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Genetic modification

Transgene introgression from genetically modified crops to their wild relatives

Nature Reviews Genetics volume 4, pages 806–817 (2003)Cite this article

Key Points

  • Introgression is the permanent integration of genes into a new genome through several generations of hybridization and backcrossing.

  • Like all genes, transgenes are subject to new selective pressures when they are transferred to another genome through hybridization. It is the new selective regime that determines whether or not transgenes will be stably introgressed.

  • The introgression of transgenes from sorghum to johnsongrass should be considered as a high risk. Crops of medium introgression risk are alfalfa, wheat, canola and sunflower.

  • Transgenes that confer herbicide tolerance will be intrinsically subject to high selective pressure in many agricultural environments, but selectively neutral outside cultivation. By contrast, other 'fitness enhancing' transgenes will have lower selective pressure in agricultural fields and variable selective advantage in nature.

  • Linkage disequilibrium (LD) is expected to be an important genomic characteristic with regards to the introgression of transgenes. If a transgene is integrated into a genomic region that is not normally subject to introgression, it would not be expected to introgress.

  • Strategies to decrease or prevent transgene introgression can manipulate selection using LD through transgene placement or engineering tandem transgenes. Biotechnological tools such as transplastomics, gene-use restriction technologies and male sterility can also be developed to decrease introgression in certain crops.

  • The risks of introgression for crops and transgenes should be assessed on a case-by-case basis. Ultimately, ecological and agronomical risk is determined more by transgene performance in a specific genomic location in a plant than by introgression per se.

Abstract

Transgenes engineered into annual crops could be unintentionally introduced into the genomes of their free-living wild relatives. The fear is that these transgenes might persist in the environment and have negative ecological consequences. Are some crops or transgenic traits of more concern than others? Are there natural genetic barriers to minimize gene escape? Can the genetic transformation process be exploited to produce new barriers to gene flow? Questions abound, but luckily so do answers.

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Figure 1: Transgene flow and potential transgene reservoirs.
Figure 2: Chromosomal blocks are the unit of selection in hybrid and introgression zones.
Figure 3: Genomic relationships among six crop species of Brassica.
Figure 4: Specific placement of transgenes in polyploid genomes might not be a barrier to introgression.

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Acknowledgements

We are grateful for support from the United States Department of Agriculture Boitechnology Risk Assessment Grants Program and the University of Tenessee Institute of Agriculture.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Tennessee, Knoxville, 37996, Tennessee, USA

    C. Neal Stewart Jr & Matthew D. Halfhill

  2. Agriculture and Agri-Food Canada, Eastern Cereal and Oilseeds Research Centre, K.W. Neatby Bldg., C.E.F., Ottawa, K1A OC6, Ontario, Canada

    Suzanne I. Warwick

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  1. C. Neal Stewart Jr
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  2. Matthew D. Halfhill
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Correspondence to C. Neal Stewart Jr.

Glossary

INTROGRESSION

The permanent incorporation of genes from one set of differentiated populations (species, subspecies, races and so on) into another.

LANDRACES

A crop cultivar that evolved with and has been genetically improved by traditional agriculturalists, but has not been directly influenced by modern breeding practices.

F1 HYBRIDIZATION

The initial cross between parent plants of different varieties, subspecies, species or genera.

BACKCROSSES

The mating of an individual with its parent, or with an individual of the same genotype as its parent, to follow the inheritance of alleles and phenotypes.

GENE FLOW

The dispersal of genes, in both gametes and zygotes, in and between breeding populations.

BC1 AND BC2 HYBRID

The offspring of a cross between a hybrid and one of the recurrent parent species or varieties. The subscript number represents the number of generations that have been crossed in this fashion.

HYBRID ZONES

(Hybrid swarms). Areas in which hybrid plants backcross to the parents and cross with themselves, so there is a continuous intergradation of forms in the population.

ISOZYME

Different forms of the same enzyme (synonymous with allozymes), which were used as some of the first biochemically-based genetic markers.

ALLOPATRIC

Occurring in geographically separate areas.

LINKAGE DISEQUILIBRIUM

(LD). A statistical measure of the non-independence of alleles. Departure from the predicted frequencies of multiple locus gamete types, assuming that all alleles are randomly associated.

CLINE

A variational trend in space that is found in a poulation, or a series of populations, of a species.

GENETIC LINKAGE MAP

A linear map of the relative positions of genes along a chromosome. Distances are established by linkage analysis, which determines the frequency at which two gene loci become separated during chromosomal recombination.

ELITE CROP VARIETIES

Agronomically desirable crop varieties that are widely used, adapted to local environments, perform well under intensive agricultural practices and are typically the product of intensive breeding.

SEED SHATTERING

Seeds dispersing from their fruits before harvest.

EXOTIC CROP VARIETIES

A variety that is from outside a breeding region or has traits that are uncommon to the prevalent crop variety.

FITNESS

The potential evolutionary success of a genotype, which is defined as the reproductive success or the proportion of genes that an individual leaves in the gene pool of a population. The individuals with the greatest fitness leave the largest numbers of offspring.

WIDE CROSSES

Hybridization between differentiated taxa.

MIGRATIONAL MELTDOWN

The theoretical state of gene flow that leads to the fixation of a 'bad' gene and the subsequent reduction of population size.

ECOTYPE

A genetic variety of a single species that is adapted for local ecological conditions.

HOMEOLOGOUS CHROMOSOME

A partially homologous chromosome, which usually indicates some original ancestral homology.

POLYPLOID

The genomic state of having three or more sets of homologous chromosomes (for example, tetraploid organisms, which have four sets of chromosomes).

FUNCTIONAL TRANSLATIONAL FUSION

The in-frame chimaera of two or more genes that gives rise to a single chimeric protein.

GENE USE-RESTRICTION TECHNOLOGY

(GURT). A biotechnological tool that controls embryo viability whereby the addition of a recoverable blocking sequence prevents some essential physiological function in a host plant and can be inducibly removed to recover viability.

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Stewart, C., Halfhill, M. & Warwick, S. Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Genet 4, 806–817 (2003). https://doi.org/10.1038/nrg1179

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