Escape! Crop-Specific Gene Flow to Wild Relatives

Written by Cody Cobb

As a molecular biologist, most of my work is done on a bench at or below room temperature. I can count on one hand the number of times I’ve been to a research field because I have more than two fingers. I’ve never taken a course in ecology, and I’ve rarely dealt with full, intact organisms. It is with just such a background that I absorbed a talk by Allison Snow at Rutgers ten days ago.
Snow* is an evolutionary biologist and ecologist who’s been running an interesting experiment on wild radishes for more than a decade now. In the 90’s, when transgenic crops like Bt corn and Roundup Ready soybean were beginning to dominant the market (and the landscape), there were concerns that wild relatives would incorporate the transgenes and spread as superweeds. Corn and soybean, with their lack of compatible relatives in the US, are exempt from this concern. However, as more and more transgenic crops with compatible relatives come down the pipeline (and with some, like canola, already here) there needs to be some hard data on just how easily transgenes can persist and spread in wild populations.

Domestic radish (Raphanus sativus), like nearly all domesticated crops, differs profoundly from its wild relative (Raphanus raphanistrum). The traits that make for a delicious ingredient in a salad often make for a wimpy competitor in the wild. Humans have been cultivating radishes for so long that some alleles are only found in the domestic varieties. In this 10 year long experiment, these crop-specific alleles served as surrogate transgenes in the sense that their presence in wild relatives had to have been the result of successful hybridization of crop and weed. Snow and collaborators chose as their genetic markers two allozymes, glucose-6-phosphate isomerase (GPI) and phosphoglucomutase (PGM), and the gene for petal color (R. sativus has white petals, the dominant allele, and R. raphanistrum has yellow petals, the recessive allele). Even though it’s typical for domestic traits to have a negative impact on fitness in the wild, no a priori assumptions were made about these specific alleles.

Four plots, each containing 100 wild radish plants and 100 wild/domestic F1 hybrids, were set up and more or less left to the devices of nature for ten years. Allele frequency at the start was 25% for all three markers, with 50% of all plants white-flowered owing to dominance. By the end of experiment, the percentage of plants with white flowers had dropped to 3-15%. Crop-specific GPI ranged from 5-12%, and crop-specific PGM declined the least with an allele frequency ranging 16-26%. As it turns out, the allele for white petals is linked to delayed flowering, a deleterious trait which seems to explain the precipitous drop in white-flowered plants in the second and subsequent years. Despite this selection pressure, the white flower allele persisted in all populations. The GPI crop allele behaved similarly, declining in frequency but never disappearing. The PGM crop allele was a little different, declining in frequency in only one population and remaining more or less the same in the other three.

What’s more, the first generation of F1 hybrids suffered from a significant disadvantage: only around 60% of their pollen was viable, compared to 80-95% viable pollen from the neighboring R. raphanistrum. And yet, despite this initial setback, each population eventually regained normal pollen fertility levels (> 70% fertile) while still retaining low-but-not-zero levels of crop-specific alleles.
So what kind of effects in the wild can we expect to see from transgenes based on this study? From the paper’s conclusion we’re warned:

Clearly, crop alleles can persist for many generations following a single hybridization event, and crop-wild hybrids may recover wild-type fitness in later generations. Thus, beneficial or neutral transgenes that recombine independently of deleterious crop alleles may spread and persist indefinitely (Snow et al., 2010).

A relevant example is her 2003 study on Bt sunflower, which found that the Bt transgene in cultivated sunflower (Helianthus annuus), when crossed into wild sunflower (also Helianthus annuus), allows each plant to produce, on average, 55% more seeds relative to non-transgenic controls under field conditions (Snow et al., 2003). Rather frustratingly, follow-up work was halted when the companies sponsoring the study — Pioneer Hi-Bred International and Dow AgroSciences — refused to allow further access to the transgene or the seeds since they decided not to sell Bt sunflowers anyway.

With all this in mind, what are some steps we genetic manipulators and tamperers can take to lower the risk of transgene flow into wild relatives? One thought is to link the transgene of interest with another gene that’s deleterious in the wild but tolerated or even desirable in agricultural situations. Better yet, find two such genes and flank the transgene. Creating such a construct would require a lot more work, not to mention the difficulty of finding appropriate crop-tolerant-but-wild-harmful genes. But then, it’s just a thought. What are yours?
*Astute readers of Tomorrow’s Table might recognize the name from a parenthetical citation on page 110: “For this reason, some ecologists see the application of GE as a way to spare even more land from destruction by enhancing yields (Qaim and Zilberman 2003; Snow et al. 2005).”
Snow, A., Pilson, D., Rieseberg, L., Paulsen, M., Pleskac, N., Reagon, M., Wolf, D., & Selbo, S. (2003). A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecological Applications, 13 (2), 279-286 DOI: 10.1890/1051-0761(2003)013[0279:ABTRHA]2.0.CO;2
Snow AA, Culley TM, Campbell LG, Sweeney PM, Hegde SG, & Ellstrand NC (2010). Long-term persistence of crop alleles in weedy populations of wild radish (Raphanus raphanistrum). The New phytologist PMID: 20122132

Written by Guest Expert

Cody Cobb is a brand new doctor, recovering plant biologist, and photography enthusiast. He received his MD at Texas A&M Health Science Center College of Medicine. Prior to medical school, he studied plant biology and plant pathology at Rutgers University.