Next Article in Journal
Numerical Modelling of High-Speed Loading of Periodic Interpenetrating Heterogeneous Media with Adapted Mesostructure
Previous Article in Journal
Remaining Useful Life Prediction of Aircraft Turbofan Engine Based on Random Forest Feature Selection and Multi-Layer Perceptron
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Applied Sciences
Volume 13
Issue 12
10.3390/app13127185
applsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effectiveness of a Priority Management Scheme of Living Modified Organism Re-Collection Areas in Natural Environments of South Korea

by
Hye Song Lim
1,2,†,
A-Mi Yoon
1,3,†,
Il Ryong Kim
1,
Wonkyun Choi
1,
Young Jun Jung
1,
Sunghyeon Lee
1 and
Jung Ro Lee
1,*
1
LMO Team, National Institute of Ecology (NIE), Seocheon-gun 33657, Republic of Korea
2
Department of Horticulture Industry, Wonkwang University, Iksan 54538, Republic of Korea
3
Division of Life Sciences, Jeonbuk National University, Jeonju 54896, Republic of Korea
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Appl. Sci. 2023, 13(12), 7185; https://doi.org/10.3390/app13127185
Submission received: 21 April 2023 / Revised: 10 June 2023 / Accepted: 14 June 2023 / Published: 15 June 2023
Browse Figures
Versions Notes

Abstract

:
Since 2009, the Ministry of Environment and the National Institute of Ecology in South Korea have been conducting a living modified organism (LMO) monitoring and post-management project in natural environments to prevent the unintentional release and spread of LMOs to natural ecosystems. The project surveyed six administrative districts of South Korea from 2009 to 2013 and collected 1960 LMO suspicious samples from 1850 monitoring sites. As a result, 113 LMOs were identified at 65 sites and removed for post-management. An analysis of the five-year LMO monitoring results showed that LMOs were re-collected in 38.4% of the 65 areas where they were initially collected. This result led to the establishment of a new LMO management system in 2014, with priority given to areas where LMOs had been re-collected twice or more within the last five years. Intensive surveys and post-management were conducted four times a year in these priority management areas. The results confirmed that the novel management system for LMO priority areas effectively prevented the continuous collection of LMOs in the same areas. In conclusion, establishing a safety management system for priority management areas, intensive surveys, and post-management efforts are crucial for protecting natural ecosystems from the putative risks of unintentionally released LMOs.

1. Introduction

Recombinant DNA technology, developed in 1973 by Paul Berg, Herbert Boyer, and Stanley Cohen, can be used to alter the genotypes of living organisms artificially [1,2]. This technology has led to the development of living modified organisms (LMOs), which include biological species whose DNA has been altered by introducing specific genes. LMOs are widely used in agriculture, food, livestock, and the environment [3]. The first genetically modified (GM) tobacco was developed in 1983, and GM crops such as cotton, soybeans, and corn were commercialized in 1994 [4,5,6]. In 1996, the first commercial production of LMO crops occurred, and the cultivation area of LMO crops had grown to 190.4 million hectares in 29 countries by 2019 [7,8,9].
Although LMO crops have brought economic benefits through increased crop yields and reduced pesticide costs, concerns remain regarding their environmental impacts and risks. These issues include LMO gene flow to related species and non-LMO crops, reduced herbicide effects, effects on non-target organisms, and uncertainty about their safety in natural environments, including developing resistance to target pests and reduced genetic diversity [10,11,12,13,14]. In addition, LM crops may affect the diversity of the microbial community and soil ecosystem function. Although the interactions between LM crops and soil microbial communities are not well known, it is possible that LMO genes can be transferred to native soil microbes, and proteins released from LM plants may affect the biodiversity of soil microbial communities [15]. For example, previous studies indicated that LM plants, such as glyphosate-resistant crops, could change the composition of the rhizosphere microbial community [16,17,18,19,20,21]. In line with the One Health concept, the root exudates of LMO plants, which contain engineered proteins, may have either positive or negative effects on the health of soil microorganisms in natural environments. Then, soil microbiomes may play a crucial role in the overall health of other ecosystem components, including plants and animals [22,23,24,25,26]. Therefore, this paper aims to highlight the significance of a new priority management system for One Health by mitigating the potential risks associated with LMO spillage in the natural ecosystem.
The Cartagena Protocol on Biosafety was adopted as an international treaty to address these concerns in 2000 [27,28]. The Parties to the Cartagena Protocol on Biosafety, such as Japan, Australia, and European Union, have controlled the development and application of LMOs through their regulation acts [29,30,31,32,33,34]. Countries that are signatories of the Protocol have strictly established risk assessment systems for LMOs to ensure their safety. The LMO risk assessment, under the Protocol, has been determined through a comprehensive evaluation in a scientific and transparent manner. The LMO environmental risk assessment in particular includes exposure evaluation results obtained through laboratory or confined fields using LMO gene products or plants [35,36]. The environmental risk assessment, considering the ecosystem’s food chain of each member country of the Protocol, is essential during the LMO risk review [37,38,39,40,41]. There have also been various claims about the potential benefits and risks of LMOs regarding ethical, environmental, health, biodiversity, and religious issues [41,42]. For this reason, the LMO risk assessment should be conducted according to the principles and methodology consisting of five steps as follows: (step 1) the identification of any novel genotypic and phenotypic traits associated with the LMO that may have adverse effects on biological diversity, (step 2) the evaluation of the likelihood of adverse effects, (step 3) the evaluation of the consequences of any adverse effects, (step 4) the estimation of the overall risk, and (step 5) a recommendation as to whether or not the risks are acceptable or manageable [43,44].
In South Korea, the safety of LMOs has also been managed through the Transboundary Movement, Etc. of the Living Modified Organisms Act (LMO Act), implemented in 2008 [45]. The Ministry of Environment (MOE) and the National Institute of Ecology (NIE) are responsible for monitoring, evaluating, and managing the environmental impact of LMOs in accordance with the LMO Act. The importation of LMO crops into South Korea has steadily increased from 8.57 million tons in 2008 to 11.15 million tons in 2021 [9]. With the rise in imports, concerns have been raised about whether LMOs may spread into natural ecosystems due to accidental spills during transportation and handling. For instance, LM canola has been found on roadsides near import ports in Japan and Canada [46,47,48]. Since 2009, the MOE has implemented an LMO monitoring project involving nationwide surveys, suspicious plant sampling, LMO detection analysis, and post-management in order to prevent the potential risks posed by LMOs in natural environments [49]. Despite these efforts, LMOs have been re-collected at the same survey sites. Thus, a priority management system, for areas where LMOs had been re-collected twice or more within the last five years, was established in 2014 to address concerns about gene flow to non-LMOs or related species and re-spreading by LMO volunteers. This study aimed to assess the effectiveness of this novel priority management system. This study suggests that intensive surveys using the system developed in 2014 effectively minimized the risks posed by LMOs to natural ecosystems and ensured their safety.

