Article appears in: Breckling B & Verhoeven R (eds) Risk Hazard Damage - Specification of criteria to assess environmental impact of genetically modified ür Naturschutz. Naturschutz und Biologische1:239-244

Transgene ecology: An ecological perspective for GMO risk assessment

David Quist
Department of Environmental Science, Policy and Management,
University of California, Berkeley, 94720-3110 USA
[email protected]

Abstract

To thoroughly identify risks and hazards associated with the environmental release of genetically modified organisms (GMOs), the most current conceptual and empirical knowledge and peer-reviewed science on transgenic biology must be considered. Recent advances in genetics, ecology, and biochemistry is have uncovered the inherent complexity of gene expression systems. Much of this information is not included in current GMO risk assessments. In order to synthesise this information into risk assessments, an expanded, integrative, and interdisciplinary framework is needed to bridge existing gaps
in scientific knowledge on gene regulation and expression in different biological and physical backgrounds. Transgene ecology is a useful approach to develop this framework. Molecular characterizations, epigenetic regulation, selective outcrossing, environmental influences on transgene expression, and horizontal gene transfer are specific areas where transgene ecology is useful as a conceptual tool. Further, transgene ecology allows the integration of scientific information from many disciplines and perspectives for sound GMO risk assessment. The occurrence of transgenic contamination of Mexican maize and the implications for maize genetic diversity is considered in this context.

Keywords: transgene ecology; GMO risk assessment; gene flow; Mexican maize; horizontal gene transfer; epigenetics

1. Introduction

Do the scientific concepts and principles utilized in GMO risk assessment reflect the current state of empirical knowledge on transgenic biology?

This would seem a reasonable first step to evaluate how likely it is that we can determine risks and hazards, which, without the most current knowledge, would might not be considered risks or hazards in the first place. What we evaluate as a risk or hazard is dependent on the epistemological and scientific concepts we apply. Thus, it is important to critically examine not only what we value in GMO environmental risk assessment, but also how we come to ask the questions from which we estimate value. This also means understanding and acknowledging scientific uncertainties, including gaps of knowledge.

With this in mind, I will examine this fundamental question further at the level of molecular biology, from which recombinant DNA technology has been conceptualized and developed. Specifically, I wish to focus on the biology and study of GMO crop plants, discuss an expanded framework for assessing risk of transgenic plants, and then apply this thinking to the real world example of transgenic contamination of maize in Mexico.

For decades, the “one gene, one protein” model of gene expression, the “Central from genotype to phenotype. Genetic determinism is the central theory applied when transgenic organisms were first developed. Similarly, GMO risk assessment has historically used this same understanding within its framework. With evolving knowledge, we have come to understand that gene expression does not quite work that way. Imbedded are overlapping levels of organization that influence the regulation and inheritance of DNA expression that are not reflected at the DNA level. With this, we have learned that reductionist approaches to agricultural problem solving (e.g. genetic engineering), not and cannot consider the broader context of their introduction. In light of this, new conceptual tools are necessary to expand the frame of understanding on how transgenic DNA behaves within a larger context of the ecosystem.

So if the current framework is inadequate to address questions of safety, what is needed? An expansion of the current frame to include a more flexible, integrative and interdisciplinary approach would shed more light on the nature and functioning of the complex interconnectedness agrosystems and ecosystems. An ecological approach may provide viable tools for bridging gaps of knowledge that exists in these networks. Gene ecology, and more specifically transgene ecology, provides an expansion of the current framework to provide the unmet need of synthesising new scientific information on the biology and ecology of GMOs for evaluating environmental risks and hazards of they may pose. As global transgenization is well underway, it is even more critical that GMO risks be considered in the context of their introductions into the environment (MARVIER 2001) and into food systems alike.

2. Transgene ecology as a conceptual approach

2.1. Molecular characterizations and ecological studies

2.2. Epigenetic gene regulation: ncRNAs

Epigenetic regulation of gene expression has emerged as one of the most exciting and revealing lines of investigation in gene expression. Epigenetic regulation of genes involves the emergence of heritable phenotypic changes that are not reflected in the actual DNA code (see ANDERSON & PANNING 2003). In the molecular biology world, where we previously thought that only DNA carried heritable information on the expression of genes (leading to a phenotype), we now know the RNA world consists of a diversity of non-coding RNA forms that can influence this expression (see review by MATTICK 2003).

As of yet, epigenetic concepts have not been integrated into GMO risk assessments of crop plants. Transgene ecology is particularly fitting in this context, by investigating these higher levels of organization – the chemical, physical, and environmental cues – involve in modulating ncRNA activity and the subsequent influence on gene expression.

2.3. Selective outcrossing

2.4. Environmental influence on gene expression systems

Even though the impact of environmental variables on gene expression in barley were not predicted (nor the point of the study), this information is quite useful in considering how genes may behave in real world conditions where variations in climatic conditions is the rule, not the exception. The inherent unpredictability of the weather paired with the variable response in gene expression suggests this would be an important area of study, where ecological investigations might shed some much needed light.

