Introgression from genetically modified plants into wild relatives
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Weeds are mainly an agricultural problem and not an environmental one, requiring adequate management practices in the field to be dealt with. The other main concern is with the displacement of related plants in the wild or the introgression of transgenes into those wild relatives, principally in centres of origin. One of the questions being debated is whether the introgression of a transgene into wild relatives could cause loss of biodiversity at all or be different in any way from traditionally bred commercial varieties.
Rice paddies harbour a plethora of organisms, including algae, microorganisms, beneficial insects, and sometimes commercially utilised crayfish. To maintain this diversity it is important to develop agronomical practices that minimise the use of biocidal compounds. Due to this difficulty in flowering, breeders have to manipulate environmental conditions in order to make effective crosses Matsuoka et al. However, in recent studies, some botanists have classified some Brazilian native plants from the Erianthus genus as belonging to the Saccharum genus: S.
Since very little is known about the biology of these plants, studies are required to check the likelihood of gene flow among these species. Overall, the breakout group agreed that inter and intraspecific gene flow associated with sugarcane poses no significant concerns for the environmental risk assessment. In this case, the PF would lead to a conclusion that no more data need to be collected for an ERA for this crop. The insertion of glyphosate tolerance in sugarcane may lead to the appearance of sugarcane volunteer plants in the field if inadequate management is performed.
This can happen due to the current use of glyphosate by growers to eradicate crop ratoons after planting ends, and as such poses a significant stewardship consideration for herbicide tolerant sugarcane. This does not mean that the GM sugarcane with tolerance to glyphosate will become weedier, since it will not have more ability to spread than the conventional variety for example: more seeds, more dormancy, presence of rhizomes, etc.
However, farmers should be aware that it will not be possible to use glyphosate to eliminate transgenic plants with tolerance to this herbicide and would need to adapt their cultural practices to the GM variety. Sugarcane Non-target Arthropods. Although there is no commercial release of a transgenic sugarcane variety, there is extensive experience and knowledge of non-GM sugarcane cultivation, which provides the essential biological and agronomic baseline information for PF. In addition, the data available from other GM crops already in the market with the same integrated traits can be used, allowing regulators to focus on the species that are unique to sugarcane and have not been studied yet.
In this manner, it is known that Bt genes have effect on a limited range of insects and that Cry2A affects only lepidopteran insects, making unnecessary to study a broad range of NTAs. It was suggested at the workshop that the impact of the transgenic variety on the population of ants should be studied. Ants belong to the order Hymenoptera, and some species are considered to be important to Brazilian sugarcane plantations because they act as predators for herbivorous pests.
However, the group recognized that, based on available information, it is expected that Cry2A should have no activity on hymenoptera at expected environmental concentrations Thus, it seemed reasonable to expect negligible risk. So, the conclusion was that the impact of GM sugarcane expressing Cry2 protein on ant populations should be discussed further, taking into consideration the insect biology and all the possible exposition pathways.
An appropriate testable risk hypothesis that is linked to a credible causal pathway leading to harm should be drawn. Without this plausible hypothesis, the specificity of Cry2A may limit the relevance and need for further studies. Sugarcane Additional Issues. Another important issue when dealing with an asexually propagated crop such as sugarcane is that the introduced trait is not easily passed to other varieties by the breeding programs.
For sugarcane, it is even more difficult because of the complexity of the genome D'hont ; Piperidis and D'hont On the other hand, there is a need for different varieties of sugarcane in order to satisfy seasonal operation needs from the mills and the different environmental conditions that the culture is cultivated. All this combined creates a challenge to regulators worldwide: how to evaluate new events of the same crop with the same construction? Without precedents, it is uncertain what kind of data this simplified analysis will require. The conclusions at the meeting were that all the data from risk assessment of the first variety approved should be used with the inclusion of the following data:.
These GM varieties are intended to be planted in Brazil, and their main products ethanol and sugar are commodities that are intended to be used for internal consumption and for exportation. Thus, the question of how the commercial release of different events of the same construction in sugarcane is going to happen is not only a concern for Brazilian regulators but also for regulators from countries importing Brazilian GM sugarcane products. Although the exported Brazilian ethanol is almost completely intended to be used as biofuel, sugar is a product for human consumption.
So, this can also raise questions about the food safety of this product and it is a problem that should be formulated and tested. On the other hand, the presence of DNA or Bt proteins at sugar and also at ethanol is expected to be negligible due to their high processing. There is a lot of knowledge on sugarcane biology that has not been published and remains with the professionals that advise sugarcane growers.