2. Materials and Methods

2.1. Data Analysis of LMO Monitoring Project from 2009 to 2013

Since 2009, the Ministry of Environment (MOE) of South Korea has conducted an LMO monitoring and post-management project in natural environments. Based on the LMO monitoring scheme of the MOE, six administrative districts (Gyeonggi-do, Gangwon-do, Chungcheong-do, Gyeongsang-do, Jeolla-do, and Jeju-do) were surveyed [49]. The nationwide survey of unintentionally released LMOs was conducted from 2009 to 2013, and the sample collection site was recorded with a handheld GPS device. In accordance with the guidance manual, survey sites were monitored every four months to collect LMO suspicious plants. Suspicious samples were collected within a 100 m radius of each survey site. The collected plant tissues were dried with silica gel and used for LMO identification using an immunochemical strip kit and polymerase chain reaction (PCR). Suspicious LMO samples were collected nationwide, and 113 LMO crops were detected at 65 sites. The distribution of LMO collection sites was investigated for the intensive survey and management of LMO re-collection sites. For post-management, a re-investigation, accompanied by removal operations, was conducted more than twice a year in areas where suspected samples were found.

2.2. Establishment of an Intensive Management Scheme for the LMO Re-Released Sites

Priority management areas of the total LMO re-collection sites were defined as sites where LMOs were re-collected twice or more in the last five years. Intensive management and surveys of priority management areas were conducted four times per year, considering the lifecycle of survey crops. The ArcGIS ArcMap 10.3.1 system was used to analyze the assigned site distributions as priority management areas from 2014 to 2021 [50]. The priority management areas in natural environments were investigated within a 1 km radius, given the possibility of crossing between LM crops and their closely related plants. Sample collection sites with GPS coordinates and survey photographs were recorded. Then, each suspicious sample was subjected to immunochemical (Envirologix Inc., Portland, ME, USA) and PCR analyses to identify LMOs, including event name and trait type.

2.3. Biological Analysis for LMO Identification of Collected Samples

The samples collected from the priority management areas were analyzed as follows. Sample tissue was ground, and extraction buffer (Envirologix Inc., Portland, ME, USA) was added to the sample powder. A lateral flow test, using an immunochemical strip kit based on the antigen-antibody reaction, was performed at the survey sites [49,51]. After loading, the bands on the strips were monitored to determine whether an event-specific LMO protein was present. In addition, an event-specific PCR was performed to characterize the LMO genes introduced in the laboratory [49,51]. Certified reference materials from the American Oil Chemists’ Society (Urbana, IL, USA) or the Institute for Reference Materials and Measurements (Geel, Belgium) were used as controls for LMO event-specific PCR analysis. The PCR analysis was performed with the 2X Lamp Taq PCR Pre-Mix (Biofact Inc., Daejeon, Republic of Korea), 50 ng genomic DNA as a template DNA, and 1 µL of each primer (10 pmol/µL). The amplification of inserted LMO genes in suspicious plants was achieved using the ProFlex PCR System (Applied Biosystems, Waltham, MA, USA) under the following detail conditions: (1) initial denaturation at 95 °C for 5 min, (2) denaturation (33 cycles) at 95 °C for 30 s, (3) annealing at 59 °C for 30 s, (4) extension at 72 °C for 30 s, (5) final extension at 72 °C for 7 min, and (6) hold at 4 °C. The PCR product’s DNA was displayed by electrophoresis on 2.5% agarose gel, and identified using the ChemiDoc XRS+ Imaging System (Bio-Rad, Hercules, CA, USA). Nucleotide sequencing of the PCR products was performed by Biofact Inc. (Daejeon, Republic of Korea) to identify the event name, manufacturer, and trait type. Sequence alignments were generated with BioEdit v7.2.6.0 [52].