2.5. Horizontal gene transfer

Horizontal gene transfer (HGT), simply stated, is the transfer of genes from one organism to another by a means other than descent (e.g. via transformation, conjugation or transduction). Transgenic organisms provide excellent models to investigate HGT, as many of the sequences used in the production of transgenic plants have high homologies to known viral and bacterial sequences and can be acquired laterally. Viruses and bacteria particularly are known to utilize HGT as a mechanism to instill genetic diversity into their populations (though not all of it necessarily useful or advantageous). Thus HGT
may be central to the evolution of life, including how prokaryotes gave rise to eukaryotic cells (DOOLITTLE 1999). Research into HGT is therefore of wide interest in many fields of biology.

In the case of GMOs, horizontal gene transfer of transgenic DNA to prokaryotes (NIELSEN et al. 1998) and some eukaryotes (HOFFMAN et al. 1994) has been documented. Although the frequency, stability and significance of such events are a matter of debate, it has not been studied adequately to address potential of HGT for altering the evolutionary trajectory of many species. This is even greater concern as genes conveying more biologically active compounds (e.g. pharmaceuticals) are being engineered into plants.

With these few examples, it becomes evident that a multidisciplinary framework for understanding the biology and ecology of GMOs is necessary for adequate risk assessment. A real world situation where risk assessments should be carried out is illustrated in the case of transgenic contamination of maize landraces in Mexico.

3. Mexican maize and GMOs

In 2000, transgenic DNA was found in native varieties of maize in Southern Mexico (QUIST & CHAPELA 2001). Subsequent work has confirmed the presence of transgenic DNA in landraces of maize in Mexico (ALVEREZ MORALES 2002; QUIST & CHAPELA 2002) at a scale much broader than previously thought. This introgression is of concern because Mexico is the centre of diversity for this important crop species. It is where breeders go back time and time again to obtain new genetic stock for the improvement of maize for future generations.

Should we be concerned that transgenes are in the native strains of maize? Does the presence of transgenic DNA negatively affect fitness and decrease this important source of genetic diversity? A thorough modeling study by HAYGOOD et al. (2003) of recurrent transgene flow into wild relative populations suggests so. They found that genetic assimilation, and demographic swamping can occur in 10’s of generations, in not only favoured but also for disfavoured crop genes.

Yet hard empirical evidence is lacking on significance of transgenic DNA introgression into Mexican maize. Currently, there are NO published generalisable studies that address the how transgene expression, or even transgenic presence, effects the fitness of individuals or populations.

Studies are necessary that:

• Considers populations from an ecological perspective at different levels of organization and interfaces



• Compare fitness effects with conventional isogenic lines replicated over space and time



• Examine effects of different genetic backgrounds and environmental stresses

4. Conclusions

One certainty in the study of transgenic organisms, particularly within molecular ecology, is that GMOs are quite a bit more complicated than we had previously thought. In all areas of biology, the more questions we ask, the more we become aware of the inherent complexity and interconnectedness of biological systems over many levels of organization. Given this complexity, an ecological approach, e.g. transgene ecology, provides the kind of integrative and holistic framework useful for investigating the impacts of transgenesis of our ecosystems. This approach can also better prepare us for filling gaps of knowledge in the biology of transgenes.

The Central Dogma of genetics, genetic determinism, inadequately reflects the current knowledge on the biology and ecology of GMOs, and needs to be revised. Transgene ecology provides an expanded and flexible framework as a basis for incorporating evolving information over multiple fields of study and modes of inquiry. To evaluate and communicate research on GMO safety more effectively, a more inclusive and standardized system, which recognizes areas of ignorance and uncertainties, and also provides a framework for methodological validity will be necessary.

In his provocative book, Degrees of Freedom (1997), Alan RAYNER reminds us:

Along with how we understand transgenic biology, what we value and evaluate in GMO risk assessment, will be crucial to a more comprehensive and accurate assessment of GMO safety.

Lastly, in the common goal of ensuring the safety of technologies (such as GMOs) for human welfare, the environment and food safety, we must insist on the highest scientific standards and knowledge to be applied in order to make sound judgements of risk. Therefore, if developer-derived scientific information is used for regulatory approval or risk assessment, we must require that it be peer-reviewed. This is currently not the case. Without such reviews by independent scientists in the field of specialization addressed, the accuracy and usefulness of these studies cannot be ascertained, obviating their utility in risk assessment. All of these efforts to improve the science used in GMO risk assessments will require greater transparency, humility, and goodwill amongst scientists and policymakers, and the political will to make sound decisions in an uncertain future. By utilizing an ecological approach, such as transgene ecology, complex issues in the risk assessment of GMOs seem much more manageable and possible.

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CITATION:Quist D (2004). Transgene ecology: An ecological perspective for
GMO risk assessment. In: Breckling B & Verhoeven R (eds) Risk Hazard
Damage - Specification of criteria to assess environmental impact of genetically
modified organisms. Bonn, Bundesamt für Naturschutz. Naturschutz und
Biologische Vielfalt 1:239-244