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Genetically modified crops pass benefits to weeds

Herbicide resistance could confer an advantage on plants in the wild.

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Xiao Yang

Weedy rice can pick up transgenes from genetically modified crop rice through cross-pollination.

A genetic-modification technique used widely to make crops herbicide resistant has been shown to confer advantages on a weedy form of rice, even in the absence of the herbicide. The finding suggests that the effects of such modification have the potential to extend beyond farms and into the wild.

Several types of crops have been genetically modified to be resistant to glyphosate, an herbicide first marketed under the trade name Roundup. This glyphosate resistance enables farmers to wipe out most weeds from the fields without damaging their crops.

Glyphosate inhibits plant growth by blocking an enzyme known as EPSP synthase, which is involved in the production of certain amino acids and other molecules that account for as much as 35% of a plant’s mass. The genetic-modification technique — used, for instance, in the Roundup Ready crops made by the biotechnology giant Monsanto, based in St Louis, Missouri — typically involves inserting genes into a crop’s genome to boost EPSP-synthase production. The genes are usually derived from bacteria that infect plants.

The extra EPSP synthase lets the plant withstand the effects of glyphosate. Biotechnology labs have also attempted to use genes from plants rather than bacteria to boost EPSP-synthase production, in part to exploit a loophole in US law that facilitates regulatory approval of organisms carrying transgenes not derived from bacterial pests.

Few studies have tested whether transgenes such as those that confer glyphosate resistance can — once they get into weedy or wild relatives through cross-pollination — make those plants more competitive in survival and reproduction. “The traditional expectation is that any sort of transgene will confer disadvantage in the wild in the absence of selection pressure, because the extra machinery would reduce the fitness,” says Norman Ellstrand, a plant geneticist at the University of California in Riverside.  

But now a study led by Lu Baorong, an ecologist at Fudan University in Shanghai, challenges that view: it shows that a weedy form of the common rice crop, Oryza sativa, gets a significant fitness boost from glyphosate resistance, even when glyphosate is not applied.

In their study, published this month in New Phytologist1, Lu and his colleagues genetically modified the cultivated rice species to overexpress its own EPSP synthase and cross-bred the modified rice with a weedy relative.

The team then allowed the cross-bred offspring to breed with one another, creating second-generation hybrids that were genetically identical to one another except in the number of copies of the gene encoding EPSP synthase. As expected, those with more copies expressed higher levels of the enzyme and produced more of the amino acid tryptophan than their unmodified counterparts.

The researchers also found that the transgenic hybrids had higher rates of photosynthesis, grew more shoots and flowers and produced 48–125% more seeds per plant than non-transgenic hybrids — in the absence of glyphosate.

Making weedy rice more competitive could exacerbate the problems it causes for farmers around the world whose plots are invaded by the pest, Lu says.

“If the EPSP-synthase gene gets into the wild rice species, their genetic diversity, which is really important to conserve, could be threatened because the genotype with the transgene would outcompete the normal species,” says Brian Ford-Lloyd, a plant geneticist at the University of Birmingham, UK. “This is one of the most clear examples of extremely plausible damaging effects [of GM crops] on the environment.” 

The study also challenges the public perception that genetically modified crops carrying extra copies of their own genes are safer than those containing genes from microorganisms. “Our study shows that this is not necessarily the case,” says Lu.

The finding calls for a rethinking of future regulation of genetically modified crops, some researchers say. “Some people are now saying that biosafety regulation can be relaxed because we have a high level of comfort with two decades of genetic engineering,” says Ellstrand. “But the study shows that novel products still need careful evaluation.”

