Increased Longevity and Dormancy of Soil-Buried Seeds from Advanced Crop–Wild Rice Hybrids Overexpressing the EPSPS Transgene

Estimating the fitness effect conferred by a transgene introgressed into populations of wild relative species from a genetically engineered (GE) crop plays an important role in assessing the potential environmental risks caused by transgene flow. Such estimation has essentially focused on the survival and fecundity-related characteristics measured above the ground, but with little attention to the fate of GE seeds shattered in the soil seed banks after maturation. To explore the survival and longevity of GE seeds in soil, we examined the germination behaviors of crop–wild hybrid seeds (F4–F6) from the lineages of a GE herbicide-tolerant rice (Oryzasativa) line that contains an endogenous EPSPS transgene hybridized with two wild O. rufipogon populations after the seeds were buried in soil. The results showed significantly increased germination of the GE crop–wild hybrid seeds after soil burial, compared with that of the non-GE hybrid seeds. Additionally, the proportion of dormant seeds and the content of the growth hormone auxin (indole-3-acetic acid, IAA) in the GE crop–wild hybrid seeds significantly increased. Evidently, the EPSPS transgene enhances the survival and longevity of GE crop–wild rice seeds in the soil seed banks. The enhanced survival and longevity of the GE hybrid seeds is likely associated with the increases in seed dormancy and auxin (IAA) by overexpressing the rice endogenous EPSPS transgene. Thus, the fate of GE seeds in the soil seed banks should be earnestly considered when assessing the environmental risks caused by transgene flow.

Environmental variation and its effect on the success of crop-wild hybridization in the Raphanus species complex

Hybridization has been suggested as mechanism that can contribute to adaptive evolution and the success of crop-wild hybrid populations; but this response appears to depend upon environmental context. I explore how environmental variation affects crop trait expression, the strength and direction of selection on crop traits in radish weed populations, and the influence environmental variation has on crop-trait introgression across agricultural landscapes. Using the Raphanus crop-wild complex as a model system to study the environmental sensitivity of crop gene flow into weed populations, I first planted advanced-generation wild and crop-wild hybrid radish plants (that had previously evolved for three generations under relatively dry, relatively wet, or ambient control soil moisture or water-evolved conditions) into sheltered common gardens that were watered with low, ambient, or high soil moisture. From this work, hybridization and watering history did not enhance the success of advanced-generation hybrid plants relative to wild progenitors in Ontario, Canada. Next, I explored how phenotypic plasticity in response to environmental variation may distort a commonly used metric to measure the rate of evolution, the haldane. To determine the extent that plasticity affected estimates of evolutionary rate, I compared haldane estimates of advanced-generation water-evolved plants grown in a common garden that did not involve manipulation of ambient watering conditions. Estimates of the magnitude and direction of contemporary evolution differed significantly due to annual environmental variation, particularly for wild populations. Thus, I propose changes to the use of these equations and changes to the equation itself to help avoid generating false estimates of evolutionary rates. Finally, a meta-analysis of radish phenology and fecundity data collected from the last twelve years across four locations revealed that geography can affect the strength and direction of selection on crop- derived traits in weedy radish populations. This large, integrated study offers environmental risk assessment a new perspective on the role of environmental change on the success of crop-wild hybridization and its ability to generate weedy species. In summary, I provide evidence that environmental variation should be considered before making predictions about a crop trait’s evolutionary trajectory and persistence in a weedy plant population.

Environmental variation and its effect on the success of crop-wild hybridization in the Raphanus species complex

Hybridization has been suggested as mechanism that can contribute to adaptive evolution and the success of crop-wild hybrid populations; but this response appears to depend upon environmental context. I explore how environmental variation affects crop trait expression, the strength and direction of selection on crop traits in radish weed populations, and the influence environmental variation has on crop-trait introgression across agricultural landscapes. Using the Raphanus crop-wild complex as a model system to study the environmental sensitivity of crop gene flow into weed populations, I first planted advanced-generation wild and crop-wild hybrid radish plants (that had previously evolved for three generations under relatively dry, relatively wet, or ambient control soil moisture or water-evolved conditions) into sheltered common gardens that were watered with low, ambient, or high soil moisture. From this work, hybridization and watering history did not enhance the success of advanced-generation hybrid plants relative to wild progenitors in Ontario, Canada. Next, I explored how phenotypic plasticity in response to environmental variation may distort a commonly used metric to measure the rate of evolution, the haldane. To determine the extent that plasticity affected estimates of evolutionary rate, I compared haldane estimates of advanced-generation water-evolved plants grown in a common garden that did not involve manipulation of ambient watering conditions. Estimates of the magnitude and direction of contemporary evolution differed significantly due to annual environmental variation, particularly for wild populations. Thus, I propose changes to the use of these equations and changes to the equation itself to help avoid generating false estimates of evolutionary rates. Finally, a meta-analysis of radish phenology and fecundity data collected from the last twelve years across four locations revealed that geography can affect the strength and direction of selection on crop- derived traits in weedy radish populations. This large, integrated study offers environmental risk assessment a new perspective on the role of environmental change on the success of crop-wild hybridization and its ability to generate weedy species. In summary, I provide evidence that environmental variation should be considered before making predictions about a crop trait’s evolutionary trajectory and persistence in a weedy plant population.

Context-specific enhanced invasiveness of Raphanus crop–wild hybrids: A test for associations between greater fecundity and population growth

Campbell, L. G., Teitel, Z., Miriti, M. N. and Snow, A. A. 2014. Context-specific enhanced invasiveness of Raphanus crop–wild hybrids: A test for associations between greater fecundity and population growth. Can. J. Plant Sci. 94: 1315–1324. Evolution by crop–wild hybridization may create plant lineages with greater population growth rates, dispersal, and persistence than weedy progenitors, depending upon plant density. We asked: (1) how does hybridization affect demography and population growth rate (lambda, λ) and (2) how does density affect demography and λ? Over 1 yr, we followed wild radish, Raphanus raphanistrum and crop-wild hybrid, Raphanus sativus×R. raphanistrum, plants grown in 18 experimental sub-populations (originally derived from three wild and three hybrid populations) to assess contributions of germination, survival, and seed production to λ. We explored genotypic differences in demographic characteristics of low- and high-density populations (from populations grown at unmanipulated densities for three generations), using a LTRE. Hybrid populations had greater λs than weedy progenitors when grown in low (but not high) densities. Seed production was more influential on λ than germination or survival, and seed mortality was least influential. Our results indicate weedy Raphanus populations may be best controlled by limiting seed production, rather than killing plants outright or preventing seeds from germinating. Furthermore, relative invasiveness of genotypes is density-dependent, low-density conditions improving potential invasiveness of hybrid populations. We emphasize that assessing invasive potential of a plant will be more successful if one uses a comprehensive demographic approach accounting for a weed's entire life history.