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Persistence of genetically engineered canola populations in the U.S. and the adventitious presence of transgenes in the environment [1]

['Steven E. Travers', 'Department Of Biological Sciences', 'North Dakota State University', 'Fargo', 'North Dakota', 'United States Of America', 'D. Bryan Bishop', 'Department Of Biology', 'Concordia College', 'Morehead']

Date: 2024-06 

Feralization of genetically engineered (GE) crops increases the risk that transgenes will become integrated into natural and naturalizing plant populations. A key assumption of the management of GE crops is that populations of escaped plants are short-lived and therefore the risks they pose are limited. However, few populations of escaped crop plants have been tracked over the long term so our understanding of their persistence in ruderal or natural landscapes is limited. We repeated a large-scale road survey of feral GE canola populations in North Dakota, USA, initially conducted in 2010. Our objectives in 2021 were to determine the current distribution of feral canola populations, and to establish the relative frequency of GE and non-GE phenotypes in populations of canola throughout North Dakota. Our results indicate that, although the incidence of feral canola was less in 2021 than 2010, escaped canola populations remain common throughout the state. The prevalence of alternate forms of GE herbicide resistance changed between surveys, and we found an overabundance of non-GE plants compared to the frequency of non-transgenic forms in cultivation. Indirect evidence of persistence includes sampling plants with multiple transgenic traits, and finding populations far from transportation routes. We conclude that feral canola populations expressing transgenic herbicide resistance are established outside of cultivation, that they may be under selection for loss of the transgene, but that they nonetheless pose long-term risks by harboring transgenes in the unmanaged landscape.

Introduction

The adventitious presence of transgenes in production systems continues to pose significant risks to U.S. agriculture. Detection of transgenes in foodstuffs has disrupted international and domestic markets, stalled supply chains, and created mistrust among consumers [1]. Durisin and Wilson [2] estimated that the threat of contamination of conventional and organic crops by genetically engineered (GE) varieties cost producers $6.3B US when food companies and foreign markets rejected transgene-contaminated supplies. Limiting the movement of transgenes in agricultural systems is central to reducing market losses, but such efforts are frustrated by the biology of plants and their ability to out-maneuver containment strategies. Numerous crop species have escaped cultivation and established persistent populations outside of cultivation [3]. Outside of managed croplands, escaped crops may evolve rapidly to become more closely adapted to, and tolerant of the non-agronomic environment [4]. Once established, they constitute a gene pool capable of generating weedy pests that carry the additional risks of harboring beneficial transgenes [5]. The risks of an adventitious presence, then, are enhanced when GE crop species escape cultivation to form stable, naturalized populations in the unmanaged landscape.

De-domestication, or feralization, of GE crops increases the likelihood that transgenes will escape cultivation and integrate with wild populations of closely related plants. De-domestication is an evolutionary process by which domesticated plants or animals escape intensive management by humans to form independent reproducing populations [3]. De-domesticates are known to originate from within crop species through multiple routes: through mutation and selection (endo-ferals), by crossing between distinct populations or land races (exo-endo ferals), or by hybridizing with wild relatives (exoferals) [3]. Once established, the genetic architecture of de-domesticated populations may be further shaped by hybridization and introgression among wild, feral, and domesticated forms [6–8]. Wild traits, such as seed-shattering, asynchronous flowering and seed dormancy, are at times quickly recovered by de-domesticates as a product of selection in non-agronomic habitats [4]. The resulting feral populations, now more closely adapted to local environments and tolerant of competition, are rich targets for ongoing gene flow from agricultural fields [9]. When they compete with related crops, or introduce deleterious traits to commercial fields, de-domesticates pose a threat to the integrity and profitability of commercial production systems.

Among domesticated species, kohl crops have an evolutionary history punctuated with repeated bouts of feralization, hybridization and introgression [8, 10, 11]. Canola (Brassica napus L.) (2n = 4n = AACC) is a hybrid of B. rapa (2n = 20, AA) and B. oleracea (2n = 18, CC) [12]. It has become one of the most important oilseed crops worldwide and has been cultivated extensively for more than 100 years [13]. It is thought to have been domesticated recently (within the last 300–400 years) [14]. Populations of domesticated canola growing outside of cultivation have been reported from Belgium, Austria, Denmark, France, Germany, U.K., Australia, the Netherlands, and New Zealand [1]. “Wild” traits still expressed in commercial canola, such as seed shattering, may contribute to its ready escape from cultivation [1]. Moreover, canola seeds retain partial dormancy and may remain viable in the soil seedbank for up to three years [15, 16]. The combined effects of seed loss on harvest and seed dormancy rapidly stock the soil seed bank, contributing to the high incidence of volunteer canola in and around agricultural fields [17, 18].

The U.S. was an early adopter of GE canola in the mid-1990s and now nearly all U.S. canola is GE [19]. In 2011, we described the presence of escaped GE herbicide resistant (GE HR) canola populations North Dakota, USA, where most of the U.S. canola is grown. More than 75% of the plants sampled from roadside populations were GE HR and most populations contained a mixture of GE HR phenotypes, either glyphosate resistance or glufosinate resistance [20]. (Both GE HR and non-GE plants are referred to here as feral.) The source of these populations has yet to be determined, but it was generally believed they result from seed spill during transportation [21]. We repeated the survey in 2021 with the objectives to:

Determine the current distribution of feral canola populations in North Dakota, USA

Establish the relative frequency of GE HR traits in North Dakota populations

Investigate the distribution and frequency of non-GE plants in roadside samples

Between census periods, U.S. production of canola increased, with a reported increase in the cultivation of glufosinate resistant varieties. Therefore, if seed spill is the dominant factor maintaining feral canola populations, as has been argued [21, 22], we anticipate an increase in the number and size of feral populations, and a change in the phenotypic profile of feral populations.

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[1] Url: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0295489

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