Risk assessment of GM plants: avoiding gridlock?
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ARTICLE IN PRESS TRPLSC 41
Opinion TRENDS in Plant Science Vol.not known No.not known Month 0000 1
Risk assessment of GM plants:
avoiding gridlock?
Mike J. Wilkinson1, Jeremy Sweet2 and Guy M. Poppy3
1
School of Plant Sciences, The University of Reading, Whiteknights, Reading, UK RG6 6AS
2
Environmental Research, National Institute of Agricultural Botany, Huntingdon Road, Cambridge UK CB3 0LE
3
School of Biological Sciences, University of Southampton, Bassett Crescent East, UK SO16 7PX
Cultivation of genetically modified crops is presently arising from some GM cultivars [7– 9]. Predicting detri-
based largely on four crops containing few transgenes mental impact becomes more challenging as the diversity
and grown in four countries. This will soon change and of GM releases grows and will be particularly difficult for
pose new challenges for risk assessment. A more struc- transgenes that fundamentally change plant physiology
tured approach that is as generic as possible is advo- (e.g. lignin content and drought tolerance). However, it
cated to study consequences of gene flow. Hazards is important to distinguish between unwanted environ-
should be precisely defined and prioritized, with mental changes attributable to a transgene and those
emphasis on quantifying elements of exposure. This caused by other aspects of a dynamic agro-environment.
requires coordinated effort between large, multidisci- Indeed, the absence of quality ‘baseline data’ on environ-
plinary research teams. mental change caused by farm practice, land use, con-
ventional or mutation breeding or by the importation of
Commercial cultivation of genetically modified (GM) crops exotics for gardening is something that warrants atten-
increased 35-fold from 1.7 Mha in 1996 to 58.7 Mha in tion. The purpose of this article is to draw attention to
2002, with soybean, cotton, maize and rapeseed occupying forthcoming problems relating to the release of future GM
. 99.9% of the area sown (http://www.isaaa.org). Just four crops and to propose a more generic strategy for RISK
countries currently account for 99% of GM hectarage ASSESSMENT (see Glossary).
(USA, Argentina, Canada and China), although the total
number of countries involved increases steadily. Trans- Developing a new way to assess risk
genes for herbicide tolerance and insect resistance pre- RISK is defined by the formula: risk ¼ f (HAZARD , exposure).
dominate, with 98% of GM cultivars containing one or both The hazard term represents the severity of the unwanted
types (http://www.isaaa.org). This situation is also about to change and often relates to a defined species. This element
change globally with the recent explosion of information
on gene identity and function. These data have spawned
a new generation of GM lines with a staggering array Glossary
of applications [1] (http://www.olis.oecd.org/biotrack.nsf). Bitrophic interaction An interaction between two species representing
For economic reasons, many of these new constructs different functions in a foodchain or food web, such as a plant and an insect
herbivore.
will never be released commercially. However, the trend
Exposure pathway A sequential series of intermediate events leading to the
towards commercial transgene diversification is illus- realization of a hazard.
trated by the presence of traits such as reduced nicotine Exposure tree A series of connected exposure pathways relating to different
hazards arising from the same crop.
content, altered fruit ripening, resistance to various Exposure The probability that a defined hazard will occur.
viruses and altered oil profiles among GM lines approved F1 hybrid formation Creation of an initial hybrid between the GM crop and the
by the United States Department of Agriculture, Animal wild recipient.
Gene flow Movement of a (trans)gene by pollen or seed.
and Plant Health Inspection Services (USDA, APHIS) for Hazard Potential of an agent or situation to cause an adverse effect.
deregulation (generally a precursor of commercialization) Introgression Stable transfer of transgene from the genetic background of the
in the USA (http://www.aphis.usda.gov/bbep/bp/petday.html crop into the genetic background of the recipient species by repeated
hybridization to the recipient species.
on 21 February 2003). Construct complexity is likewise Risk assessment Process of evaluation, including the identification of the
expanding following numerous advances in the control of attendant uncertainties, of the likelihood and severity of an adverse effect(s) or
event(s) occurring to the environment following exposure under defined
transgene expression [2 –4]. Overall then, we expect more conditions to a transgenic plant.
