1 From Genetically Modified to Genome Edited Plants: The Global Context

The global production status of genetically modified (GM) crops has steadily grew since their commercial adoption in 1996, to reach a 112-fold increase [1] to around 190 million hectares in 2019, almost equally split between 21 developing countries and five industrial countries [2]. In terms of the share of the main crops in which transgenic traits have been commercialized, GM traits accounted for 47% of the global plantings to soybeans, maize, cotton, and canola in 2020 [3]. The global economic benefits, over the period 1996 to 2020, have been significant with farm incomes for those using the GM crop technology, having increased by 261.3 billion USD [4]. All the above are based on a sharp increase in the approval of the number of plant species with GM varieties. At global level, 44 countries, plus the European Union (EU) Member States (MS), have approved a total of 46 commercial GM traits introduced, as single or stacked transformation events, in 32 GM crop species for use in commercial cultivation, food, and feed.Footnote 1

Genome editing (GE) was being applied to more than 40 crops across 25 countries [5]. The GE plant varieties in advanced development pipeline span now a wide range of crops, including alfalfa, camelina, canola, citrus, flax, maize, pennycress, potato, lettuce, tomato, and watermelon, and are suggesting the flexibility of the new breeding techniques (NBTs) in crop improvement [6]. Despite the apparent potential, however, only six GE crop traits - in soybean, canola, rice, maize, mushroom and camelina - have been approved for commercialization to date [7]. The United States (US) farmers are growing from 2016 a oligonucleotide-directed mutagenesis (ODM)- based GE sulfonylurea tolerant weed control canola (Cibus), a transcription activator-like effector nucleases (TALEN)- based genome edited soybean with modified oil composition (Calyxt) [5] but also a Clustered Regularly Interspaced Short Palindromic Repeats -associated protein 9 (CRISPR–Cas9) edited waxy corn (Corteva Agriscience) [8]. The hectarage cultivated with Calyxt genome edited soybean alone has increased significantly, to approximately 40,000, from 17,000 in 2019 [5, 9]. The two genome editing pioneering companies, Cibus and Calyxt, have recently announced they had entered into a definitive merger agreement [10]. Genome edited food was first sold on the open market in 2021, when the Sicilian Rouge tomatoes, genetically edited to contain high amounts of γ-aminobutyric acid (GABA), was sold direct to consumers in Japan by Sanatech Seed [11]. Two years before that, was marketed the first genome edited food product, the high-oleic soybean oil Calyno™, obtained from plants that have been edited to produce fewer saturated fats and zero trans fats (Calyxt) [9]. To date, the GE crops and products have still limited commercial prevalence because they are new and unfamiliar to consumers relative to other breeding techniques and the regulatory process is ill defined and shifting in many countries [12].

To reach the market, each GM plant event must undergo a long and costly process. Two decades ago, it was estimated that 8–12 years of research and development were needed prior to commercialization of GM plants [13]. A recent agri-biotech market survey has reported that the cost of discovery, development and authorization of a new plant biotechnology derived single genetic trait has declined from 136 million USD in the 2008–2012 period to the current value of 115 million USD, but the time required to complete the process has increased from 13.1 to 16.5 years [14]. This data suggest a twice as long period needed nowadays, compared with the early 2000s, for a new GM single trait plant to reach the commercialization phase. On the other hand, early commercial applications of genome editing for crop improvement appear to confirm the inherent speed and overall cost efficiency of genome editing [6]. For comparison, the cost for GE crops development to commercialization were estimated to cost ten million USD and the time needed is 5 years [15]. The genome editing is faster and cheaper approach to market than conventional GM technology [16].

Consumers response to GM products is largely influenced by the decision of the governments to ban or approve the GM crops cultivation and between acceptance for cultivation of GM crops and market exists a wide gap across countries, a comprehensive bibliometric analysis has concluded [17]. On the other hand, a recent systematic global overview has concluded that GE foods are often more accepted than the GM foods, which is partially due to the fact that genome editing is perceived as more natural [16, 18].

2 The Commercial Cultivation of Genetically Modified Plants in the EU

In 1998, only two years after the GM crops were first marketed worldwide [3], their cultivation in the EU started, being among the first territories to commercially adopt the cultivation of biotech crops at global level [19] (Fig. 31.1), well in advance of countries such as Brazil, India, Paraguay, and Pakistan, each of them cultivating millions of hectares with GM crops nowadays [20].

Fig. 31.1
A dual-axis line graph plots the G M crop cultivation and field trial notification versus years. The line of commercial cultivation ascends from 1998 to 2013 and drops from 2013 to 2022. The line of field trial notifications remains constant from 1998 to 2022, fluctuates and ascends up to 2009, and drops.