It is necessary to mine this knowledge base in order to have a complete package of information for the risk assessment prior to the commercial release of a GM sugarcane variety. The conclusions of the workshop include:. Andow, D. Ecological risk assessment for Bt crops. Nature Biotechnology Barroso, P. Freire, J. Amaral J. Brett, P.
Flowering and pollen fertility in relation to sugarcane breeding in Natal. Craig, W. Tepfer, G. An overview of general features of risk assessmenrts of genetically modified crops. Euphytica Cross, F. Paradoxical perils of the precautionary principle.
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Law Rev. Cytogenet and Genome Res Duan, J. Marvier, J. Huesing, G. Freire, E. Distribuicao, coleta uso e preservacao das especies silvestres de algodao no Brasil. Algodao, Embrapa. Garcia-Alonso, M. Jacobs, A. Raybould, T. Nickson, P. Sowig, H. Willekens, K. Van der, R. Layton, F. Amijee, A. Fuentes, and F.
A tiered system for assessing the risk of genetically modified plants to non-target organisms. Haygood, R. Population genetics of transgene containment. Ecology Letters 7: Hilbeck, A. James, C. Johnson, K.
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Raybould, M. How does scientific risk assessment of GM crops fit within the wider risk analysis? Trends Plant Sci. Keese, P. Risks from GMOs due to horizontal gene transfer. Environmental Biosafety Research 7: Matsuoka, S. Hibridacao em cana-de-acucar. Borem, ed. Hibridacao Artificial de Plantas. Vicosa: Editora UFV. Moore, P. Studies on sugarcane pollen II Pollen storage. Phyton Argentina Flowering and flower synchronization. In: Heinz DJ Ed.
Amsterdam: Elsevier The biology of Saccharum spp.
Transgene introgression from genetically modified crops to their wild relatives
Environmental risk assessment: tasks and obligations. Human and Ecological Risk Assessment 4: Piperidis, G. Chromosome composition analysis of various Saccharum interspecific hybrids by genomic in situ hybridization GISH. Popper, K. Objective Knowledge: an Evolutionalry Approach. Oxford University Press. Rao, P. Raybould, A. Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops. Plant Science Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops. Roach, B. A review of the origin and improvement of sugarcane.
Romeis, J. It can therefore be the source of resistance to these stresses, as has been reviewed by de Lange et al. Resistance to biotic stresses in teosinte has been well documented. Nault and Gordon found Z. Kling et al. In addition, abiotic stress resistance is also easy to find in teosinte. Zea luxurians , Z.
Teosinte should possess useful functional variation to improve maize traits that are not immediately apparent or easily measured in a teosinte background , including improved nutritional quality Melhus, ; Swarup et al. This has provided proof that useful phenotypic variation can be tapped from teosinte for maize improvement. Despite arguments to the contrary, it is also known that introgression occurs in maize via gene flow from teosinte and is an ongoing process in the center of origin Warburton et al.
Tropical maize populations introgressed with various traits from teosinte have been created, including resistance to striga Striga hermonthica ; Menkir et al. In addition, various desirable characteristics have been transferred into maize by substituting three of the maize chromosomes with three chromosomes from Z.
However, finding documentation of even one trait present in a temperate maize hybrid currently on the market in the United States has been extremely elusive. It has been repeatedly cautioned that teosinte has been vastly underused for the improvement of maize because the time and uninterrupted effort needed is very high; however, the possibility of eventual discovery of unique and useful alleles is great Goodman ; Goodman et al. The reduced use of wild Zea and related species for crop improvement is reflected by an underutilization of exotic maize landraces, the majority of which are adapted to tropical and subtropical growing environments.
Although they have been found to contain much more sequence diversity than elite US temperate maize germplasm, the use of exotic maize parents in temperate breeding programs is very rare. The Germplasm Enhancement of Maize GEM project is one systematic and largescale effort to move useful sequence diversity from exotic to elite maize breeding populations Salhuana and Pollak, Many other projects have also used exotic sources to create populations with higher levels of important traits, including drought stress resistance Meseka et al.