GM cultivars grown over a wider area and containing a Risk A function of the probability and severity of an adverse effect or event
broader array of transgenes, expressed in various ways. occurring to the environment following exposure, under defined conditions, to
a transgenic plant.
These developments should radically increase the adapt- Transgene spread Dispersal of transgene by seed, vegetative propagule or
ability of farming, with benefits to farmers and, in some pollen from the population of initial hybrid formation and into other
cases, to the environment [5,6]. Conversely, there are legi- populations of the recipient species.
Tritrophic interaction An interaction between three species representing
timate concerns over possible environmental consequences different functions in a food chain or food web such as a plant, an insect
herbivore and a predator or parasitoid of the insect herbivore.
Corresponding author: Mike J. Wilkinson (m.j.wilkinson@reading.ac.uk).
http://plants.trends.com 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00057-8ARTICLE IN PRESS TRPLSC 41
2 Opinion TRENDS in Plant Science Vol.not known No.not known Month 0000
inevitably carries a degree of subjectivity and is usually
semi-qualitatively represented (e.g. severe, moderate or GM recipients significantly depress numbers of specialist
low). In essence, we define how unwanted the environ- herbivore in target region
mental change is. The exposure term represents the Resistance depresses herbivore feeding
probability that the hazard will occur and so is quantifi- Transgene spreads to most populations
able, provided the hazard is adequately defined. We quan-
tify the risk by combining a well-defined hazard with Infraspecific gene flow
probability of occurrence. Note that risk assessment in Transgene stabilizes in at least one recipient by introgression
this sense does not accommodate for ‘beneficial’ change
Backcrossing to recipient
because this is part of the risk communication process in
which cost–benefit analyses are considered (see EU report, F1 hybrids
http://europa.eu.int/comm/food/fs/sc/ssc/out83_en.pdf).
There are several routes by which a GM cultivar could Pollination, seed
impact on the broader environment. Quantifying risk is development and germination
made difficult by the many ways a transgene could influ-
Cultivar A GM crop Cultivar B
ence the ecology of a recipient and associated organisms.
Publications seeking to describe such scenarios can be TRENDS in Plant Science
categorized as ‘hazard identification’ studies [10] and
Fig. 1. Elements of exposure are arranged as a pathway to examine the probability
include the well-publicized work of John Losey and col- of population decline of a specialist herbivore feeding on a genetically modified
leagues [11]. These workers highlighted the possibility (GM) crop relative after transgene recruitment. Two scenarios are presented:
that Bt-containing maize pollen deposited on milkweed cultivar A has insect resistance alone but cultivar B also has a terminator construct
to depress hybrid formation. Arrow size indicates probability of reaching the sub-
leaves (Asclepias spp.) could depress survivorship of sequent step in the exposure pathway (indicated in text box). Purple text next to
feeding monarch butterfly (Danaus plexippus) larvae the arrows denotes the biological process leading to step completion. Note a high
such that the abundance of the insect declines. Having probability of hazard realization in cultivar A but a negligible probability for
cultivar B after adjusting for hybridization repression by the terminator construct.