2.4. Survey Analysis of the Priority Management Areas for Eight Years

The number of collected LMO samples between the nationwide general monitoring project and priority management areas was compared. The number of samples identified as LMOs and their crop types were investigated in the priority management areas from 2014 to 2021. Furthermore, crop types, such as cotton, corn, canola, and soybean, were identified annually in the area. LM soybeans were not collected during this period. The category of the LMO collection site in the priority management areas was investigated for post-management and survey strategy in priority management areas. The collection sites were classified as stockbreeding farms, feed factories, roadsides, ports, and others, where “others” included festivals and planting sites [49].
The tendency of LMO discovery per individual priority management area was analyzed annually to evaluate the effect of intensive management over eight years. Among all priority management areas, the ratio of LMO uncollected sites was assessed from 2014 to 2021 for further post-management of the LMO re-collection areas.

2.5. Post-Management of the Priority Management Area

Survey information on all priority management areas, including plant life cycles, cultivation trends, and LMO import and export status data, was used as post-management data. The LMO distribution status was schematized using the ArcGIS ArcMap [50].

3. Results and Discussion

3.1. LMO Monitoring Project from 2009 to 2013

Since 2009, the MOE has been conducted, monitoring projects for the unintentional release of LMOs into natural environments. This study analyzed project results from 2009 to 2013 to efficiently survey and systematically manage LMO collection sites.
The MOE surveyed spills of LMOs in all natural ecosystems of six administrative districts from 2009 to 2013 (Figure 1). The MOE’s survey manual provided to all investigators played an essential role in keeping the unity of the MOE’s surveys. Suspicious samples and environmental information were collected in annual survey sites each season. The sample collection site was recorded with a handheld GPS device. For five years, spilled LMO crops were collected at 65 sites: 8 in 2009, 10 in 2010, 10 in 2011, 19 in 2012, and 18 in 2013 (Figure 1A). The number of LMO collection sites doubled between 2009 and 2013, indicating increased concerns about the unintentional release of LMOs into natural ecosystems nationwide. Notably, 38.4% of LMO collection sites remained unchanged during this period (Figure 1B). This information highlights the importance of the intensive management of LMO re-collection sites to minimize their potential risks in natural environments.

3.2. Classification Analysis of the LMO Re-Collection Sites and LMO Volunteers

The number of LMOs approved for food, feed, and processing imported into South Korea in 2021 was approximately 11.14 million tons, with 9.39 million tons (84.3%) being used for feed and 1.75 million tons (15.7%) for food. In particular, LM corn for feed, LM soybean for food, and LM corn for food accounted for 83%, 9%, and 8% of imported LMOs, respectively [9]. During transportation and use, an unintentional release of these LMOs into natural environments may occur near import ports, stockbreeding farms, feed factories, roadsides, or consumption areas.
As shown in Figure 1, the MOE and NIE surveyed unintentionally released LMOs in natural environments from 2009 to 2013 and analyzed the LMO collection sites to develop a suitable management system. A total of 113 LMOs were detected at 65 sites, and 52 LMOs were re-collected at the same sites (25). This result indicates that LMO spillage may likely occur in areas where they have previously been detected, and that intensive surveys and management of LMO re-collection sites are necessary.

3.3. Development of an Intensive LMO Management Scheme

Therefore, an intensive investigation and management system for LMO re-collection sites is necessary. In 2014, the NIE attempted to establish and apply a priority management scheme for LMO re-collection areas in the natural environments of South Korea.
The general LMO monitoring process from 2009 to 2013 was conducted in three steps: (1) survey and sampling based on the results of the previous year, (2) LMO detection and data analysis using event-specific PCR and sequencing analysis, and (3) post-management at the collection site (Figure 2A). To establish and apply a priority management scheme, priority management areas of the total LMO re-collection sites were defined as sites where LMOs were re-collected twice or more in the last five years (Figure 2B). Priority management areas have been assigned annually since 2014. As shown in Table 1, LMOs were consistently found at the same sites, indicating the need for intensive surveys and post-management.
Figure 2 shows the differences between the general environmental LMO monitoring process and the priority management survey. Firstly, a priority management area was assigned where LMOs had been collected twice or more in the last five years. Secondly, while the general LMO monitoring survey was conducted within a 100 m radius of the site, the priority management survey was performed within a 1 km radius. Thirdly, LM crops and closely related plants were collected and analyzed. Fourthly, while general environmental LMO monitoring was conducted twice a year, priority management areas were surveyed more than four times yearly. According to the newly established scheme, intensive surveys and post-management of the priority management areas were conducted after selecting priority management areas in 2014.

3.4. Selection and Distribution Analysis of Priority Management Areas

The priority management areas were determined by implementing a newly established LMO management scheme (Figure 2). As shown in Figure 3, 198 priority management areas were selected and surveyed in six administrative districts over eight years, from 2014 to 2021. The distribution of these sites varied annually, with 11 areas selected in 2014, 19 in 2015, 24 in 2016, 22 in 2017, 23 in 2018, 32 in 2019, 38 in 2020, and 29 in 2021. The district with the highest priority management areas was Gyeonggi-do (80), followed by Chungcheong-do (33), Gyeongsang-do (29), Jeolla-do (35), and Jeju-do (12). Nine priority management areas in Gangwon-do were only selected from 2014 to 2016.
Of the 198 priority management areas with 55 addresses, 192 (97%) sites with 49 addresses were re-selected twice or more, and 6 (3%) sites with 6 addresses were selected once. In particular, of the re-selected 49 areas, 3 areas were re-selected 8 times (5.5%), 2 areas 7 times (3.6%), 5 areas 6 times (9.1%), 6 areas 5 times (10.9%), 6 areas 4 times (10.9%), 16 areas 3 times (29.1%), and 11 areas 2 times (20%). These results suggest that many sites reassigned as priority management areas require intensive surveys and post-management. Priority management areas are distributed nationwide and are not restricted to any region or location.

