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Scientific Article on Genetic Pollution of
Gene-Altered Crops

When Transgenes Wander, Should We Worry?

Norman C. Ellstrand; <ellstrand@ucrac1.ucr.edu> Professor of Genetics,
University of California, Riverside, California; Plant Physiol. 2001;
EDITOR'S CHOICE April 2001, Vol. 125, pp. 1543-1545

http://www.plantphysiol.org/cgi/content/full/125/4/1543

It is hard to ignore the ongoing, often emotional, public discussion of
the impacts of the products of crop biotechnology. At one extreme of the
hype is self-righteous panic, and at the other is smug optimism. While the
controversy plays out in the press, dozens of scientific workshops,
symposia, and other meetings have been held to take a hard and thoughtful
look at potential risks of transgenic crops. Overshadowed by the loud and
contentious voices, a set of straightforward, scientifically based
concerns have evolved, dictating a cautious approach for creating the best
choices for agriculture's future.

Plant ecologists and population geneticists have looked to problems
associated with traditionally improved crops to anticipate possible risks
of transgenic crops. Those that have been most widely discussed are: (a)
crop-to-wild hybridization resulting in the evolution of increased
weediness in wild relatives, (b) evolution of pests that are resistant to
new strategies for their control, and (c) the impacts on nontarget species
in associated ecosystems (such as the unintentional poisoning of
beneficial insects; Snow and Palma, 1997; Hails, 2000).

Exploring each of these in detail would take a book, and such books exist
(e.g. Rissler and Mellon, 1996; Scientists' Working Group on Biosafety,
1998). However, let us consider the questions that have dominated my
research over the last decade to examine how concerns regarding engineered
crops have evolved. Those questions are: How likely is it that transgenes
will move into and establish in natural populations? And if transgenes do
move into wild populations, is there any cause for concern? It turns out
that experience and experiments with traditional crops provide a
tremendous amount of information for answering these questions.

The possibility of transgene flow from engineered crops to their wild
relatives with undesirable consequences was independently recognized by
several scientists (e.g. Colwell et al., 1985; Ellstrand, 1988; Dale,
1992). Among the first to publish the idea were two Calgene scientists,
writing: "The sexual transfer of genes to weedy species to create a more
persistent weed is probably the greatest environmental risk of planting a
new variety of crop species" (Goodman and Newell, 1985). The movement of
unwanted crop genes into the environment may pose more of a management
dilemma than unwanted chemicals. A single molecule of DDT
[1,1,1,-trichloro-2,2-bis(p-chlorophenyl)ethane] remains a single molecule
or degrades, but a single crop allele has the opportunity to multiply
itself repeatedly through reproduction, which can frustrate attempts at
containment.

In the early 1990s, the general view was that hybridization between crops
and their wild relatives occurred infrequently, even when they were
growing in close proximity. This view was supported by the belief that the
discrete evolutionary pathways of domesticated crops and their wild
relatives would lead to increased reproductive isolation and was supported
by challenges breeders sometimes have in obtaining crop-wild hybrids.
Thus, my research group set out to measure spontaneous hybridization
between wild radish (Raphanus sativus), an important California weed, and
cultivated radish (the same species), an important California crop
(Klinger et al., 1991). We grew the crop as if we were multiplying
commercial seed and surrounded it with stands of weeds at varying
distances. When the plants flowered, pollinators did their job. We
harvested seeds from the weeds for progeny testing. We exploited an
allozyme allele (Lap-6) that was present in the crop and absent in the
weed to detect hybrids in the progeny of the weed. We found that every
weed seed analyzed at the shortest distance (1Ým) was sired by the crop
and that a low level of hybridization was detected at the greatest
distance (1Ýkm). It was clear, at least in this system, that crop alleles
could enter natural populations.

But could they persist? The general view at that time was that hybrids of
crops and weeds would always be handicapped by crop characteristics that
are agronomically favorable, but a detriment in the wild. We tested that
view by comparing the fitness of the hybrids created in our first
experiment with their non-hybrid siblings (Klinger and Ellstrand, 1994).
We grew them side by side under field conditions. The hybrids exhibited
the huge swollen root characteristic of the crop; the pure wild plants did
not. The two groups did not differ significantly in germination, survival,
or ability for their pollen to sire seed. However, the hybrids set about
15% more seed than the wild plants. In this system, hybrid vigor would
accelerate the spread crop alleles in a natural population.

When I took these results on the road, I was challenged by those who
questioned the generality of the results. Isn't radish probably an
exception? Radish is outcrossing and insect pollinated. Its wild relative
is the same species. What about a more important crop? What about a more
important weed? We decided to address all of those criticisms with a new
system. Sorghum (Sorghum bicolor) is one of the world's most important
crops. Johnsongrass (Sorghum halepense) is one of the world's worst weeds.
The two are distinct species, even differing in chromosome number, and
sorghum is largely selfing and wind pollinated. Sorghum was about as
different from radish as you could get.

We conducted experiments with sorghum paralleling those with radish. We
found that sorghum and johnsongrass spontaneously hybridize, although at
rates lower than the radish system, and detected crop alleles in seed set
by wild plants growing 100Ým from the crop (Arriola and Ellstrand, 1996).
The fitness of the hybrids was not significantly different from their wild
siblings (Arriola and Ellstrand, 1997). The results from our
sorghum-johnsongrass experiments were qualitatively the same as those from
our cultivated radish-wild radish experiments. Other labs have conducted
similar experiments on crops such as sunflower (Helianthus annus), rice
(Oryza sativa), canola (Brassica napus), and pearl millet (Pennisetum
glaveum; for review, see Ellstrand et al., 1999). In addition, descriptive
studies have repeatedly found crop-specific alleles in wild relatives when
the two grow in proximity (for review, see Ellstrand et al., 1999). The
data from such experiments and descriptive studies provide ample evidence
that spontaneous hybridization with wild relatives appears to be a general
feature of most of the world's important crops, from raspberries (Rubus
idaeus) to mushrooms (Aqaricus bisporus; compare with Ellstrand et al.,
1999).