Increased sequence variation in tropical maize may be higher because a second bottleneck occurred when maize moved from Mexico into more northern climates in the United States, and also because gene flow between tropical maize and sympatric teosinte continues to bring in new variation from maize CWR Warburton et al. Thus, tropical maize could be used as a bridge between temperate breeding pools and maize CWR. Several biological challenges have been given as reasons that wild Zea species or Z. These include photoperiod sensitivity; division of tropical and temperate maize in their adaptation, and the fact that most landraces and all CRW are tropical; carefully balanced heterotic patterns into which most elite maize is assigned, and which introgression of exotic germplasm would disturb; and the very high yield demanded by growers, which is generally suppressed, if only for a few generations, by genetic drag during introgression.
Introgression of a few genes, with a quick return to the background of the recurrent parent, avoids the problems associated with a complete mixing. However, since most agronomically important traits are under the control of many genes, this may not be a successful breeding option unless a few quantitative trait loci QTLs or genes have a larger effect on the phenotype.
Gain from selection in the mixed germplasm pools have been demonstrated to continue for these quantitative traits Albrecht and Dudley, and can be expected to eventually surpass the performance of the original exotic or elite populations. This would take many generations, however, which the need for a quick return on investment or research grant-imposed deadlines may not allow.
The identification of useful variation from teosinte can also be slowed by a lack of genetic resources in which to study this variation, particularly for quantitative traits that cannot be estimated for breeding purposes in a teosinte background including most yield, ear, kernel, and plant morphology traits. However, the recent release of near-isogenic introgression lines NILs from 10 Z. Linkage analysis of the newest NILs have already identified positive alleles from teosinte on traits including male flowering time, number of kernel rows, and kernel weight in maize Liu et al.
Researchers have suggested methods to introgress useful traits from teosinte into maize breeding pools, including sequential backcrosing Casas-Salas et al. Generating largescale genomic information from cereal CWR is now much more economical than ever, and much progress has already been made in sequencing and resequencing CWR to date, including studies published by Brozynska et al.
Using sequence information to guide introgression for genomic regions known to be associated with useful traits will make this process very efficient, with negligible linkage drag from outside genomic regions of interest. This should allow minimal perturbation of heterotic groups and yield potential of the resulting backcrossed progeny.
It may also be possible to use maize wild relatives in a less direct manner to tap the allelic diversity necessary to incorporate new traits. If a beneficial allele can be found in an exotic source, including landraces or wild species, the sequence information itself may be sufficient to seek the same allele in a much more closely related temperate maize line and introgress it into the elite breeding pool via marker-assisted backcrossing, thus eliminating the potential for genetic drag from wide crosses.
Alternatively, if this sequence diversity does not exist in elite maize breeding pools, it may still be possible to use the allele information from exotic sources to guide improvement in the elite temperate genome. Once the precise genomic region is identified via genetic mapping or other genomic, proteomic, or metabolomic studies of landraces or wild species, the causal mutation defining the beneficial allele from the exotic source can be characterized.
If the sequence change is small, this information can be used to improve elite breeding lines via genome editing. Although the method is less straightforward, the resulting improved line may be more acceptable to large private companies who would also control the intellectual property of the line.
Useful phenotypic variation and vast sequence variation exist in the CWR of both sunflower and maize. In both species, this variation has often been successfully transferred to experimental interspecific populations, but linkage drag has made the resulting hybrids not immediately useful. Rounds of intermating or backcrossing, followed by selection against traits brought in unintentionally, has been necessary to create acceptable breeding lines. This is simplified in the case of qualitative or oligogenic traits, which can be introgressed quickly and with a minimum of linkage drag via marker-assisted backcrossing.
In the case of quantitative traits, population-level selection is generally required and is a slower process. The development and extensive characterization of genetic resources consisting of backcrossed interspecific populations can benefit many researchers simultaneously, and the sharing of all the characterization data will make the work more efficient. Taking this process through the research stage all the way to the release of new cultivars is slow but has been done successfully on many occasions in sunflowers and with significant economic impacts.
It would appear that the constraints on the use of maize CWR have been greater than those on sunflowers, as maize breeders have never successfully transferred allelic variation from CWR to a final commercial product for temperate growing areas.
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In fact, it would appear on the surface that insurmountable biological obstacles are preventing the use of the vast array of useful diversity from teosinte and other related Zea species in maize breeding, but that these obstacles are either much smaller, or have somehow been overcome, in sunflowers. It is true that many sunflower CWR evolved in temperate growing conditions, whereas all maize CWR are tropically adapted, and that cultivated sunflowers and maize grown in the United States and Europe are temperate.