3.5. Survey Analysis of the Priority Management Areas for Eight Years

The number of identified LMOs and types of LMO crops were investigated to understand the LMO collection patterns in the priority management areas from 2014 to 2021. In total, 684 LMOs were detected at 237 LMO monitoring sites and 299 LMOs at 198 priority management areas for eight years (Figure 4A). From 2014 to 2016, similar numbers of LMOs were collected in the general and priority surveys. Since 2017, the number of general monitoring surveys has accidentally increased because of the massive cultivation of unapproved LM canola and LM cotton in 2017. Accordingly, the number of priority management areas dramatically increased from 2018 to 2021 compared with that in 2017.
Figure 4B shows the crop types and the number of collected LMOs in the priority management areas by year. From 2014 to 2021, 531 suspicious samples collected from the priority management area were investigated using LMO event-specific PCR analysis (Figures S1–S3, Tables S1 and S2) [49,53,54]. The LMO gene identified by PCR was subjected to sequencing, and its event name was finally confirmed (Figures S4–S6). In summary, various LM cotton and LM maize events were identified, but all LM canola were only GT73 events. A total of 299 LMOs were identified (44 LM corn, 188 LM cotton, and 67 LM canola). As shown in Figure 4B, cotton was the dominant LMO crop collected from 2014 to 2017, along with several LM corn and canola crops. Due to this issue, in 2017, the numbers of LM cotton and LM canola significantly increased in 2018 and 2019, respectively. LM soybeans were not collected during this period.
The categories of LMO collection sites and LMO collection numbers in the priority management areas were investigated (Table 2). The different types and numbers of LMO crops collected from priority management areas each year were believed to be related to the various types of priority management areas assigned each year. The categories of LMO collection sites were classified as stockbreeding farms, feed factories, roadsides, ports, and others, where “others” included festival and planting sites. The main collection sites of 299 LMOs were roadsides (51.8%), stockbreeding farms (25.4%), feed factories (12.0%), others (8.4%), and ports (2.3%). Interestingly, as time has passed, the variety of places where LMOs have been found has increased. One of the reasons is that, as the nationwide monitoring survey sites have increased from 2014 to 2021, the LMO collection site category has been diversified with the increase in priority management areas. The other is an intensive survey and post-management in the priority management areas since 2014. This result suggests that classifying collection sites may help with post-management and survey strategies in individual priority management areas.

3.6. Impacts of Intensive Management on Priority Management Areas

An annual, systematic, and scientifically intensive survey of priority management areas was conducted using previous survey results, such as the LMO collection site type, type of crop, collection time, event name, and GIS database. A survey radius of 1 km for each priority management area was established around the LMO collection site, and suspected LMO samples and related plants were collected in the area. This strategy allows for the prompt post-management of LMO re-collection sites.
The tendency of LMO discovery in each area was individually analyzed yearly to assess the impact of intensive management of LMO re-collection sites over eight years. A total of 198 priority management areas were assigned from 2014 to 2021, with 55 addresses in Gyeonggi-do (15), Gangwon-do (3), Chungcheong-do (13), Gyeongsang-do (10), Jeolla-do (10), and Jeju-do (4) (Figure 5). Of all the priority management areas between 2014 and 2021, no LMO was found at 21 addresses (Table S2). Repeated intensive surveys, LMO removal, and continuous post-management in the LMO re-collection areas have prevented the rediscovery of LMOs in natural ecosystems. The results of this study indicate the need for a novel priority management scheme for LMO re-collected areas. Moreover, the accumulated survey results regarding priority management can be leveraged to implement LMO safety management effectively in the natural environments of South Korea.
Based on the study results, we suggested a novel priority management scheme that combined intensive LMO survey and post-management in LMO re-collected areas to supplement the nationwide monitoring project’s weakness (Figure 2) [49]. The new priority management strategy is divided into four steps: (1) intensive survey and sampling, (2) detection and analysis, (3) revisit and survey, and (4) post-management. If repetitive spills of LMOs into the same environments occur during transportation and use, the MOE and the NIE change the nationwide monitoring process to the priority management scheme. Therefore, the new scheme has been introduced to forestall the putative risk of the LMO re-collected environments since 2014. Finally, the priority management results can be used to improve the following biosafety policy of the MOE to manage the hardened LMO spillage sites in South Korea’s natural ecosystem.

4. Conclusions

In this study, a new priority management system was developed for the effective post-management of LMO re-collected sites assigned as priority management areas in the natural ecosystems of South Korea. As shown in Table S1, intensive surveys, LMO removal, and continuous post-management effectively prevented LMO re-spill. These findings highlight the importance of the newly developed system for LMO priority management, which effectively prevents the continuous release of LMOs in the same areas. Furthermore, management efforts are crucial for protecting natural ecosystems from the putative risks of unintentionally released LMOs, such as gene flow to related species, reduction in genetic diversity, and impact on non-target organisms. The new priority scheme, and its applied survey results by the NIE and the MOE, may be essential in removing the putative risks of LMO spillage, preventing its diffusion, and preserving the natural environments of South Korea.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app13127185/s1, Table S1: Oligonucleotide primers used in this study; Table S2: LMO discovery patterns by year in 198 priority management areas with 55 addresses from 2014 to 2021; Figure S1: Event-specific PCR results of LM cotton collected from priority management areas from 2014 to 2021; Figure S2: Event-specific PCR results of LM corn collected from priority management areas from 2014 to 2021; Figure S3: Event-specific PCR results of LM canola collected from priority management areas from 2014 to 2021; Figure S4: Sequencing analysis result of LM cotton; Figure S5: Sequencing analysis result of LM corn; Figure S6: Sequencing analysis result of LM canola.

