2.1. The Arguments of the Organic Sector’s Ban on Genetic Engineering
As the organic certification is based on the farming process rather than on the end products as such, it implies that also breeding as an activity within the agricultural process and is evaluated for compliance to organic values and rules [
34]. The first ban on GE came from IFOAM’s General Assembly in 1993 [
35], followed by the European Regulation for organic agriculture in 1999 [
29]. The main arguments given at that time by IFOAM were mainly related to ecological risks but also included a first notion of ethical arguments based on respect for the integrity of life, including plants [
35]. The conceptualization of this argument of integrity of life was elaborated some years later [
36], and further discussed in
Section 2.2. Verhoog [
37] further analyzed the arguments of the organic sector and summarized them in three categories: (i) environmental and health risks; (ii) socio-economic and legal aspects; and (iii) values and principles of sustainability of the organic sector.
With respect to the first category of arguments concerning environmental and health risks, the organic sector feared the unpredictability of undesired side effects such as environmental and health risks considered from the organic holistic view as inherent to the reductionist approach of GM, supported by the fact that many scientists were not agreeing on the risk-analyses and the interpretation of those data [
37]. While the risk of GMO plants might have been overestimated, their claimed benefit was also exaggerated [
10]. The widespread use of herbicide resistant genotypes eased the workload of conventional farmers, however, it also resulted in increased herbicide residues in feed and human food [
38] and within short time their benefits are overcome by resistant weeds. Similar for Bt cotton, after wide spread use, severe yield losses were caused in India in 2016 due to resistant pink bollworm attack [
39]. Giving high priority to holistic approaches, the organic sector has a different risk perception and therefore different interpretation of outcomes of risk analyses. Hence, it rather applies the precautionary principle (Principle of care) to avoid any ecological risks and therefore seeks for alternative solutions.
With respect to the second set of arguments (socio-economic aspects), the organic sector was concerned about the freedom of choice for the farmer and consumer due to contamination of GE and non-GE products as not every country has clear coexistence rules [
37]. Another aspect in this category is the concern about the intellectual properties rights through patenting and the loss of independence of farmers in their choice of seeds and their ability to save their own seeds.
The third category of arguments was related to the incompatibility of GE with the principles of sustainability of the organic sector based on the holistic approach to the living nature, respecting and supporting the ability of self-regulation by ecological management and respecting the integrity of living entities, based on the four basic principles of OA as described above [
36,
37].
2.2. Continuous Developments and the Need for Clear Evaluation Criteria
In the early stages (end of the 1990s) of the GE development, the Dutch government accepted the exclusion of GE by the organic sector but required the Louis Bolk Institute to develop a clear and consistent framework and criteria to evaluate all at that time existing breeding techniques. This resulted in a process with many national and international workshops with organic players and reports since 1997 [
40,
41,
42]. The organic sector goes a step further than from a stewardship attitude that considers natural resources at the disposal of mankind albeit managed with care in order to maintain resources for next generations. From the holistic view the organic sector embraces the partner attitude towards nature which includes that not only humans and animals but all living entities, including plants, are considered ethically relevant out of respect for the integrity of life, referring not only to an extrinsic value (usefulness for mankind) but also to a perceived intrinsic value of living organisms (worth as an living entity as such based on respect for their “otherness”, dignity, wholeness and autonomy). The dignity of living organism including plants have for example been implemented as a common value in the Swiss Federal Constitution of 2002 [
43]. This respect for the integrity of life has consequences in the decision making on how to manage (cultivated) plants in OA, refraining from violating the integrity of life and as a consequence cooperating with nature rather than excluding nature [
36]. This respect for the integrity of life is also one of the reasons for organic agriculture to refrain from inorganic (chemical-synthetic) substances and to allow only organic substances.