Nevertheless, on closer inspection, the real constraints in maize turn out to be logistical, economical, and habit driven. No biological constraint has been identified to date that would not be easily overcome with time and long-term financial support. Time and funding for such activities have been lacking in largescale temperate maize breeding, however, which values the fastest time to new cultivar release and profitability.
To date, sufficient allelic diversity has been present to allow continued gain from selection in temperate maize breeding pools, although this may change at any time; given the evolution or introduction of a new disease agent or abiotic constraint, the risk has not yet been given sufficient weight in the private industry to change current breeding schemes.
Sunflowers may have benefited from the diversity available in CWR partly because the industry does not operate on the razor-thin profit margins that maize growers face, especially since maize is so heavily cultivated in the United States that supply is almost always equal to and sometimes exceeds demand, driving down prices and profits. Thus, tiny reductions in yield in new sunflower cultivars would not spell financial ruin for sunflower growers as it may in maize, especially if the new cultivars were substantially better in other respects.
These possible yield reductions, caused by linkage drag from wild relatives and removable over time, will also be compensated in a bad growing year if varieties with robust biotic and abiotic stress resistance genes from CWR are able to withstand future epidemics of new diseases or environmental stresses from a changing environment.
Genomics approaches may help level the field between maize and sunflowers by more efficiently tapping diversity from CWR while reducing or eliminating linkage drag more quickly. Sharing of sequence and gene identification data is necessary for the most efficient transfer of sequence diversity or sequence information from maize CWR to elite populations, but this is not the norm in private industry. In sunflowers, a major portion of the breeding effort is still done in the public sector, and more open sharing of information may be a factor in the successful use of CWR for sunflower improvement in comparison with maize.
The difference in the use of transgenic technology in maize versus sunflower may also be causing a difference in the use of CWR in the two species. To date, there has been little focus on transgenic work in sunflowers, because the primary centers of production and breeding are outside of the United States, in countries where there is strong resistance to the release of transgenic cultivars. The opposite is true of maize, where the United States is the leading global producer and breeder of maize, and the vast majority of the acreage in the United States is now planted to transgenic maize.
Traits found in CWR and backcrossed into cultivated material may not lend themselves to intellectual protection as easily as traits inserted into a cultivar via transgenesis, which may encourage the use of GMOs by for-profit companies where possible.
The cost of funding a program to identify and introgress CWR-derived genetic variation into modern elite maize would be a tiny fraction of the cost of a single failed harvest season in the United States. Particularly for traits where sufficient sequence variation does not exist in the domesticated gene pool, investment in the identification and transfer of new sequence variation from CWR is long overdue.
The consequence of a narrow genetic base in maize has been demonstrated on a large scale during the Southern Corn Leaf Blight of in the United States. The genetic base of US commercial maize has narrowed even further in the intervening 45 yr, leaving the nation even more vulnerable to a new epidemic and decreased yield due to more difficult and less predictable maize growing environments.
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The potential cost of increased genetic vulnerability is smaller than the cost of reducing this vulnerability. Sunflower CRW will continue to be sources of important traits, including diverse cytoplasmic male sterility, increased oil content, and disease resistance; these efforts must continue. The authors thank Sherry Flint Garcia, H. Thomas Stalker, and Major M. Goodman for thoughtful review and excellent suggestions for the manuscript. Editorial Board. Subscription Questions. Skip to main content.
Email Address. Password Forgot My Password. Reset your password. View My Binders. View Comments. This article in CS Vol. Published: June 16, Proper attribution is required for reuse. No permissions are needed for reuse unless it is derivative or for commercial purposes. Printer-friendly PDF. Marilyn L. Abstract Conservation of crop wild relatives CWR has always been predicated on the promise of new and useful traits, and thus modern genetics and genomics tools must help fulfill the promise and continue to secure the conservation of these resources.
Breeding material developed from the introgression of wild traits into cultivated sunflower. Phenotypic diversity for plant type as seen in various teosinte and maize entries. Evaluation of four maize populations containing different proportions of exotic germplasm. Crop Sci. Roles of interspecific hybridization and cytogenetic studies in sunflower breeding. Helia 27 : 1 — The challenges of maintaining a collection of wild sunflower Helianthus species. Crop Evol. Using genomic approaches to unlock the potential of CWR for crop adaptation to climate change.
Beard Germplasm resources of oilseed crops: Sunflower, soybeans, and flax. Genotypic and phenotypic characterization of isogenic doubled haploid exotic introgression lines in maize.
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