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a Department of Soil, Environmental and Atmospheric Sciences,University of Missouri, Columbia, MO 65211
b USDA-ARS, University of Missouri, Columbia, MO 65211
* Corresponding author (motavallip{at}missouri.edu).
Received for publication May 5, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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Abbreviations: Bt crop, transgenic crop engineered to express Bacillus thuringiensis toxin
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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Although some research has examined the environmental impacts of the "aboveground" portion of transgenic crops, relatively less research effort has examined the effects of these crops on soil microbially mediated processes and functions in soils (O'Callaghan and Glare, 2001; Bruinsma et al., 2003). Among the many essential functions of soil biota are soil organic matter decomposition and nutrient mineralization and immobilization. Other microbially mediated processes in soil related to nutrient cycling include oxidation–reduction reactions (e.g., nitrification and denitrification), biological N fixation, and solubilization (e.g., solubilization of soil P).
Among the many challenges facing researchers examining the environmental effects of transgenic crops on biogeochemical cycles is the potential dependence of expression of those effects on factors such as climate, soil chemical and physical properties, crop variety, and time (Trevors et al., 1994). A major problem in evaluating the environmental effects of transgenic crops is the lack of sufficient long-term baseline information on the variation in soil microbially mediated nutrient cycling in diverse agroecosystems to compare with agroecosystems in which transgenic crops have been introduced (Dale et al., 2002; Bruinsma et al., 2003). In addition, knowledge of the complex diversity of soil microorganisms is limited since only a small portion of soil microbial populations can be cultured and identified using standard analytical methods, although some new methodological approaches, including use of molecular biological techniques, show some promise in helping to understand the impact of transgenic crops on soil microbial ecology (Angle, 1994; Bruinsma et al., 2003).
The introduction of transgenic crops expressing multiple traits ("stacked" genes) may further complicate determination of environmental impacts due to potential interactions among the inserted genes (National Research Council, 2002). An additional challenge will be to evaluate the potential environmental impacts of the wide range of transgenic crops under development. These new transgenic crops include plants containing modifications for improved resistance to stress conditions, plants with better nutritional qualities and vitamins, plants with enhanced N fixation and photosynthesis, and plants that produce industrial products or precursors, such as bioplastics, pharmaceutical proteins, and vaccines (Nottingham, 2002).
The objectives of this paper are to (i) review the available literature related to the environmental effects of transgenic crops and their management on soil microbially mediated nutrient transformations and (ii) consider soil properties and climatic factors that may affect the impact of transgenic crops on nutrient transformations. Although the current literature on the issue of the environmental impact of transgenic crops on soil nutrient transformations is not extensive, a review at this time may facilitate the determination of future priorities for research.
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TARGETED TRANSGENIC TRAITS AFFECTING PLANT NUTRIENT ACQUISITION |
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TOPABSTRACTINTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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The mechanisms by which these transgenic crops may overcome nutrient deficiencies, such as increased root exudation of organic acids, may directly or indirectly affect soil microbially mediated nutrient transformations. For example, the decrease in rhizosphere soil pH due to increased root exudation of organic acids may reduce the rate of microbially mediated processes sensitive to acidic pH (e.g., nitrification). However, the presence of organic anions in soil can also stimulate microbial activity and increase nutrient availability (Ryan et al., 2001). More subtle and complex environmental effects may occur to soil microbially mediated processes when previously marginal lands are converted to cultivation of stress-tolerant transgenic crops with concomitant changes in soil management (National Research Council, 2002).
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POTENTIAL NONTARGETED DIRECT AND INDIRECT EFFECTS |
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TOPABSTRACTINTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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A well-documented nontarget effect of root exudates has been with transgenic crops that incorporate the Cry1Ab gene from the bacterium Bacillus thuringiensis that codes for the production of an insecticidal protein that kills Lepidopteran pests (Schnepf et al., 1998; Donegan and Seidler, 1999; Saxena et al., 1999). The insecticidal toxin in root exudates (as well as pollen and crop residues) produced by Bt corn binds rapidly to montmorillonite and kaolinite clay minerals, humic acids, and organomineral complexes, which protect the toxin from microbial degradation (Tapp et al., 1994; Crecchio and Stotzky, 1998, 2001; Saxena et al., 2002). The bound toxin retains its insecticidal activity and has been observed to persist in soil for up to 234 d (Saxena et al., 1999). Similar results on the persistence of the insecticidal toxin of Bt cotton but for shorter periods of time (up to 140 d) have also been reported by Palm et al. (1996). That study observed a general pattern of rapid degradation of the toxin during the first 14 d of incubation followed by a slower rate of degradation over the total 140-d study period. Zwahlen et al. (2003) observed some variation in long-term persistence of the Bt toxin derived from degradation of corn residues in field trials depending on tillage practice.