To make the concept of intrinsic value of plants operational, four levels of integrity have been distinguished: (i) the level of the nature of life in general; (ii) the level of the specific nature of plant life; (iii) the level of the species-specific nature of plants; and (iv) the level of the nature of individual plants [
36]. Breeding techniques can be evaluated for violating one of more levels of integrity of life.
Techniques for variation induction, selection, maintenance and propagation can be applied at three levels: plant or crop; cell or tissue (in vitro), and DNA. As organic agriculture aims to work within the realm of life while respecting the integrity of life, the techniques that go beyond the whole plant level are considered not suitable with the values of organic agriculture and thus not suitable for use in organic plant breeding programs. As the cell can be technically considered as the lowest level of self-organizing life (as the plant can be regenerated from a single cell), one could argue that it could be allowed and it is not forbidden in the organic regulation and reflects the middle position between the two other more clearly defined categories. Techniques directly engineering at DNA level go beyond the level of the self-organized life and are therefore violating the integrity of life, and more specifically the genotypic integrity e.g., when it forces natural crossing barriers [
36]. Similarly, cell fusion where cell DNA and cell cytoplasm from different organisms are merged by technological means are considered as GE according to IFOAM definition of GE in the IFOAM norms [
44]. On the other hand, the use of molecular markers is not excluded in organic breeding as they are diagnostic tools for plants and do not directly interfere in DNA [
45]. The organic approach is aimed at the quality of the process, respecting the integrity of living entities, therefore the focus is on a holistic approach at all organization levels, and not on an approach whereby the parts are dissected in order to guide processes on a lower organization level. This approach has been very helpful for the organic sector to determine what approaches are suitable, but sometimes criticized by scientists. The criticism is that if the organic sector wants to be completely consistent, it should also exclude all varieties bred with techniques (e.g., through mutation breeding) in the 1950 to 1980s that do not comply with the development of the IFOAM definitions [
46].
With the advent of new breeding techniques and methodologies, it became clear, that the organic sector needs an agreement on transparent criteria for their evaluation. After various discussions on a national and European level the European Consortium of Organic Plant Breeding (ECO-PB), being one of the IFOAM member organizations, submitted in 2012 a position paper on the goals and values of organic plant breeding and defined various criteria for the assessment of new breeding techniques [
41,
42]. ECO-PB formulated the aims of organic plant breeding as follows: (1) The breeding goals shall match the respective crop species and the needs of the complete value chain of the organic sector (producers, processers, traders and consumers). The breeding goals shall aim at the sustainable use of natural resources and at the same time account for the dynamic equilibrium of the entire agro-ecosystem; (2) Organic plant breeding supports sustainable food security, food sovereignty, secure supply of plant products (e.g., fiber, medicine, timber), and the common welfare of society by satisfying nutritional and quality needs of animal and human beings; (3) Organic plant breeding sustains and improves the genetic diversity of our crops, and thus contributes to the promotion of agro-biodiversity; (4) Organic plant breeding makes an important contribution to the development of our crops and their adaptation to future growing conditions (e.g., climate change). The ethical criteria, criteria for breeding strategies and the socio-economic criteria are described in detail in the position paper of the European Consortium of Organic Plant Breeding (ECO-PB) [
41]. The ethical criteria to respect the genome and the cell as indivisible functional entity follow the concept of respecting integrity of life, and which is also at the basis of the basic principles of OA as above described. Therefore any technical or physical invasion into the isolated cell is refrained from and plant specific crossing barriers are respected, irrespective of potential benefit risk assessments. An important point in the breeding strategy is that organic plant breeders—breeding exclusively for OA—perform all steps from crossing till selection and multiplication under organic growing conditions. On the socio economic aspects, ECO-PB is promoting free exchange of germplasm, transparency of the breeding process, open pollinated varieties instead of F1-hybrids, participatory breeding involving farmers and the value chain and a plurality of breeding initiatives to enable a more diverse and sustainable agriculture.