Journal name:
Nature
DOI:
doi:10.1038/nature.2013.13517

References

  1. Wang, W. et al. New Phytol. http://dx.doi.org/10.1111/nph.12428 (2013).

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  1. Avatar for Mary Mangan
    Mary Mangan
    A weed scientist has taken a hard look at the paper, and you might be interested to see the discussion over there: http://weedcontrolfreaks.com/2013/08/epsps-weedy-rice/
  2. Avatar for Ray Perkins
    Ray Perkins
    Molecular "Cane Toads?"
  3. Avatar for Sampo Smolander
    Sampo Smolander
    I read the original article, and Wang et al. measure fitness by (i) measuring photosynthesis in glasshouse-grown plants (ii) measuring seed germination on wet paper in petri dishes and (iii) growing plants in garden (grown 20 cm apart, fertilized, hand-weeding and insecticides applied). We probably can assume that the extra copies of EPSP synthase genes increase the metabolic throughput (by boosting some of the protein synthesis pathways) of the plants, and when grown in abundant light (20 cm apart, no shadowing and competition from neighbouring plants), water and nitrogen (grown in garden conditions, fertilized), it is plausible that these individual grow faster and larger. This is all that Wang et al. did and all that their article claims. The higher throughput capacity only comes into use if supplies of energy or raw materials are not bottlenecks. But the Nature News conclusion "effects of such modification have the potential to extend beyond farms and into the wild" and Brian Ford-Lloyd's conclusion "genetic diversity [of wild rice], which is really important to conserve, could be threatened because the genotype with the transgene would outcompete the normal species" are very much unsupported by the results of Wang et al. In the wild, seeds may need to germinate in more challenging conditions that wet paper on a petri dish, there may not be abundant light, nitrogen or water. So the EPSP synthase -boosted plants grow better in the garden. But maybe there is a good reason why the EPSP synthase levels are lower in the plants from the wild. Maybe something else is more valuable to them, something that helps in e.g. low-light photosynthesis, nutrient or water uptake in scarce conditions, or defence against insects. Maybe the wild EPSP levels are just optimal for growing in wild conditions and the plants with boosted EPSP synthase levels would have lower fitness in wild conditions. (I assume that the higher levels of the synthase don't come for free, but have a related metabolic cost that cannot then be used elsewhere). As Wang et al. only measured fitness in garden, not in the wild, the conclusions are unwarranted.
  4. Avatar for Ananyo Bhattacharya
    Ananyo Bhattacharya
    As far as I can see, we have not reached any definitive conclusions about what will happen in the wild. The article warns what -could- happen and the -possible- consequences of such transgene spread. The sentence that you cite is a direct quote from Brian Ford-Lloyd, a plant geneticist at the University of Birmingham, UK (as the article clearly notes), who was unoconnected with the current study. He goes on to say: “This is one of the most clear examples of extremely plausible damaging effects [of GM crops] on the environment.” If you take issue with -his- conclusions, why not contact him? ONe of the key findings here is that, contrary to what many have argued, transgenes -may- confer some value/advantages to wild species. At least, this is no longer something that can be ruled out.
  5. Avatar for Sampo Smolander
    Sampo Smolander
    A large part of the history of plant breeding has been about getting rid of traits that are beneficial in wild conditions, and replacing them with traits what would be detrimental in the wild. Grow short stem, and save more energy for the edible parts. Good for the farmer, detrimental in the wild when the shorter plant gets shadowed by others. Grow less roots, and put more energy in the edible parts. Good for the farmer, and the farmer provides irrigation and fertilization for the plant. Detrimental in the wild when you're responsible for harvesting much scarcer water and nutrient resources. Be tasty. Good for the farmer, and the farmer protects you from the insects. Detrimental in the wild, better to develop more bitter taste, against insects. This depends on your view of evolution, but in my view there are no ultimate solutions, there are usually no traits that would be beneficial in every environment. (However we can imagine traits what would be plain stupid in every environment, e.g. growing leaves underground.) Everything is a trade-off, and different solutions are optimal in different environments. "ONe of the key findings here is that, contrary to what many have argued, transgenes -may- confer some value/advantages to wild species." So based on my long story there is some ground to conjecture that the traits Wang et al. found to increase fitness in the protected, fertilized, irrigated garden environment could be detrimental to fitness in the wild environment. Your argument is, that because something was beneficial in environment A, it's sound to assume it to be maybe beneficial in environment B, too. My argument is that precisely because something was good in environment A, there is some ground to suspect that it might be detrimental in environment B. Also, natural mutations leading to higher levels of EPSP synthase have been observed in the wild, Wang et al. give some references. So if the wild species really benefited from that trait (when growing in the wild), I believe it would have been able to produce that trait on its own, too.