The presence of the insecticidal toxin from Bt crops either through root exudates or by incorporation of residues of Bt crops has not generally been shown to have a significant effect on soil biological populations, which may affect soil nutrient transformations. Saxena and Stotzky (2001a) observed no apparent effects of Bt toxin from corn added to soil on earthworms, nematodes, protozoa, bacteria, and fungi. However, they suggested that more detailed research needs to be conducted to determine the effects of the toxin on soil biodiversity (Saxena and Stotzky, 2001a). Another study reported no direct effects of purified Bt toxin and Bt toxin contained in transgenic Bt cotton on soil microorganisms, but observed a transient but significant increase in culturable aerobic bacteria and fungi with two of three transgenic cotton lines, which was attributed to unexpected changes in plant characteristics as a result of genetic manipulation or tissue culture (Donegan et al., 1995). A survey of levels of Cry1Ac protein levels contained in soil samples of six fields grown to continuous Bt cotton for 3 to 6 yr indicated that no detectable Cry1Ac protein or biological insecticidal activity was present in any of the fields despite incorporation of the transgenic Bt cotton plant residues into the soil by postharvest tillage (Head et al., 2002). Similarly, aerobic bacterial and fungal populations, fungal species diversity, and abundance in soil planted to transgenic Bt potato (Solanum tuberosum L.) did not differ significantly from soil planted with non-transgenic potato plants (Donegan et al., 1996). The specificity of the Cry proteins for target pests, the small amount of the protein contained in plants, and its rapid degradation in soil reduces the risk of environmental impacts from cultivation of Bt crops (Betz et al., 2000).
Some evidence exists that transgenic plants currently under development may affect soil nutrient transformations, but whether root exudates or other nontargeted physiological changes in the plant are the mechanisms for these effects is unclear. Soil from field plots in which lignin peroxidase-producing transgenic alfalfa (Medicago sativa L.) was grown over two years had significantly higher population levels of culturable, aerobic spore-forming and cellulose-utilizing bacteria, lower activity of the soil enzymes dehydrogenase and alkaline phosphatase, and higher soil pH levels compared with that of the parental non-transgenic lines (Donegan and Seidler, 1999). However, population levels of protozoa, nematodes, and microarthropods, DNA fingerprints of indigenous bacteria, and rates of microbial substrate-induced respiration were not significantly affected by the growth of the transgenic alfalfa (Donegan and Seidler, 1999). The study also observed that the transgenic alfalfa had significantly lower shoot weight and higher tissue N and P contents compared with the parental non-transgenic plants. Further research examining nontargeted traits in transgenic crops under development and the mechanisms by which these traits may affect soil biologically mediated processes, including changes in root exudates, is needed to better understand the potential impact of these introduced crops on soil biological functions.
Herbicide Applications
One of the major changes in crop management practices that has occurred with the introduction of transgenic crops with herbicide resistance has been the widespread application of glyphosate [commonly applied as the isopropylamine salt of N-(phosphonomethyl) glycine]. In 2001, glyphosate-resistant soybean accounted for 46% (33.3 million ha) of the total area in the world planted to soybeans (Council for Agricultural Science and Technology, 2002). In the United States, glyphosate-treated land constituted 62% of the total area planted to soybeans in 2000 (Council for Agricultural Science and Technology, 2002).
An extensive review of the ecotoxicological risks associated with use of glyphosate and its formulations, including the herbicide Roundup (Monsanto, St. Louis, MO), is presented in Giesy et al. (2000). Among the factors affecting the toxicity of glyphosate and Roundup to soil microorganisms and invertebrates are the rate of glyphosate applied, soil properties such as soil texture and organic matter content, and whether the testing was done in artificial substrates or natural soil ecosystems (Giesy et al., 2000).
