ISB NEWS REPORT
NOVEMBER 2011
Biotic and Abiotic Stress Tolerance in Transgenic Plants:
Greater Gene Flow and Fitness?
C. Neal Stewart, Jr.
Even before the first transgenic crops were commercialized over 15 years ago, regulators and scientists raised questions
about the effects of transgenes that move from agricultural fields into wild and weedy populations of crop relatives.
When I first studied the magnitude and consequences of crop-to-wild transgene flow in 1994, I thought it was an interesting topic that would result in an interesting career of positive important data; i.e., gene flow would be a significant
environmental risk. That is to say, my initial expectation was that biotic-stress-tolerance proteins, such as those conferred
by insecticidal Bacillus thuringiensis crystal endotoxin (Bt cry) genes, would enhance fitness to their host plants—both
crop and wild × crop hybrids.
While my initial expectation proved to be false, it has nonetheless been interesting. Indeed, there was a fitness boost
observed in Bt canola (Brassica napus)1, a crop that has a wild relative, wild turnip/birdseed rape (Brassica rapa), that
hybridizes easily with canola2,3. However, in nature, few plant species are observed to produce interspecific hybrids and
even fewer species produce stably introgressed hybrids4. This is also the case for B. rapa and B. napus—few introgressed
hybrids have been observed in nature and only one instance of a transgenic introgressed hybrid has been observed—this
single plant was a backcrossed B. rapa plant harboring a glyphosate-resistance transgene originally from B. napus5.
These worst case transgene flow scenarios—the ones that many scientists and regulators originally feared—have
not come to pass; the reasons why are still unknown6. One possible explanation could be the genetic hitchhiking effect
of crop genes linked with wild relatives4,6,7. Yet, gene flow to wild relatives is still a regulatory and scientific concern. A
recent scientific workshop held at the Lorentz Center at the University of Leiden (the Netherlands) had a title that comprises the key question “Transgenes Going Wild?” (http://www.lorentzcenter.nl/lc/web/2011/451/info.php3?wsid=451)
in which several presentations showed results from computer simulations of these hitchhiking effects.
Despite the unfounded dire potential ecological effects of transgenes running wild6, there are legitimate regulatory
and biosafety concerns about biocontainment of certain types of transgenes and in certain plant species. Among these are
abiotic stress-tolerance transgenes, such as those that confer water, salt, cold, and nutrient stress8,9. For example, cold tolerant semi-tropical transgenic trees could conceivably become adapted to new temperate environments and displace current species if they were to spread beyond plantations. If this were to occur, it would be considered a potential ecological
disruptor. On the other hand, drought tolerant transgenic grasses could increase the productivity of biofuel feedstocks
and allow higher biological productivity and carbon sequestration on marginal and even xeric lands that are not currently
wild; a positive ecological effect. It is clear that each case of novel transgenes and crops will need to be studied during
risk assessments, but clearly abiotic stress tolerance could have great value to crop agriculture and it is being pursued by
all the major crop agriculture companies.
A recent study led by professor Jarmo Holopainen and graduate student (now postdoc) Sari Himanen at the University of Kuopio in Finland analyzed a much different scenario than those posed by direct biotic- or abiotic- stress tolerance
transgenes10. They asked questions pertaining to the effect that a biotic stress tolerance gene, in this case a Bt cry1Ac
transgene, might have on ozone tolerance relative to gene flow effects in future climates. At first blush this scenario
might seem to be contrived, but under global climate change scenarios, there are many potential biotic and abiotic-stress
interactions that have been documented in the literature, especially related to volatile organic compounds11.
Four genotypes of Brassica plants were compared in ozone-injected plant growth chambers: Bt canola; non-transgenic
canola; non-transgenic B. rapa; and a transgenic Bt BC2F2 backcross to B. rapa hybrid. Cytogenetically the BC2F2 hybrid
plants are indistinguishable from B. rapa—each with 20 chromosomes—in contrast with the 38 chromosome count of
canola. Under elevated ozone (100 ppb) experiments conducted in these plant growth chambers, hybrids seemed to be as
sensitive to foliar ozone damage as B. rapa and had equivalent fecundity. However, B. rapa had a stronger compensatory
response than all the other genotypes, including the transgenic hybrids. This compensation—allocating more resources
toward seed production—would likely allow B. rapa to outcompete crop and hybrid alike in unmanaged ecosystems, an
effect observed in another study12 that did not include a transgene factor.