Organic plant breeding is a holistic approach where the process of breeding, including technical, socio-economic and ethical aspects, is equally important as the final product (cultivar) with its characteristics [
47]. With new labels for organically bred varieties such as “Bioverita” in Switzerland the sector tries to communicate its values and create valorization along the value chain up to consumers (
www.bioverita.org).
New sequencing approaches combined with an increase in identification of candidate genes and more precise techniques of genetic engineering will have a big impact on plant breeding, especially since the new methods like CRISPR-Cas9 are much easier and cheaper in their application than former methods [
48,
49,
50,
51]. The potential advantages of these new techniques have been widely published. However, there has been on ongoing debate in the European Union (EU) regarding how to handle novel breeding techniques like Zinc finger nucleases, oligonucleotide directed mutagenesis, cisgenesis and intragenesis, RNA-dependent DNA methylation, grafting on GM rootstock, reverse breeding, agro-infiltration and synthetic genomics with respect to commercialization of derived cultivars for several years. Until now no legally binding decision has been made by the EU if the individual techniques shall fall under present rules for genetically modified organism (GMO) legislation [
52,
53]. The main drivers for adopting such techniques are their technical potential and their economic advantage by speeding up breeding processes, whereas prerequisite of known genetic information and the uncertainty if final cultivars will be classified as GMO or non-GMO are hampering the utilization of these techniques [
52]. In their recommendation, Lusser et al. [
53] differentiated between those techniques that: (i) introduce whole genes or longer DNA fragments versus those with less than 20 base insertion; (ii) if these genes are from the same species or different species; (iii) if they are transient or stable integrated; and (iv) if the modified plant can be detected, i.e., if they can be clearly distinguished from plants derived from cross breeding or not. If only small DNA changes have been introduced (e.g., gene editing through oligonucleotide, zinc finger nucleases, TALEN or CRISPR-Cas9) or if the gene regulation is modified (e.g., RNA-dependent DNA methylation) it will not be possible to detect such changes, except if it is protected by a patent which requires traceability.
In addition, other countries such as the USA, Japan, and Australia are struggling with proper regulation. A notable difference between EU and USA regulation is that in the EU legislation on GE the process and the product of GE are considered, while in the USA only the final product is evaluated [
49]. The US recently released the first products, an anti-browning mushroom and a waxy corn, genetically modified with the gene editing tool CRISPR-Cas9 for commercialization without the oversight of the US Department of Agriculture with the justification that these products do not contain genetic material from plant pests such as viruses or bacteria [
54]. The general public’s view on safety aspects of foods derived from products of new genetic engineering techniques and the process based approach in Europe are the greatest hurdle faced for definition and implementation of regulatory processes for new plant breeding technologies in Europe. Given the difficulty in conveying concepts of modern biotechnology to the general public, there is considerable potential that the public may not immediately embrace genome editing [
55]. Therefore, several attempts are made to convince the organic sector about new technologies [
46,
56] in order to reach out to the consumers. New genome editing technologies/modern biotechnology techniques have the promise to make plant breeding more efficient and precise. They create specific mutations and have the potential to generate plants that differ from the original plant at a single nucleotide position and otherwise carry no signs of the modification [
49,
56,
57]. Although these techniques are causing off-target mutations, the expectation is that in the future the number of off-target mutations is likely to reduce due to technological advances [
49]. However, off-target mutations caused by gene editing need to be compared to a mutation rate of 3.3 base substitutions per generations in
Arabidopsis thaliana [
58].