One potential effect of the application of glyphosate-based herbicides to soil is the stimulation or inhibition of soil microbially mediated nutrient transformations and related processes (Table 2). Toxic effects of glyphosate on soil microorganisms may occur because the enzyme 5-enolpyruvylshikamate-3-phosphate synthase (EPSPS), which glyphosate inhibits, is in both plants and soil microorganisms (Busse et al., 2001). However, Haney et al. (2000)( 2002) observed significantly higher C and N mineralization when Roundup Ultra was added to nine soils from Georgia and Texas with a range in soil pH, soil organic C, and clay content. The difference in C and N mineralization with added herbicide was directly attributed to the low C to N ratio of Roundup Ultra. They also observed higher rates of C mineralization of added Roundup Ultra in soils with higher organic C, which they attributed to the larger initial microbial biomass in these soils. However, differences in soil organic C, pH, and clay content among the soils in the study did not relate to the potential rate of C mineralization of the added Roundup Ultra.
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Inhibition of the growth of mycorrhizal fungi by glyphosate applications may affect soil nutrient transformations because of the often significant role of these fungi in plant nutrient acquisition among several plant species. Chakravarty and Chatarpaul (1990) observed reduction in the growth of five species of ectomycorrhizal fungi when exposed to glyphosate concentrations higher than 50 µL L–1 in culture media. This study also observed significantly lower fungal and bacterial populations in a sandy loam soil 2 mo after glyphosate treatment with a rate of 0.54 kg a.i. ha–1. Similarly, Estok et al. (1989) observed reductions in radial growth of three species of ectomycorrhizal fungi at glyphosate concentrations of 
1000 µL L–1 in culture media and complete inhibition of growth at concentrations of 5000 µL L–1. Further field research is required on glyphosate effects on soil mycorrhizae since research findings from artificial media assays may have limited relevance for predicting glyphosate effects on soil microorganisms under field conditions due to the greater complexity and variability of agricultural and forest ecosystems (Estok et al., 1989; Busse et al., 2001).
Another potential toxic effect of glyphosate applied to soil is inhibition of symbiotic N2 fixation. King et al. (2001) observed in greenhouse and growth chamber experiments using potting media that early applications of glyphosate at a rate of 1.68 kg a.i. ha–1 delayed N2 fixation and decreased biomass and N accumulation in glyphosate-tolerant soybean, especially when soil water content was low. However, affected soybean plants recovered 40 d after emergence. The observed delay in N2 fixation was attributed to the lack of resistant EPSPS in the N-fixing symbiotic bacteria, Bradyrhizobium japonicum, in glyphosate-resistant soybeans (King et al., 2001). In field experiments conducted on a Pembroke silt loam (fine-silty, mixed, active, mesic Mollic Paleudalfs) and a Sharkey clay (very-fine, smectitic, thermic Chromic Epiaquerts) in Arkansas by the same researchers, glyphosate-tolerant soybeans had decreased biomass and seed yields at one of two locations, possibly due to conditions of limited soil water at the affected site (King et al., 2001). Similarly, Reddy et al. (2000) determined that glyphosate applications of 2.24 kg a.i. ha–1 reduced shoot and root weights in glyphosate-resistant soybeans, and glyphosate applications of both 1.12 and 2.24 kg a.i. ha–1 reduced leghemoglobin content of nodules by 6 to 18%. Application of 2.24 kg a.i. ha–1 3 wk after planting resulted in a 30% reduction in nodule numbers and a 39% decrease in nodule mass.
Subsequent field studies revealed that glyphosate, regardless of formulation, reduced both leghemoglobin content and nodule mass of glyphosate-resistant soybean, indicating that nodule development was inhibited (Reddy and Zablotowicz, 2003). In addition, glyphosate accumulated in nodules of glyphosate-treated plants, with concentrations ranging from 39 to 147 ng g–1 nodule dry weight. The interference of nodule development combined with the sensitivity of B. japonicum to glyphosate concentrations at 1 to 5 mM (Moorman et al., 1992) suggests potential adverse effects on nitrogen fixation in soybean. However, the researchers for both studies noted that even though glyphosate application at recommended application rates may reduce nodule development, effects were minimal and soybean varieties studied so far have the potential to compensate after short durations of stress that may occur due to glyphosate application.