defined the hazard, subsequent works systematically
quantified the probability that the hazard would occur
[12 – 14]. These are termed ‘exposure studies’. A combi-
nation of hazard identification and exposure evaluation different hazard. All pathways ultimately root to the crop
allowed for a rapid assessment of risk [15]. It was con- and usually share early stages in common. An attractive
cluded that although the hazard is significant, exposure is strategy for assembling exposure data of generic value is
so small that the risk of monarch population decline is therefore to focus first on the generic base of the EXPOSURE
negligible. In most instances, the relationship between TREE and progress towards the hazards. In the case of
crop and hazard is more complex and so risk assessment gene flow to wild relatives (Fig. 1), the first stage is the
would be more protracted. Furthermore, as diversity of formation of F 1 HYBRIDS , followed by INTROGRESSION , gene
GM cultivars grows, the number of associated hazards spread and other exposure elements relating to various
might become too numerous for all to be identified and categories of hazards. In assembling exposure trees from
assessed at a rate that keeps pace with submissions. the basal node upwards, it should be possible to prioritize
Unstructured hazard identification under these circum- research towards classes of hazard and recipients with the
stances can favour the obvious or dramatic rather than highest probability of occurrence within a targeted geo-
those likely to cause large-scale environmental conse- graphic area. Importantly, it should therefore be possible
quences. We therefore propose that a structured approach to discount groups of hazards or even crops in a region
be adopted for hazard prioritization and risk assessment on the basis of a negligible cumulative exposure along a
such that new information is as generic as possible. To shared pathway. It is also possible to accommodate for
some extent, this is a formalization of the approach already measures that reduce exposure (Fig. 1). Final steps of
adopted by some regulatory bodies but, in addition, we an exposure pathway (after TRANSGENE SPREAD ) require
advocate that data be assimilated in a coordinated fashion separate attention. Here, we suggest the most appropriate
to provide information on the relevant geographic scale strategy is to work backwards from the hazard using a
for legislation. progressive ‘tiered experimental approach’. Viewed in
For consequences of GENE FLOW, the proposed strategy combination, both these strands allow unlikely hazards
focuses first on the exposure term so that consideration can to be rapidly eliminated and enable detailed information
be limited to those crop – location combinations with more generated by focused research efforts to be integrated in a
than a negligible probability of transgene establishment in holistic manner. This procedure means that prolonged
wild relatives. Exposure can be divided into a series of research is restricted to hazards with a significant like-
steps in a sequential pathway. The pathway must be lihood of occurrence.
completed for the hazard to be realized (e.g. Fig. 1).
Exposure is therefore quantified as the cumulative prob- Case study of gene flow from GM oilseed rape
ability of completing the pathway. If the cumulative Brassica napus (rapeseed) to Brassica rapa gene flow is
probability approximates to zero at any point in the perhaps the best-characterized system for risk assess-
pathway, then the risk of hazard realization is negligible. ment. Here, we examine the gene flow exposure pathway
However, for any GM crop there is a complex tree of between these species, considering hazards caused by
interconnected EXPOSURE PATHWAYS , each leading to a mono- and BITROPHIC (plant – plant and plant– herbivore)
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or more complex TRITROPHIC (involving plant –herbivore – to describe the rate and pattern of gene exchange between
parasitoid) interactions between introgressed GM B. rapa recipient populations must take account of the life history
and other organisms. Exposure follows the order: F1 hybrid of the recipient as well as separation and genetic differen-
formation, introgression, transgene spread, mono-, bi- and tiation between populations. Whichever statistical approach
tritrophic interactions. We consider data at the national is employed to infer gene spread between populations,
scale for maximum relevance for regulation. efforts should ultimately aim to develop spatially explicit
models based on the distribution of the recipient.