Author Contributions

Conceptualization, H.S.L. and J.R.L.; methodology, H.S.L., A.-M.Y. and J.R.L.; validation, H.S.L., A.-M.Y. and J.R.L.; formal analysis, H.S.L. and J.R.L.; investigation, H.S.L., A.-M.Y., I.R.K., W.C., Y.J.J., S.L. and J.R.L.; resources, H.S.L. and J.R.L.; data curation, H.S.L., A.-M.Y. and J.R.L.; writing—original draft preparation, H.S.L., A.-M.Y. and J.R.L.; writing—review and editing, J.R.L.; visualization, H.S.L. and J.R.L.; supervision, J.R.L.; project administration, J.R.L.; funding acquisition, J.R.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by a grant from the National Institute of Ecology (NIE), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIE-A-2023-07).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Berg, P.; Mertz, J.E. Personal Reflections on the Origins and Emergence of Recombinant DNA Technology. Genetics 2010, 184, 9–17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Nandi, K.; Mahanti, S.; Dhrubo, D.; Sen, D.D.J.; Dastider, D.; Sudip, K.; Mandal, S. Genetic Engineering-the Foundation of Cutting-Edge Extramural Research. Wjpmr 2020, 6, 257–269. [Google Scholar]
  3. Kim, H.J.; An, J.-H.; Han, T.-H. Study on the Safety Management of Environmental Risk Assessment Field Trial of Genetically Modified Crops in Korea. J. Agric. Sci. Technol. 2015, 50, 9–14. [Google Scholar] [CrossRef] [Green Version]
  4. Zeljezić, D. Genetically Modified Organisms in Food—Production, Detection and Risks. Arh. Hig. Rada. Toksikol. 2004, 55, 301–312. [Google Scholar]
  5. Raman, R. The Impact of Genetically Modified (GM) Crops in Modern Agriculture: A Review. GM Crops Food 2017, 8, 195–208. [Google Scholar] [CrossRef]
  6. Cho, J.-I.; Park, S.-H.; Lee, G.-S.; Kim, S.-M.; Lim, S.-M.; Kim, Y.-S.; Park, S.-C. Current Status of GM Crop Development and Commercialization. Korean J. Breed. Sci. 2020, 52, 40–48. [Google Scholar] [CrossRef]
  7. Khush, G.S. Genetically Modified Crops: The Fastest Adopted Crop Technology in the History of Modern Agriculture. Agric. Food Secur. 2012, 1, 14. [Google Scholar] [CrossRef] [Green Version]
  8. Adenle, A.A. Global Capture of Crop Biotechnology in Developing World over a Decade. J. Genet. Eng. Biotechnol. 2011, 9, 83–95. [Google Scholar] [CrossRef] [Green Version]
  9. Korea Biosafety Cleaning House. Available online: https://www.biosafety.or.kr (accessed on 10 June 2023).
  10. Tsatsakis, A.M.; Nawaz, M.A.; Tutelyan, V.A.; Golokhvast, K.S.; Kalantzi, O.I.; Chung, D.H.; Kang, S.J.; Coleman, M.D.; Tyshko, N.; Yang, S.H.; et al. Impact on Environment, Ecosystem, Diversity and Health from Culturing and Using GMOs as Feed and Food. Food Chem. Toxicol. 2017, 107, 108–121. [Google Scholar] [CrossRef] [Green Version]
  11. Brookes, G.; Barfoot, P. Global Income and Production Impacts of Using GM Crop Technology 1996–2014. GM Crops Food 2016, 7, 38–77. [Google Scholar] [CrossRef] [Green Version]
  12. Finger, R.; El Benni, N.; Kaphengst, T.; Evans, C.; Herbert, S.; Lehmann, B.; Morse, S.; Stupak, N. A Meta Analysis on Farm-Level Costs and Benefits of GM Crops. Sustainability 2011, 3, 743–762. [Google Scholar] [CrossRef] [Green Version]
  13. Züghart, W.; Benzler, A.; Berhorn, F.; Sukopp, U.; Graef, F. Determining Indicators, Methods and Sites for Monitoring Potential Adverse Effects of Genetically Modified Plants to the Environment: The Legal and Conceptional Framework for Implementation. Euphytica 2008, 164, 845–852. [Google Scholar] [CrossRef]
  14. Damgaard, C.; Kjellsson, G. Gene Flow of Oilseed Rape (Brassica napus) According to Isolation Distance and Buffer Zone. Agric. Ecosyst. Environ. 2005, 108, 291–301. [Google Scholar] [CrossRef] [Green Version]
  15. Dunfield, K.E.; Germida, J.J. Impact of Genetically Modified Crops on Soil- and Plant-Associated Microbial Communities. J. Environ. Qual. 2004, 33, 806–815. [Google Scholar] [CrossRef] [PubMed]
  16. Wen, Z.-L.; Yang, M.-K.; Du, M.-H.; Zhong, Z.-Z.; Lu, Y.-T.; Wang, G.-H.; Hua, X.-M.; Fazal, A.; Mu, C.-H.; Yan, S.-F.; et al. Enrichments/Derichments of Root-Associated Bacteria Related to Plant Growth and Nutrition Caused by the Growth of an EPSPS-Transgenic Maize Line in the Field. Front. Microbiol. 2019, 10, 1335. [Google Scholar] [CrossRef] [PubMed]
  17. Dunfield, K.E.; Germida, J.J. Seasonal Changes in the Rhizosphere Microbial Communities Associated with Field-Grown Genetically Modified Canola (Brassica napus). Appl. Environ. Microbiol. 2003, 69, 7310–7318. [Google Scholar] [CrossRef] [Green Version]