Commercial cultivation of GM crops and GM plant field trial notifications in EU (1998–2022) [19, 21, 22]

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Only two GM maize varieties, both producing Cry1Ab toxin, insecticidal protein from Bacillus thuringiensis, have been authorized for commercial cultivation in EU: Bt176 (1998–2005), and MON810 (since 2003). The maize hybrids derived from event Bt176 were officially withdrawn from the European market in 2006 because this event contained an ampicillin resistance gene as selectable marker [23]. It took 15 years to reach the cultivation peak, in 2013, with 148,013 ha, on all growing YieldGard™ maize (single trait event MON-ØØ81Ø-6) which, since 2006, continues to be the only GM plant commercially cultivated in the EU [20]. Yet, this GM maize line is one of the 49 insect resistant (IR) transgenic events approved for food and feed use in the EU Register of authorised GMOs.Footnote 2 Since then, the hectarage cultivated with GM maize has gradually decreased to approx. 70,000 ha in 2022, a comparable value with the one register 15 years ago. Last year was also registered the biggest reduction of the cultivated area, with approx. 30%, the most abrupt yearly variation ever recorded in EU [21, 22].

The gradually decrease of the cultivated area with GM plants in Europe was accompanied by a reduction of the countries growing these biotech crops, as farmers from Romania (in 2015) [24], Czech Republic, and Slovakia (in 2017), have voluntarily stopped the commercial cultivation of GM maize [19]. Only two countries, Spain [22] and Portugal [21], are commercially cultivating GM crops in Europe for the last 5 years.

Worth mentioning that the provisions of the EU GMO opt-out Directive 2015/412 [25], which have allowed to a significant number of EU MSs to officially restrict the cultivation of genetically modified organisms (GMOs) in their territory, did not changed the status quo of the EU-28 countries, as 11 countries have officially chosen to legally allow the commercial cultivation of GM crops [19]. Yet, in 2018 the Court of Justice of the EU (CJEU) ruled (case C-528/16) that organisms obtained by mutagenesis, as can be achieved using New Plant Breeding techniques (NPBTs), including genome editing techniques, are genetically modified organisms (GMOs) as defined in the European Directive 18/2001/EC [26]. This decision, imposing for the genome edited plants to follow exactly the same authorization procedure as the GM plants, was expected to delay their development, testing, approval and availability of these new plant varieties on the EU market and their commercial cultivation [19].

3 The Notifications for Field Trials with Genetically Modified and Genome Edited Plants in the EU

The field trial under field conditions is a preliminary, but essential step for developing GM plants, especially if they are intended for commercial cultivation. In the EU, a new GM crop event has to be compared to its closest non-GM counterpart as a corner stone of the pre-market risk assessment. This is a critical final test to monitor their effects on the receiving environment (e.g. non-target organisms) and also detect possible occurrence of differences, caused by intended and unintended effects, in composition, as well as in agronomic, phenotypic and molecular characteristics [27]. The EU continues to have the broadest and most stringent regulations in the world governing these field trials as an essential part of the risk assessment before market approval [28].

During the regulatory framework set by the Directive 90/220/EEC (1991–2001) [29] 1687 field trial notifications were registered and their number dropped by 76% between 1998 and 2001, mainly due to the de facto moratorium in place since 1999 [13]. The notifications documented by the dedicated European Commission’ GM Plants Register,Footnote 3 containing the list of summary notifications (SNIFs) submitted to the competent authority of the EU MS under the Directive 2001/18/EC (from 2002) [30], has also dramatically dropped by 91% in the last 9 years (Fig. 31.1).

The CJEU’s decision from 25 July 2018, stating that plants obtained with the new genome editing techniques are GMOs from the regulatory point of view, has immediately changed the legal status of the first field trial of a CRISPR-Cas-9 genome edited crop, i.e., Camelina sativa, in Europe (EU-28) [31], that began on 5 June the same year at Rothamsted Research (UK) [32]. Yet, the first notification of a field trial with a genome edited plant in Europe recorded in the dedicated GMO Register was carried out in 2018 by the Flemish Institute for Biotechnology (VIB) (Ghent, BE) with maize with an impaired DNA-repair mechanism and maize with modified growth characteristics (Fig. 31.2).3

Fig. 31.2
A multiline graph plots field trial notifications versus years. The line labeled G M decreases from 8 to 2 from 2018 to 2022. The line labeled G E increases from 1 to 5 from 2018 to 2019, decreases from 2 to 1 from 2020 to 2021, and increases to 4 in 2022.

The notification for field trials with GM and GE plants under Directive 2001/18/EC (2018–2022)

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That first field trial with a GE plant has immediately raised a strong concern that limiting their feasibility by expanding the complexity of the regulatory process and the associated financial burden of dedicated experimental sites will certainly hinder research [32].

The evolution of the field trial notification with GE plants since than (2018–2022) (Fig. 31.2) has fully confirmed, to date, that assumption: their yearly total number being maximum 5 (in 2019).