It is clear that scientists are aware of public concerns [
49,
56,
57,
59]. However, opinions of scientists on increasing the acceptability of these technologies for the public vary. Some expect that over time GE will become accepted by the organic sector [
56]. Others recognize that although new biotechnologies are becoming more precise and consumer disapproval gradually reduces, techniques such as cisgenesis still is considered as unnatural by those consumers [
59]. It is expected that consumers of conventional products prefer more precise novel biotechnologies over transgenesis, and that this change in attitude is not the case for consumers of organic products [
57]. Hence, it is important that scientists acknowledge the pluriformity in public opinions, and that a pluriformity in science and plant breeding is equally important. This also means that in scientific debate similar space should be available for criticism of the soundness of the arguments of the organic sector to determine acceptable principles for organic breeding [
45] as for the arguments of the organic sector itself [
36]. Based on the principles of organic plant breeding described by the ECO-PB [
41] and in the IFOAM Norms for organic production and processing in 2014 [
44] any breeding technique can be evaluated against these criteria (
Table 1). The first five criteria are mandatory, whereas the possibility of farm saved seed is preferred but not an exclusive criterion. For example, marker assisted selection is a diagnostic tool based on the analysis of DNA. It does not interfere physically at the genome or cell level, it does not overcome species specific crossing barriers, and does not affect breeder’s privilege or farmers’ right to produce farm save seed; therefore this is acceptable for the majority of organic plant breeders. In contrast, methods which technically alter the DNA or RNA by methods of genetic engineering are not considered to be compatible with organic breeding, as this violates the integrity of the genome. Likewise, cytoplast fusion is not accepted as this is based on technically forced fusions of somatic cells to overcome species specific crossing barriers in order to introduce traits such as male sterility. This violates the integrity of the cell as a functional unit.
For the organic sector this debate is of great importance at two levels. First of all, the organic sector has to define in a participatory process including all stakeholders of the organic sector clear criteria for the evaluation of new techniques for organic plant breeding. Secondly, the organic sector has to decide which cultivars derived from conventional breeding programs are acceptable for organic production as they meet the IFOAM principles as well as the expectations of the consumers.
With respect to the first task to evaluate the NBT, the organic plant breeders of ECO-PB share common values expressed in the position paper and they will not apply the above mentioned techniques in their breeding programs as in their understanding this violates the integrity of the genome or the cell. The second task to define which cultivars should be allowed in OA is much more difficult and presently under discussion at IFOAM International. Here the criteria might obtain a different priority. An example is cell fusion, which is not applied by organic plant breeders, but used widely to obtain male sterile plant for hybrid seed production in brassica vegetables. Some private labels in Germany have already banned cultivars based on cell fusion for OA, due to the fact that the integrity of life and more specifically the genotypic integrity is violated and species specific crossing borders are overcome. In order to have a well-informed discussion the different breeding methods have been described indicating their applications, potentials and ethical issues [
42]. As the application of some of the novel genetic engineering techniques are not detectable, the organic sector is very concerned that they might be released without labeling. In that case, the organic sector will no longer have the freedom of informed choice. Therefore, there is a strong lobbying of IFOAM for disclosure of the breeding methods, which is presently only given if the techniques fall under the GE regulation. Transparency and freedom of choice for farmers and consumers as well as a plurality of breeding strategies will allow co-existence of GM and non-GM food chains, and will be beneficial to pluriform societies (e.g., [
1,
2,
3]). Having experienced the impact of coexistence of GE on OA [
60], and the disappearance of non-GE cotton seed in India within only 10 years [
61], it is important to take measures in advance that different farming systems can co-exist.
In the USA, the National Organic Standards Board has decided to update the organic standards to exclude cultivars and derived organic products developed with new generation genetic engineering end gene editing techniques [
62]. In Europe, a position paper of the IFOAM EU GROUP [
63] urges that cultivars derived from NBT which engineer living organisms in the cell and/or nucleus through technical, chemical or biotechnological intervention shall be defined as GE and be subject to a risk assessment and if authorized for release be subject to the mandatory traceability and labeling requirements that apply to other GE techniques. This transparency is important to ensure organic farmers and customers free choice of non-GE seed and food, respectively. At the international level, the IFOAM has set up working groups on the definition of GE and the criteria for the evaluation of NBT to be discussed among the organic movement and IFOAM’s members at the next general assembly in 2017.