Crop Residues and Organic Wastes
Changes in the fate of crop residues from transgenic crops compared with non-transgenic crops may occur through several mechanisms including: (i) alterations in the composition, quantity, and physical form of residues from transgenic crops; (ii) inhibition or stimulation of soil microbial communities involved in nutrient transformations, possibly through chemical compounds contained in the transgenic residues; (iii) changes in management practices (e.g., tillage) for transgenic crops affecting biotic and abiotic factors involved in decomposition and nutrient turnover of crop residues; and (iv) the effects of any possible physical or chemical changes in transgenic residues on feeding and digestion of the residues in animals that may affect animal waste characteristics and its decomposition in soil (Fig. 1).
Differences in the composition of crop residues due to the introduction of a transgenic trait have been primarily observed in transgenic Bt crops. Masoero et al. (1999) determined that two transgenic Bt corn hybrids had higher starch and lignin and lower protein and soluble N contents compared with non-transgenic corn, depending on the Bt hybrid. Similarly, Saxena and Stotzky (2001b) observed 33 to 97% higher lignin content in 10 Bt corn hybrids, either grown in a plant growth chamber or in the field, compared with their respective non-Bt isolines. In contrast, Escher et al. (2000) found a lower C to N ratio and lignin content and a higher content of soluble carbohydrates in the leaves of one Bt corn variety compared with the corresponding non-transgenic corn variety. These differences in tissue composition resulted in a lower mortality of woodlice (Porcellio scaber), but bacterial growth on leaves and fungal growth on feces of P. scaber were equal for both corn varieties. However, this study also observed a faster rate of lignin decomposition in transgenic corn.
The effects of crop residue composition and the importance of several indices of residue quality, including the C to N ratio, lignin content, lignin to N ratio, initial N content, polyphenol content, polyphenol to N ratio, and initial soluble C concentrations of the residue, on decomposition and N mineralization have been extensively examined under both temperate and tropical conditions (Franzluebbers et al., 1996; Fernandes et al., 1997; Trinsoutrot et al., 2000). In general, as the lignin or polyphenolic content to N ratio of the plant material increases or the initial N content decreases, the decomposition rate of the material is lower and short-term N availability may be reduced (Fernandes et al., 1997). Therefore, the lower or higher lignin content observed in some Bt crops may act to increase or reduce rates of residue decomposition and N mineralization of organic N contained in the residues. However, any reductions in the rate of N mineralization due to transgenic residues could be offset by the larger amount of total N added in crop residues under Bt crops, which may have higher yields than non-transgenic crops, especially after exposure to Bt-sensitive insect pests.
Differences in decomposition and N transformations due to changes in the physical form of transgenic versus non-transgenic crop residues have not been extensively studied. For example, Bt tolerant corn residues may have less corn borer damage in stem tissue and therefore, these residues would possibly have less physical accessibility for biological decomposition.
Increased crop residues that are more or less resistant to decomposition due to the growth of transgenic crops may also affect the amount of environmental nutrient loss through soil erosion and runoff since a higher content of crop residues, especially on the soil surface, has been linked with increased soil conservation (Alberts and Neibling, 1994; Lal et al., 1994). In addition, improved weed control with herbicide-tolerant crops has also stimulated a larger proportion of producers to adopt conservation tillage leaving more crop residues on the surface and potentially reducing soil erosion (Council for Agricultural Science and Technology, 2002).
The effects of transgenic crop residues on any changes in animal waste characteristics and the subsequent decomposition of that animal waste in soil has also not been extensively examined. One problem in assessing the impact of transgenic crop residues on soil microbial processes and functions is the wide range in feed quality that occurs in non-transgenic residues (Klopfenstein, 1994). Folmer et al. (2002) studied the utilization of Bt corn residues by grazing beef steers and found no significant differences in daily weight gain of the steers and in grazing preferences between Bt and non-Bt corn residues. Transgenic low phytate or high available phosphorus (HAP) crops are being developed that would contain less phytate thereby increasing the efficiency of feed P absorption in monogastric animals, such as pigs and poultry (Huff et al., 1998; Sands et al., 2001). This increased efficiency would result in possible reductions in the P content of animal wastes applied to land, effectively lowering the potential for water quality problems due to excessive P in the environment. Since research related to transgenic HAP crops has been primarily focused on use of HAP grain as the feed source, information related to the fate in soil of other residues of HAP crops and associated transgenic crops that produce phytase, an enzyme that facilitates the breakdown of phytin, is limited.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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TOPABSTRACTINTRODUCTIONTARGETED TRANSGENIC TRAITS...POTENTIAL NONTARGETED DIRECT AND...CONCLUSIONSREFERENCES |
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