The field trial notifications with GM plants in EU proved to be a sensitive indicator of the overall research and development activities in the past [33]. Moreover, the dramatic reduction of field trials in the EU has also coincided with increasing safety demands, decreases in funding, and changes in the European directives [34]. Under the regulatory framework set by the Directive 2001/18/EC, the last 20 years can be generally divided into two separate periods: the first years characterized by a sharp increase of both number of field test notifications and hectarage of commercial cultivation followed by a decrease of both of them (Fig. 31.1). This data suggests a high degree of interdependence of their overall trend in the EU. While the notifications for field tests with GM plants do follow a clear descendent trend in the last 4 year, the notifications for GE are variable but their status in 2022, compared with the total number, was bigger than of the field trials with GM plants, for the first time (Fig. 31.2), offering hopes for an ascendant trend to be expected in the coming years, hopefully translated into their commercial cultivation status in EU. Worth remembered that all the field trials, including with GE plants, are carried out following the regulatory framework developed more than two decades ago [30], well before the NBTs to be proposed, developed and commercially validated, as it is the situation nowadays. The current regulatory regime for field trials was found ill-fitted to breeding activities [35].

4 The Awareness and Concerns of the EU Citizens About the Use of Genetically Modified and Genome Edited Plants in Agri-Food

Eurobarometer is the polling instrument used by the European Commission (EC), and other EU institutions, to monitor regularly the state of public opinion in Europe on issues related to the EU as well as attitudes on subjects of political or social nature.Footnote 4 It is a cross-temporal and cross-national comparative program of regularly repeated cross-sectional surveys [36]. Additionally, special Eurobarometers are used to monitor if citizens want the EU to act on a specific policy topic or support the EC’s solution to a policy problem [37]. In order to guarantee the representativeness of results, Eurobarometer surveys rely on a randomly selected sample of persons and the total sample is weighted to ensure demographic and geographical representativeness and the EU average is calculated taking into account the relative weight of each country.4

4.1 The Concern of the EU Citizens About the Use of GM Plants for Farming

The attitude of EU citizens toward the release of GMOs into the environment was assessed through a special series of four Eurobarometers during a 9-year period (2002–2011). In 2002, when they were first asked about, the “use of GMOs” was a concern ranked 18th, from 25 different environmental issues, representing 30% from the worries expressed by the EU citizens [38]. The following three surveys (2004, 2007, 2011) have specifically asked for concerns related to the use of GMOs for farming [39,40,41]. The percentage of worried EU citizens about the use of GM plants in the environment, for farming purposes, has decreased, constantly, down to 19% (Fig. 31.3).

Fig. 31.3
A line graph plots the percentage of worried E U citizens about G M plant farming versus years. The line is at 24 in 2004, decreases to 20 in 2007, and then further decreases to 19 in 2011.

Concerns expressed by the EU citizens toward the use of GM plants in farming (2004–2011)

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4.2 The Awareness and Concern of the EU Citizens About the Use of GM and GE Ingredients in Food

A series of four Eurobaromer surveys (2005, 2010, 2019, and 2022), initiated by the European Food Safety Agency (EFSA), aimed to investigate Europeans’ perceptions of and attitudes towards food safety by exploring the Europeans’ interest in food safety-related topics and factors affecting food-related decisions and awareness of and main concerns about food-safety topics [42], including “genetically modified ingredients in food or drinks” (2005, 2010, 2019, and 2022) and, more recently, “genome editing” in food (2019, and 2022).

4.2.1 The Awareness of the EU Citizens About the Use of GM and GE Ingredients in Food

Awareness of food safety topics remains high among EU citizens [42]. The awareness among the EU consumers of the use of both GM and GE in food production was investigated in the last two Special Eurobarometers [42, 43], offering a valuable insight on how the two plant biotech technologies, GMOs, used for almost three decades for farming, and food and feed production in Europe, and GE, only recently has entered into the EU consumer’s attention, but with no farming and food production applications in Europe, yet, are perceived and aware off at the consumers’ level (Fig. 31.4).

Fig. 31.4
A multiline graph plots the percentage of awareness expressed by consumers versus years. The line labeled genome editing increases from 21 in 2019 to 29 in 2022. The line labeled G M ingredients decreases from 60 in 2019 to 56 in 2022.

Awareness expressed by the EU citizens about the use of GM and GE in food production

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As expected, in 2019, the awareness level about GM were considerably higher (three fold) than about GE-food associated issue, but only 3 years later, due to a marginal decrease (4%) of the declared awareness about GMO, and a significant increase (38%), of the GE among the EU citizens, the difference between the two food safety-associated topics decreased by one third from the previous levels. Notably, in 23 of the 27 EU MSs, awareness of the use of new biotechnology in food production, i.e., GE, has risen since 2019 [42].