Exposure steps leading to transgene spread
F1 hybrid formation: two components are required to Exposure steps leading to hazard realization
estimate UK hybrid abundance – ‘local’ hybridization at The later stages in the exposure pathway can lead directly
sites of co-occurrence and long-range hybridization. Local to hazard realization. There is currently no data relating to
hybridization is affected by the ecology of B. rapa, which these elements for rapeseed B. rapa. The decision to evalu-
grows occasionally as a ruderal or weed and frequently on ate these exposure steps could be based on the outcome of
riverbanks. These settings present divergent exposure the gene flow and spread evaluations above. In the absence
profiles for hybridization. In each case, we need first to of such data, we advocate a precautionary stance in which
quantify hybrid abundance when donor and recipient are transgene recruitment and spread is assumed. Priorities
coincident, and then the frequency of coincidence. Esti- should then be assigned to final exposure steps leading to
mates of hybrid seed formation are available for both weed hazards deemed of greatest ecological importance. Inter-
[16,17] and riverbank B. rapa [18], although seed dormancy, actions at the first, second and third trophic levels (Fig. 2)
fitness and crop rotation should be considered before should be examined using a tiered system of experimen-
attempting to infer hybrid plant frequency. To date, we tation (Fig. 3) [10,27]. In this approach, hazards are
are unaware of any suitable empirical observations of identified during first-tier laboratory experiments under
F1 hybrid plant abundance that would provide the best ‘worst-case scenario’ conditions. Progression to larger-
estimate of this element of exposure. Data are also lacking scale experiments in higher tiers aims to provide increas-
for the frequency of coincidence at the national scale, ingly refined estimates of exposure and thus quantification
although Mike Wilkinson and colleagues [19] used remote- of risk. Thus, the strategy is opposite to that used for gene
sensing-directed surveying to establish coincidence of flow, where exposure was measured before the hazard.
rapeseed and riverside B. rapa across SE England (UK). However, even when gene flow occurs, the ecological con-
Quantifying long-range hybridization is more problem- sequence of such gene movement needs to be measured
atic and inevitably involves spatially explicit modelling to assess the risks of geneflow. This allows simplification
using donor and recipient distributions, pollen dispersal in our proposed scheme because the consequence of
patterns, and the relationship between pollination and
hybrid frequency. Data are currently only available for
pollen dispersal [20]. Third trophic level
Introgression: F1 hybrids are triploid (2n ¼ 3x ¼ 29, (Predator or
AAC) but partially fertile [21]. Introgressive backcrossing parasitoid)
to B. rapa yields diploid plants within two backcross
generations [22]. The likelihood of a transgene becoming
stably introgressed into B. rapa is dependent upon inte-
gration site and plant reproductive success during intro- Second trophic
gression. There are two aspects of transgene integration level
site that need to be described. First, the degree of homeo- (Herbivore)
Tritrophic
logous pairing between A and C genomes during intro- interaction
gression, as this might or might not influence the probability
of transfer for transgenes on the C genome [23,24]. Second,
Bitrophic
the regions in the rapeseed genome that incur fitness costs interaction
by linkage drag during introgression. Appropriate data are
currently unavailable for either component. Reproductive
success and fitness during introgression can be inferred
from studies on weedy B. rapa [25,26] but are unavailable First trophic level
for riverside B. rapa. (Plant)
Transgene spread: weed populations are scattered,
effectively controlled in cereals and so generally only
flower in rapeseed. This means that populations are highly
Introgressed Inter- and Intraspecific
isolated in time and space, and are most likely to recruit GM recipient plant interaction
transgenes by local hybridization. Conversely, riverside
B. rapa are mostly separated from the crop, with few TRENDS in Plant Science
populations recruiting transgenes each year [19]. Here,
the capacity and extent of gene flow between populations Fig. 2. Possible levels of interaction between genetically modified (GM) recipient
wild species and other organisms. Interactions segregate into layers: monotrophic
will strongly affect the spread and ultimate distribution of (plant –plant interaction), bitrophic (plant– herbivore interaction) and tritrophic
transgenes. No data are currently available but any attempt (plant –herbivore– preditor or parasitoid).
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Tritrophic interactions: there are many possible tritro-
Risk quantification Third-tier phic interactions and any could lead to hazard realization.
Field studies These are too complex to consider collectively and although
three-way interaction studies are feasible, the complexity of
Second-tier
these interactions still dictates that studies are performed
Extended laboratory studies,
'semi-field' under controlled environments.