  6. Avatar for Ananyo Bhattacharya
    Ananyo Bhattacharya
    My principle point was that Nature News was NOT drawing the conclusions you'd ascribed to us. The sentence was a direct quote from an independent scientist who the reporter had contacted in good faith (no cherry picking etc). This is responsible reporting not sensationalism. I wanted to make this very clear as you had accused us drawing conclusions and making inferences that we had not.
  7. Avatar for Richard Smith
    Richard Smith
    I would argue that, while most of the article is fine and attributes the various statements appropriately, the title and first paragraph appear sensationalist. GM crops are a sensitive issue and deserve extra care in reporting. The title implies a much broader result than was found - this finding doesn't generalise at all. The first paragraph, I think, implies that this finding in itself suggests possible effects in the wild. That is not consistent with their results - they didn't test . Wild conditions are worth testing as a next step (and I'm surprised the authors didn't do that as part of the original expt). If particular bit were attributed to whoever claimed it, it would look less sensational on the part of Nature.
  8. Avatar for Sampo Smolander
    Sampo Smolander
    My apologies. I have edited my first post to attribute the Brian Ford-Lloyd quote to him.
  9. Avatar for Ananyo Bhattacharya
    Ananyo Bhattacharya
    Thanks. And thanks for the critique. I believe other plant scientists are discussing the paper including here http://www.biofortified.org/community/forum/general-genetics-group4/breeders-corner-forum13/herbicide-resistance-transgene-giving-fitness-advantage-thread372.0/ for example.
  10. Avatar for Ed Rybicki
    Ed Rybicki
    "Lu and his colleagues genetically modified the cultivated rice species to overexpress its own EPSP synthase and cross-bred the modified rice with a weedy relative. The team then allowed the cross-bred offspring to breed with one another..." I have a problem with this - and it lies in the fact that rice does not normally outbreed, so that their hybrids are lab-created and would not normally occur in natural conditions. Meaning they have shown what COULD happen, under ideal conditions, but not what WOULD happen.
  11. Avatar for Richard Smith
    Richard Smith
    As pointed out in the original paper, weedy rice (Oryza sativa f. spontanea) is the same species as cultivated rice (O. sativa), so this gene flow *is* expected.
  12. Avatar for Ursula Symmons
    Ursula Symmons
    I'm not a plant biologist, so might be wrong here, but in the original publication the authors claim that gene flow from rice to weedy rice has been reported, and that transgenes could spread to weedy rice within a few generations. Is this incorrect?
  13. Avatar for Ananyo Bhattacharya
    Ananyo Bhattacharya
    Actually Ursula, having checked with the scientists, Richard Smith is correct-weedy rice DOES breed with cultivated rice. So you would expect gene flow in this case. My comment below relates to GM maize and other GM crops where gene flow has not been firmly established. Thanks for the comment!
  14. Avatar for Richard Smith
    Richard Smith
    Confusion is understandable because other rice species are sometimes called 'weedy rice'. See the FAO page: http://www.fao.org/docrep/006/Y5031E/y5031e09.htm
  15. Avatar for Ananyo Bhattacharya
    Ananyo Bhattacharya
    I believe it is not well-established whether GM crops do or do not pass genes onto wild species. A feature published earlier this year (http://www.nature.com/news/case-studies-a-hard-look-at-gm-crops-1.12907), highlighted that transgene spread to wild crops remains controversial - though there are some reports of it happening. The study is important though as some have argued that even if transgenes DID spread, they're unlikely to give weeds a boost. This work would seem to challenge that assumption.
  16. Avatar for Sampo Smolander
    Sampo Smolander
    "Weedy rice, also known as red rice, is a species of rice (Oryza) that produces far fewer grains per plant than cultivated rice and is therefore considered a pest." (Wikipedia) And now from Wang et al.: "weedy rice produced 48–57% more seeds per plant than non-GE controls in pure monoculture plots, and 85–125% more seeds per plant in mixed plots, where direct competition favored the GE plants" So the rice - weedy rice hybrids produced more seeds (i.e. more rice) when they are "boosted" and outcompete the less seeds producing (thus more weedy), less boosted versions of hybrids. So are we here getting boosted weeds, or is the weedy rice boosted to produce more rice, and thus be less weedy and more alike the cultivated rice?
  17. Avatar for Richard Smith
    Richard Smith
    Please see my other comments: weedy rice in this case does not refer to a different species. It refers to a growth form of cultivated rice, O. sativa f. spontanea
  18. Avatar for Richard Smith
    Richard Smith
    Weedy rice (Oryza sativa f. spontanea) is the same species as cultivated rice (O. sativa), so this gene flow *is* expected.
  19. Avatar for Viktor Jakobsson
    Viktor Jakobsson
    Or more importantly, not what HAS happened, as the article header implicitly suggests. Nature news need to realize that this is a heavily politicized subject, thus, specialist attention is required before posting articles about GMOs.

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