  18. Dunfield, K.E.; Germida, J.J. Diversity of Bacterial Communities in the Rhizosphere and Root Interior of Field-Grown Genetically Modified Brassica napus. FEMS Microbiol. Ecol. 2001, 38, 1–9. [Google Scholar] [CrossRef]
  19. Lee, Y.-E.; Yang, S.-H.; Bae, T.-W.; Kang, H.-G.; Lim, P.-O.; Lee, H.-Y. Effects of Field-Grown Genetically Modified Zoysia Grass on Bacterial Community Structure. J. Microbiol. Biotechnol. 2011, 21, 333–340. [Google Scholar] [CrossRef]
  20. Babujia, L.C.; Silva, A.P.; Nakatani, A.S.; Cantão, M.E.; Vasconcelos, A.T.R.; Visentainer, J.V.; Hungria, M. Impact of Long-Term Cropping of Glyphosate-Resistant Transgenic Soybean [Glycine max (L.) Merr.] on Soil Microbiome. Transgenic Res. 2016, 25, 425–440. [Google Scholar] [CrossRef]
  21. Lu, G.-H.; Zhu, Y.-L.; Kong, L.-R.; Cheng, J.; Tang, C.-Y.; Hua, X.-M.; Meng, F.-F.; Pang, Y.-J.; Yang, R.-W.; Qi, J.-L.; et al. Impact of a Glyphosate-Tolerant Soybean Line on the Rhizobacteria, Revealed by Illumina MiSeq. J. Microbiol. Biotechnol. 2017, 27, 561–572. [Google Scholar] [CrossRef] [Green Version]
  22. Banerjee, S.; van der Heijden, M.G.A. Soil Microbiomes and One Health. Nat. Rev. Microbiol. 2023, 21, 6–20. [Google Scholar] [CrossRef] [PubMed]
  23. Trinh, P.; Zaneveld, J.R.; Safranek, S.; Rabinowitz, P.M. One Health Relationships Between Human, Animal, and Environmental Microbiomes: A Mini-Review. Front. Public Health 2018, 6, 235. [Google Scholar] [CrossRef] [PubMed]
  24. Singh, B.K.; Liu, H.; Trivedi, P. Eco-Holobiont: A New Concept to Identify Drivers of Host-Associated Microorganisms. Environ. Microbiol. 2020, 22, 564–567. [Google Scholar] [CrossRef] [PubMed]
  25. Chun, S.-J.; Cui, Y.; Yoo, S.-H.; Lee, J.R. Organic Connection of Holobiont Components and the Essential Roles of Core Microbes in the Holobiont Formation of Feral Brassica Napus. Front. Microbiol. 2022, 13, 920759. [Google Scholar] [CrossRef]
  26. Pepoyan, A.Z.; Chikindas, M.L. Plant-Associated and Soil Microbiota Composition as a Novel Criterion for the Environmental Risk Assessment of Genetically Modified Plants. GM Crops Food 2019, 11, 47–53. [Google Scholar] [CrossRef] [PubMed]
  27. Kinderlerer, J. The Cartagena Protocol on Biosafety. Collect. Biosaf. Rev. 2008, 4, 12–65. [Google Scholar]
  28. Meyer, H. The Cartagena Protocol on Biosafety. Biotechnol. Dev. Monit. 2000, 43, 2–7. [Google Scholar]
  29. Moon, G.H. The Status of Biosafety Management and Control for Industrial Contained Use of LMOs. Food Sci. Ind. 2019, 52, 140–152. [Google Scholar] [CrossRef]
  30. Yamanouchi, K. Regulatory Considerations on Transgenic Livestock in Japan in Relation to the Cartagena Protocol. Theriogenology 2007, 67, 185–187. [Google Scholar] [CrossRef]
  31. Law Concerning the Conservation and Sustainable Use of Biological Diversity through Regulations on the Use of Living Modified Organisms (Law No. 97 of 2003). 30. Available online: http://www.env.go.jp/content/.pdf (accessed on 10 June 2023).
  32. Care, H.; Gene, A. Technology Act 2000. Available online: https://www.legislation.gov.au/Details/C2016C00792/ (accessed on 10 June 2023).
  33. Davison, J.; Bertheau, Y. EU Regulations on the Traceability and Detection of GMOs: Difficulties in Interpretation, Implementation and Compliance. CAB Rev. 2007, 2, 077. [Google Scholar] [CrossRef]
  34. Directive 2001/18/EC of the European Parliament and of the Council on the Deliberate Release into the Environment of Genetically Modified Organisms and Repealing Council Directive 90/220/EEC | UNEP Law and Environment Assistance Platform. Available online: https://leap.unep.org/countries/eu/national-legislation/directive-200118ec-european-parliament-and-council-deliberate (accessed on 10 June 2023).
  35. Kim, H.-C.; Kim, H.M. Risk Assessment of Genetically Modified Organisms. Risk Assess. Genet. Modif. Org. 2003, 19, s1008. [Google Scholar] [CrossRef]
  36. Oh, S.-W.; Kim, E.-H.; Lee, S.-Y.; Baek, D.-Y.; Lee, S.-G.; Kang, H.-J.; Chung, Y.-S.; Park, S.-K.; Ryu, T.-H. Compositional Equivalence Assessment of Insect-Resistant Genetically Modified Rice Using Multiple Statistical Analyses. GM Crops Food 2021, 12, 303–314. [Google Scholar] [CrossRef] [PubMed]
  37. Kim, E.-S. Technocratic Precautionary Principle: Korean Risk Governance of Genetically Modified Organisms. New Genet. Soc. 2014, 33, 204–224. [Google Scholar] [CrossRef]
  38. Choi, W.K.; Jo, B.H.; Seol, M.A.; Eum, S.J.; Park, J.H.; Song, H.R. Presence of Environmental Risk Assessments for LMOs in nature and Future Considerations based on New Biotechnologies. J. Korean Soc. Int. Agric. 2014, 26, 297–302. [Google Scholar] [CrossRef]