First-tier Conclusions
Laboratory studies, Risk assessment is entering a new phase. Increased
'worst case scenario' diversity of GM cultivars will create the need for an
Hazard identification
integrated approach to risk assessment. The concept of
TRENDS in Plant Science exposure trees has appeal in allowing case-by-case assess-
ments to focus on hazards that have high impact and
Fig. 3. A tiered risk-assessment scheme. First-tier experiments are conducted
strong likelihood of realization. This is important for both
to identify hazards in a ‘worst case-scenario’ and subsequent tiers are used to
quantify risk by introducing more realistic probability and exposure levels. scientific and public confidence. Current data on gene flow
and spread are either insufficiently integrated or of an
transgenes in wild relatives is only measured if it can occur inappropriate scale to predict the likelihood or extent of
and the impact can then be assessed via a tiered risk- transgene movement in a geographic region except in the
assessment scheme. More details on the use of tiered risk broadest of terms. The need for at least semi-quantitative
assessment are described elsewhere [10,27]. Thus, hazards estimates will nevertheless grow as new submissions
failing to realize under ‘worst case scenario’ conditions can include genetic elements to prevent or repress hybridiz-
effectively be disregarded. Failing this, some hazards might ation. Where widespread gene dispersal is deemed likely,
be eliminated as conditions become more similar to those attention turns towards the final exposure elements in the
encountered in the field. In this way, effort is focussed upon tree, working back from the hazard using a tiered strategy
hazards with the greatest likelihood of realization. of experimental design. This dual approach (from hybrid-
Mono- and bitrophic interactions: interactions between ization towards the hazard and from the hazard to assess
GM recipients and other organisms could cause hazard later elements of exposure) provides scope for rapid and
realization (e.g. decline of interacting organisms). Inter- systematic elimination of improbable hazards, thereby
actions can be plant– plant or plant– animal. Detailed life reducing tendency towards gridlock. However, in all cases,
history data of the recipient and associated flora collected precise definition of the hazard is of paramount importance.
in situ provides the best measure of plant– plant inter- The desire for risk assessment at the geographic scale
actions. Ideally, the aim would be to evaluate the extent to requires assimilation of mutually compatible datasets
which interactions such as competition impact on popu- from many scientific disciplines. This necessitates close
lation dynamics of cohabiting plants. In practice, inter- cooperation of diverse research teams. Although indepen-
pretation will be difficult and it is probably also desirable dent research efforts can be valuable for hazard identifi-
to perform ex situ competition experiments [28] in a con- cation and exposure assessment on a small scale, it is
trolled environment (first tier) and field (second tier). difficult to imagine integrating their findings to predict
Plant – herbivore interactions are more difficult to study outcomes reliably at the national or geographic scale. As
in situ because of herbivore mobility. Although surveying illustrated above, lack of coordination leads to gaps in
can be used to identify associated insects, heavy reliance knowledge. We therefore reason that there is a real need
must be placed on ex situ experimentation to provide for a move from the current practice of largely disparate
quantitative data relating to the nature and extent of research projects towards substantial, coordinated research
interaction. This is partly because the nature of change initiatives to produce generic datasets relating to the early
caused by interaction will be determined largely by stages of the exposure tree and to provide preliminary
transgene function. There is a choice between controlled exposure assessments for high-priority hazards. This will
a priori releases of a GM recipient (a ‘suck and see’ allow risk assessment to be more predictive, as is required
approach) and/or controlled experimentation. The a priori from robust risk-assessment schemes. We believe this can
releases yield the most appropriate data for exposure be achieved most effectively through cooperation between
quantification but controlled experimentation is the only funding bodies to ensure complimentarity in research
practical option in many cases. Where the GM intro- projects. It will also reduce the financial burden on com-
gressed recipients are unavailable, it might be preferable panies who will need to provide information more relevant
to mimic the action of the transgene. For example, the to the trait or crop in question, rather than unnecessarily
action of transgenes conferring insect resistance could be repeating measures of geneflow and its consequences.
mimicked by the targeted application of selective insecti-
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