and the presence of predators in the soil) plant growth-promoting bacteria may not always be as persistent in field conditions as they are in the greenhouse. One way around this problem may be to select or engineer endophytic bacterial strains that promote plant growth by employing some of the above mentioned bacterial mechanisms [53-55]. Finally, it should also be noted that plant ethylene levels may be decreased through a variety of genetic manipulations (e.g., the use of antisense versions of ACC oxidase) other than ACC deaminase. .
In another study, the growth of canola plants expressing ACC deaminase under the control of two tandem 35S cauliflower mosaic virus promoters in the presence of arsenate was monitored . About 70-80% of the transgenic plants germinated while a maximum of 25-30% of the non-transformed plants germinated. Although a small ethylene pulse is important in breaking seed dormancy in many plants, too much ethylene can inhibit plant seed germination . In the presence of arsenate, ACC deaminase may enhance the process of germination by hydrolyzing any excess ACC that forms as a consequence of the stress, hence lowering the inhibitory level of ethylene in seeds. Transgenic canola also had much higher fresh and dry weights of roots and shoots, and higher leaf chlorophyll contents, than non-transformed canola grown in the presence of arsenate. Moreover, the addition of plant growth-promoting bacteria to the roots of transgenic canola plants grown in arsenate-contaminated soils helped the plants to grow to a slightly larger size. In this case, growth promotion is probably attributable to the bacterial indoleacetic acid. When biomass and rate of seed germination are considered in calculating arsenate accumulation, for each seed planted, transgenic canola expressing ACC deaminase takes up approximately eight times as much arsenate as non-transformed canola. This notwithstanding, considerable work remains to be done before a practical system for the phytoremediation of arsenic can be implemented.
Microbial activities exerted in the rhizosphere can influence plant growth, development and metabolism at both the root and the shoot levels, and can reduce the effects of various stresses. More specifically, traits that directly contribute to the promotion of plant growth and stress reduction include the synthesis of indoleacetic acid, siderophores and the enzyme ACC deaminase. Several strains of plant growth-promoting bacteria with different properties are already commercially available and are being used to increase crop yields.
Given the current reluctance on the part of many consumers worldwide to embrace the use of foods derived from genetically modified plants, it may be advantageous to use either natural or genetically engineered plant growth-promoting bacteria as a means to promote growth or reduce disease through induction of resistance, rather than genetically modifying the plant itself to the same end. Moreover, given the large number of different plants, the various cultivars of those plants and the multiplicity of genes that would need to be engineered into plants, it is not feasible to genetically engineer all plants to be resistant to all pathogens and environmental stresses. Rather, it seems more logical to engineer plant growth-promoting bacteria to do this job; the first step in this direction could well be the introduction of appropriately regulated ACC deaminase genes. While ethylene signalling is required for the induction of systemic resistance elicited by rhizobacteria, a significant increase in the level of ethylene is not. Hence, lowering of ethylene levels by bacterial ACC deaminase is not incompatible with the induction of systemic resistance. Indeed, some bacterial strains possessing ACC deaminase also induce systemic resistance.
Work from the author's laboratory was supported by grants from the Natural Science and Engineering Research Council, CRESTech (a province of Ontario Centre of Excellence), Ontario Hydro, and Inco. The following individuals contributed to the work reviewed here: Genrich Burd, George Dixon, XiaoDong Huang, Sibdas Ghosh, Bruce Greenberg, Varvara Grichko, Jiping Li, Qiaosi Li, Wenbo Ma, Shimon Mayak, Barbara Moffatt, Lin Nie, Cheryl Patten, Donna Penrose, Lucy Reed, Saleema Saleh-Lakha, Elena Sergeeva, Saleh Shah, Jennifer Stearns, Tsipi Tirosh, Chunxia Wang and Barry Warner.
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