  39. Nam, K.-H.; Han, S.M. Seed Germination of Sunflower as a Case Study for the Risk Assessment and Management of Transgenic Plants Used for Environmental Remediation in South Korea. Sustainability 2020, 12, 10110. [Google Scholar] [CrossRef]
  40. European Food Safety Authority (EFSA). Guidance on the Environmental Risk Assessment of Genetically Modified Plants. EFSA J. 2010, 8, 1879. [Google Scholar] [CrossRef]
  41. Gray, A. Problem Formulation in Environmental Risk Assessment for Genetically Modified Crops: A Practitioner’s Approach. Collect. Biosaf. Rev. 2012, 6, 10–65. [Google Scholar]
  42. Gatew, H.; Mengistu, K. Genetically Modified Foods (GMOs); a Review of Genetic Engineering. J. World’s Poult. Res. 2019, 9, 157–163. [Google Scholar] [CrossRef]
  43. Convention on Biological Diversity. Guidance on Risk Assessment of Living Modified Organisms and Monitoring in the Context of Risk Assessment. 2016. UNEP/CBD/BS/COP-MOP/8/8/Add.1. Available online: https://www.cbd.int/doc/meetings/bs/mop-08/official/bs-mop-08-08-add1-en.pdf (accessed on 10 June 2023).
  44. Kuiper, H.A.; Davies, H.V. The SAFE FOODS Risk Analysis Framework Suitable for GMOs? A Case Study. Food Control 2010, 21, 1662–1676. [Google Scholar] [CrossRef]
  45. Transboundary Movement, Etc. of Living Modified Organisms Act. Available online: https://www.fao.org/faolex/results/details/en/c/LEX-FAOC195089/ (accessed on 10 June 2023).
  46. Saji, H.; Nakajima, N.; Aono, M.; Tamaoki, M.; Kubo, A.; Wakiyama, S.; Hatase, Y.; Nagatsu, M. Monitoring the Escape of Transgenic Oilseed Rape around Japanese Ports and Roadsides. Environ. Biosaf. Res. 2005, 4, 217–222. [Google Scholar] [CrossRef]
  47. Nakajima, N.; Nishizawa, T.; Aono, M.; Tamaoki, M.; Saji, H. Occurrence of Spilled Genetically Modified Oilseed Rape Growing along a Japanese Roadside Over 10 Years. Weed Biol. Manag. 2020, 20, 139–146. [Google Scholar] [CrossRef]
  48. Yoshimura, Y.; Beckie, H.J.; Matsuo, K. Transgenic oilseed rape along transportation routes and port of Vancouver in western Canada. Environ. Biosaf. Res. 2006, 5, 67–75. [Google Scholar] [CrossRef] [PubMed]
  49. Lim, H.S.; Kim, I.R.; Lee, S.H.; Choi, W.K.; Yoon, A.-M.; Lee, J.R. Establishment and Application of a Monitoring Strategy for Living Modified Cotton in Natural Environments in South Korea. Appl. Sci. 2021, 11, 10259. [Google Scholar] [CrossRef]
  50. Kim, Y.-C.; Kim, A.R.; Lim, J.P.; Kim, T.-S.; Park, S.-G.; Kim, M.H.; Lee, J.R.; Kim, D.-H. Distribution and Management of Nutria (Myocastor coypus) Populations in South Korea. Sustainability 2019, 11, 4169. [Google Scholar] [CrossRef] [Green Version]
  51. Kim, D.W.; Kim, I.R.; Lim, H.S.; Choi, W.K.; Lee, J.R. Development of Multiplex PCR Assay to Monitor Living Modified Cottons in South Korea. Appl. Sci. 2019, 9, 2688. [Google Scholar] [CrossRef] [Green Version]
  52. Hall, T. BIOEDIT: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/ NT. Available online: https://www.semanticscholar.org/paper/BIOEDIT%3A-A-USER-FRIENDLY-BIOLOGICAL-SEQUENCE-EDITOR-Hall/0ae262d9cf78536754bc064e07113ab5e978f208 (accessed on 10 June 2023).
  53. Eum, S.-J.; Kim, I.R.; Lim, H.S.; Lee, J.R.; Choi, W. Event-Specific Multiplex PCR Method for Four Genetically Modified Cotton Varieties, and Its Application. Appl. Biol. Chem. 2019, 62, 52. [Google Scholar] [CrossRef] [Green Version]
  54. Choi, W.; Lee, J.R.; Yoon, A.-M.; Yi, S.M.; Park, J.H.; Nam, K.-H.; Jung, Y.J.; Kim, I.R.; Chun, S.-J.; Lee, E.S.; et al. Detection Method for LMO in Natural Environment; National Institute of Ecology: Seocheon, Republic of Korea, 2022; pp. 1–143. [Google Scholar]
Applsci 13 07185 g001 550
Figure 1. Survey results of living modified organism (LMO) monitoring project from 2009 to 2013. (A) Number of LMO collected sites by year. (B) Distribution of LMO collection sites in South Korea.
Figure 1. Survey results of living modified organism (LMO) monitoring project from 2009 to 2013. (A) Number of LMO collected sites by year. (B) Distribution of LMO collection sites in South Korea.
Applsci 13 07185 g001
Applsci 13 07185 g002 550
Figure 2. Novel management scheme for priority management areas. (A) Process of general LMO monitoring. (B) Novel survey and management system for priority management areas (PMA) or LMO re-collection sites.
Figure 2. Novel management scheme for priority management areas. (A) Process of general LMO monitoring. (B) Novel survey and management system for priority management areas (PMA) or LMO re-collection sites.
Applsci 13 07185 g002
Applsci 13 07185 g003 550