4.2.2 The Concerns Expressed by EU Citizens About the Use of GM and GE Ingredients in Food

Around one quarter (26%) of the EU citizens indicate the presence of genetically modified ingredients in food or drinks as a concern in 2022 while only a smaller proportions (8%), the use of new biotechnology in food production, i.e. genome editing (Fig. 31.5).

Fig. 31.5
A multiline graph plots the percentage of concerns expressed by consumers versus years. The line labeled genome editing increases from 4 in 2019 to 8 in 2022. The line labeled G M ingredients decreases from 27 in 2019 to 26 in 2022.

Concerns expressed by the EU citizens about the use of GM ingredients and genome editing in food and drinks

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Compared with 2019, for most of the concerns expressed by EU consumers, listed in the Special Eurobaromer survey, there have been increases in the proportions and this is particularly the case for the use of GE in food production which has doubled, from 4% to 8% from the total, among the EU citizens [42].

4.2.3 Trends and Evolution of the Awareness and Concerns Expressed by the EU Citizens About the Use of GM and GE in Food Production

The time series of Special Eurobaromer surveys on Food Safety, spanning over 18 years (2005–2022), offer a consistent and clear overview on the opinions the EU citizens have on the most relevant food-safety related issues. Included right from the start among the investigated topics, the opinion about the concerns about the presence of GM ingredients in food was recorded and it reveals a clear and significant reduction of them, from approximately 2/3 (62–66%) of the citizens to less than 1/3 (27–26%) (Fig. 31.6).

Fig. 31.6
A multiline graph plots the percentage of awareness and concerns expressed by consumers versus years. The line labeled concern ascends from 62 in 2005 to 66 in 2010 and then descends to 27 in 2019, and then to 26 in 2022. The line labeled awareness descends from 60 in 2019 to 56 in 2022.

Trends of the awareness and concern expressed by the EU citizens about the use of GM ingredients in food

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4.3 The EU Citizens’ Awareness and Concerns During the Transition from GM to GE Plants

Gathered in the last three decades, scientific evidence about the perception of GM plants and derived food products is large enough, the EU especially being one of the territories well represented in such analyses [16]. Comprehensive analyses have concluded that EU consumers have more negative perception and less purchase intention toward GM foods in contrast to the consumer perception in North America while in developing nations, the positive perception arises owing to the persistent demand for food [17].

In Europe, during the first decade of the new millennium (1999–2010) a 12% increase was recorded, by a series of Special Eurobarometers, among the EU citizens optimistic about biotechnology [44]. Unfortunately, this share of optimism was not reflected towards the use of GM plants in agri-food in EU. The awareness levels, recorded lately among the citizens regarding the use of GM ingredients in food, were at medium levels and have even decreased slightly [45]. This could be correlated with the abrupt decrease of both GM crop testing and commercial cultivation in Europe. The lower level of awareness was inevitably followed by the proportion of EU citizens concerned about the use of GM crops in farming and for food production, as shown by a long time series of Special Eurobarometers.

The available data about the perception from the public and relevant stakeholders of GE is very limited [16] and, in this context, the recent surveys of the awareness and concerns among the EU citizens regarding the use of GE in food production is all the more relevant considering the large territory covered and the trends revealed [42]. In only 4 years (2019–2022), the awareness about GE among the EU citizens has significantly increased, reaching more than the half of the one about GM products – a three decade old technology in Europe though. Moreover, the number of concerned EU citizens about GE has doubled in the same period, as well as the proportion compared with the level of concerns about the GM ingredients.

NBTs and their products tend to be valued more highly than their GMO counterparts [12, 16] but because large differences occurs within target groups, regions and products [16] a large, highly and multidimensional heterogeneous territory, as the EU proved to be along the years with respect to biotechnology, is scientifically and practically relevant for all stakeholders. It is critically important the public attitude towards new breeding techniques, and their field testing, commercial cultivation and products, to be extensively investigated as they could be misperceived and rejected even though they hold much promise to improve food supply chains’ sustainability, foster better health outcomes for consumers and the environment [12] and their acceptance will be a key factor for policy support [16].

5 Conclusion and Future Perspectives

Relevant time series of Eurorometers have surveyed the awareness and concerns of the EU citizens about the use of GM crops for farming and food production. The public opinion has shown a steady decrease of both indicators along with the notification for field trials and commercial cultivated of GM plants in the EU. More recently, both the awareness level and concerns expressed by the EU citizens about the use of GE in food production has increased significantly in only 4-year period.

The public opinion is fundamental for the acceptance and adoption of any new technology, including NBTs, in Europe. The long term evolution of the public attitude and acceptance of the GE plants and foods is particularly relevant considering the substantial opposition to GMOs recorded in the past, among the European citizens. The current level of awareness and concerns about GE, and their short term evolution, is important as a new regulatory framework is in preparation by the European Commission.