B. rapa along with other weedy and wild species have evolved the ability to respond to damage of all sorts by increasing resource allocation to seed production. Therefore, a Bt protein that confers the protection of leaves against damage may not play a significant role in the fitness of wild plants. We might conclude then that Bt and other transgenes that
ISB NEWS REPORT
NOVEMBER 2011
offer the services of plant protection will likely not alter population dynamics of their wild plant hosts. Indeed, it appears
that transgenes face significant difficulties passing through the backcrossing hybridization bottleneck (i.e., F1, BC1, BC2,
BC3, etc.) so that the transgene (or any gene) now resides in stable introgressed wild or weedy genetic backgrounds4,7.
Although the transgene had a neutral effect in this study, transgenic plants provide good models for the study of plant
responses to changing environments. Indeed, since many wild plants are much more susceptible to ozone damage than
their crop relatives13, it might be that if ozone-tolerance transgenes are moved into crops, that such genes could boost the
fitness of their wild relatives to a greater extent than in the crops.
References
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Stewart CN Jr, All JN, Raymer PL, and Ramachandran S. Increased fitness of transgenic insecticidal rapeseed under insect selection pressure. Mol Ecol
6,773-779 (1997)
Metz PLJ, Jacobsen E, Nap JP, Pereira A, and Stiekema WJ. The impact of biosafety of the phosphinothricin tolerance transgene in inter-specific B. rapa
× B. napus hybrids and their successive backcrosses. Theor Appl Genet 95, 442–450 (1997)
Halfhill MD, Millwood RJ, Raymer PL, and Stewart CN Jr. Bt-transgenic oilseed rape hybridization with its weedy relative, Brassica rapa. Environ Biosafety Res 1, 19-28 (2002)
Stewart CN Jr, Halfhill MD, and Warwick SI. Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4, 806-817
(2003)
Warwick SI, Legere A, Simard MJ, and James T. Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy
Brassica rapa population. Mol Ecol 17, 1387–1395 (2008)
Kwit C, Moon HS, Warwick SI, and Stewart CN Jr. Transgene introgression in crop relatives: molecular evidence and mitigation strategies. Trends Biotechnol 29, 284-293 (2011)
Rose CW, et al. Genetic load and transgenic mitigating genes in transgenic Brassica rapa (field mustard) × Brassica napus (oilseed rape) hybrid populations. BMC Biotechnol 9, 93 http://www.biomedcentral.com/1472-6750/9/93/ (2009)
Warwick SI, Beckie HJ, and Hall LM. Gene flow, invasiveness, and ecological impact of genetically modified crops. Ann NY Acad Sci 1168, 72–99 (2009)
Beckie HJ, Hall LM, Simard M-J, Leeson JY, and Willenborg CJ. A framework for postrelease environmental monitoring of second-generation crops with
novel traits. Crop Sci 50, 1587–1604 (2010)
Himanen SJ, Nerg A-M, Poppy GM, Stewart CN Jr, and Holopainen JK. Abiotic stress and transgenics: implications for reproductive success and crop-wild
gene flow in Brassicas. Basic Appl Ecol 11, 513-521 (2010)
Yuan JS, Himanen S, Holopainen JK, Chen F, and Stewart CN Jr. Smelling climate change: plant volatile organic compounds in changing environments.
Trends Ecol Evol 24, 323-331 (2009)
Black VJ, Stewart CA, Roberts JA, and Black CR. Ozone affects gas exchange, growth and reproductive development in Brassica campestris (Wisconsin
Fast Plants). New Phytol 176, 150–163 (2007)
Davison AW, and Barnes JD. Effects of ozone on wild plants. New Phytol 139, 135–151 (1998)
C. Neal Stewart, Jr.
Department of Plant Sciences
University of Tennessee
Knoxville, TN, USA 37996
[email protected]