When I gave seminars on the results of these experiments, I was met by a
new question: "If gene flow from crops to their wild relatives was a
problem, wouldn't it already have occurred in traditional systems?" A good
question. I conducted a thorough literature review to find out what was
known about the consequences of natural hybridization between the world's
most important crops and their wild relatives.

Crop-to-weed gene flow has created hardship through the appearance of new
or more difficult weeds. Hybridization with wild relatives has been
implicated in the evolution of more aggressive weeds for seven of the
world's 13Ýmost important crops (Ellstrand et al., 1999). It is notable
that hybridization between sea beet (Beta vulgaris subsp. maritima) and
sugar beet (B.Ývulgaris subsp. vulgaris) has resulted in a new weed that
has devastated Europe's sugar production (Parker and Bartsch, 1996).

Crop-to-wild gene flow can create another problem. Hybridization between a
common species and a rare one can, under the appropriate conditions, send
the rare species to extinction in a few generations (e.g. Ellstrand and
Elam, 1993; Huxel, 1999; Wolf et al., in press). There are several cases
in which hybridization between a crop and its wild relatives has increased
the extinction risk for the wild taxon (e.g. Small, 1984). The role of
hybridization in the extinction of a wild subspecies of rice has been
especially well documented (Kiang et al., 1979). It is clear that gene
flow from crops to wild relatives has, on occasion, had undesirable
consequences.

Are transgenic crops likely to be different from traditionally improved
crops? No, and that is not necessarily good news. It is clear that the
probability of problems due to gene flow from any individual cultivar is
extremely low, but when those problems are realized, they can be doozies.
Whether transgenic crops are more or less likely to create gene flow
problems will depend in part on their phenotypes. The majority of the
"first generation" transgenic crops have phenotypes that are apt to give a
weed a fitness boost, such as herbicide resistance or pest resistance.
Although a fitness boost in itself may not lead to increased weediness,
scientists engineering crops with such phenotypes should be mindful that
those phenotypes might have unwanted effects in natural populations. In
fact, I am aware of at least three cases in which scientists decided not
to engineer certain traits into certain crops because of such concerns.

The crops most likely to increase extinction risk by gene flow are those
that are planted in new locations that bring them into the vicinity of
wild relatives, thereby increasing the hybridization rate because of
proximity. For example, one can imagine a new variety that has increased
salinity tolerance that can now be planted within the range of an
endangered relative. It is clear that those scientists creating and
releasing new crops, transgenic or otherwise, can use the possibility of
gene flow to make choices about how to create the best possible products.

It is interesting that little has been written regarding the possible
downsides of within-crop gene flow involving transgenic plants. Yet a
couple of recent incidents suggest that crop-to-crop gene flow may result
in greater risks than crop-to-wild gene flow. The first is a report of
triple herbicide resistance in canola in Alberta, Canada (MacArthur,
2000). Volunteer canola plants were found to be resistant to the
herbicides Roundup (Monsanto, St. Louis), Liberty (Aventis, Crop Science,
Research Triangle Park, NC), and Pursuit (BASF, Research Triangle Park,
NC). It is clear that two different hybridization events were necessary to
account for these genotypes. It is interesting that the alleles for
resistance to Roundup and Liberty are transgenes, but the allele for
Pursuit resistance is the result of mutation breeding. Although these
volunteers can be managed with other herbicides, this report is
significant because, if correct, it illustrates that gene flow into wild
plants is not the only avenue for the evolution of plants that are
increasingly difficult to manage.

The second incident is a report of the Starlink Cry9C allele (the one
creating the fuss in Taco Bell's taco shells) appearing in a variety of
supposedly nonengineered corn (Callahan, 2000). Although unintentional
mixing of seeds during transport or storage may explain the contamination
of the traditional variety, inter-varietal crossing between seed
production fields could be just as likely. This news is significant
because, if correct, it illustrates how easy it is to lose track of
transgenes. Without careful checking, there are plenty of opportunities
for them to move from variety to variety. The field release of "third
generation" transgenic crops that are grown to produce pharmaceutical and
other industrial biochemicals will pose special challenges for containment
if we do not want those chemicals appearing in the human food supply.

The products of plant improvement are not absolutely safe, and we cannot
expect transgenic crops to be absolutely safe either. Recognition of that
fact suggests that creating something just because we are now able to do
so is an inadequate reason for embracing a new technology. If we have
advanced tools for creating novel agricultural products, we should use the
advanced knowledge from ecology and population genetics as well as social
sciences and humanities to make mindful choices about to how to create the
products that are best for humans and our environment.

Acknowledgments: This article was written while I was receiving support
from the U.S. Department of Agriculture (grant no. 00-33120-9801). I thank
Tracy Kahn for her thoughtful comments on an earlier draft of the
manuscript and Maarten Chrispeels for his encouragement and patience.

Literature Cited
* Arriola PE, Ellstrand NC (1996) Crop-to-weed gene flow in the genus
Sorghum (Poaceae): spontaneous interspecific hybridization between
johnsongrass, Sorghum halepense, and crop sorghum, S.Ýbicolor. Am J Bot
83: 1153-1160
* Arriola PE, Ellstrand NC (1997) Fitness of interspecific hybrids in the
genus Sorghum: persistence of crop genes in wild populations. Ecol Appl 7:
512-518
* Callahan P (2000) Genetically altered protein is found in still more
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