Figure 3. Distribution of priority management areas in South Korea using the GIS system. Survey sites were assigned as priority management areas from 2014 to 2021. Management areas in six administrative districts: Gyeonggi-do (a), Gangwon-do (b), Chungcheong-do (c), Gyeongsang-do (d), Jeolla-do (e), and Jeju-do (f). Red circle indicates the distribution of priority management areas in South Korea.
Figure 3. Distribution of priority management areas in South Korea using the GIS system. Survey sites were assigned as priority management areas from 2014 to 2021. Management areas in six administrative districts: Gyeonggi-do (a), Gangwon-do (b), Chungcheong-do (c), Gyeongsang-do (d), Jeolla-do (e), and Jeju-do (f). Red circle indicates the distribution of priority management areas in South Korea.
Applsci 13 07185 g003
Applsci 13 07185 g004 550
Figure 4. Survey results of the priority management area for eight years. (A) The number of collected LMO samples through the nationwide LMO monitoring project (white bar) and priority management areas (black bar). (B) Crop type and the number of collected LMOs in priority management areas.
Figure 4. Survey results of the priority management area for eight years. (A) The number of collected LMO samples through the nationwide LMO monitoring project (white bar) and priority management areas (black bar). (B) Crop type and the number of collected LMOs in priority management areas.
Applsci 13 07185 g004
Applsci 13 07185 g005 550
Figure 5. Distribution of the priority management areas with 55 addresses in South Korea from 2014 to 2021. Information from supplementary Table S1 was reflected to show a location map of the priority management areas. The number indicates the priority management area assigned in six administrative districts; numbers 1–15 are in Gyeonggi-do (a), 16–18 in Gangwon-do (b), 19–31 in Chungcheong-do (c), 32–41 in Gyeongsang-do (d), 42–51 in Jeolla-do (e), and 52–55 in Jeju-do (f).
Figure 5. Distribution of the priority management areas with 55 addresses in South Korea from 2014 to 2021. Information from supplementary Table S1 was reflected to show a location map of the priority management areas. The number indicates the priority management area assigned in six administrative districts; numbers 1–15 are in Gyeonggi-do (a), 16–18 in Gangwon-do (b), 19–31 in Chungcheong-do (c), 32–41 in Gyeongsang-do (d), 42–51 in Jeolla-do (e), and 52–55 in Jeju-do (f).
Applsci 13 07185 g005
Table
Table 1. The number of living modified organism (LMO) collection sites and LMO plants in the same places from 2009 to 2013.
Table 1. The number of living modified organism (LMO) collection sites and LMO plants in the same places from 2009 to 2013.
20092010201120122013Total
LMO collection sites8 (19) a10 (12)10 (19)19 (42)18 (21)65 (113)
LMO re-collection sites5 (14) b3 (3)4 (11)8 (18)5 (6)25 (52)
a Number of LMO samples at LMO collection sites. b Number of LMO samples at LMO re-collection sites.
Table
Table 2. Number of LMOs and their collection site category in priority management areas.
Table 2. Number of LMOs and their collection site category in priority management areas.
Categories20142015201620172018201920202021Total
Roadside1939118482136155
Stockbreeding farm41373187101476
Feed factory002010221136
Port002121017
Other0201766325
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Lim, H.S.; Yoon, A.-M.; Kim, I.R.; Choi, W.; Jung, Y.J.; Lee, S.; Lee, J.R. Effectiveness of a Priority Management Scheme of Living Modified Organism Re-Collection Areas in Natural Environments of South Korea. Appl. Sci. 2023, 13, 7185. https://doi.org/10.3390/app13127185

AMA Style

Lim HS, Yoon A-M, Kim IR, Choi W, Jung YJ, Lee S, Lee JR. Effectiveness of a Priority Management Scheme of Living Modified Organism Re-Collection Areas in Natural Environments of South Korea. Applied Sciences. 2023; 13(12):7185. https://doi.org/10.3390/app13127185

Chicago/Turabian Style

Lim, Hye Song, A-Mi Yoon, Il Ryong Kim, Wonkyun Choi, Young Jun Jung, Sunghyeon Lee, and Jung Ro Lee. 2023. "Effectiveness of a Priority Management Scheme of Living Modified Organism Re-Collection Areas in Natural Environments of South Korea" Applied Sciences 13, no. 12: 7185. https://doi.org/10.3390/app13127185

APA Style

Lim, H. S., Yoon, A.-M., Kim, I. R., Choi, W., Jung, Y. J., Lee, S., & Lee, J. R. (2023). Effectiveness of a Priority Management Scheme of Living Modified Organism Re-Collection Areas in Natural Environments of South Korea. Applied Sciences, 13(12), 7185. https://doi.org/10.3390/app13127185

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop