Next Article in Journal
Climate Change-Related Temperature Impact on Human Health Risks of Vibrio Species in Bathing and Surface Water
Previous Article in Journal
Bioeconomy-Based Approaches for the Microbial Valorization of Citrus Processing Waste
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effects of Transgenic Insect-Resistant Maize HGK60 on Rhizosphere Soil Bacterial Communities

1
State Environmental Protection Key Laboratory of Regional Eco-Process and Function Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China
2
School of Ecology & Environment, Renmin University of China, Beijing 100782, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2025, 13(8), 1892; https://doi.org/10.3390/microorganisms13081892
Submission received: 27 May 2025 / Revised: 14 July 2025 / Accepted: 1 August 2025 / Published: 14 August 2025
(This article belongs to the Section Plant Microbe Interactions)

Abstract

While genetically modified crops bring significant economic benefits, the environmental safety issues they may pose have also received increasing attention. To study the impact of planting genetically modified insect-resistant crops on soil ecosystems, this research employed methods such as 16S rDNA amplicon full-length sequencing, using transgenic Cry1Ah insect-resistant corn HGK60 and its conventional counterpart Zheng 58 as subjects for a three-year continuous survey to analyze the effects of planting transgenic Cry1Ah insect-resistant corn HGK60 on the rhizosphere bacterial community. The following results were obtained. (1) A total of 216 corn rhizosphere soil samples were annotated to 51 phyla, 119 orders, 221 families, and 549 genera. (2) Overall, there was no significant difference in the composition of the rhizosphere bacterial community between HGK60 and Zheng 58 at the phylum, class, order, or family levels (p > 0.05), and the planting of HGK60 did not significantly affect the relative abundance of rhizosphere probiotics (p > 0.05). Some differences appeared only briefly and were not reproducible. (3) Alpha and beta diversity analyses showed that overall, the planting of HGK60 had no significant impact on the structure of the rhizosphere bacterial community (p > 0.05). (4) Significant changes in the rhizosphere bacterial community were observed across different growth stages of corn. It can be concluded that the planting of HGK60 has no significant impact on the rhizosphere bacteria. This study provides valuable data support for the environmental safety assessment of genetically modified crops.

1. Introduction

Food security is one of the most critical issues of this century [1]. As the fastest-growing biotechnology in modern times, genetically modified biotechnology plays a crucial role in addressing food problems. Genetically modified crops, which introduce beneficial genes into conventional crops, can provide sustainable agricultural and economic benefits for human society [2]. Since the first commercial planting of genetically modified crops in 1996, various types of genetically modified crops have been developed, including insect-resistant, herbicide-tolerant, virus-resistant, and dual-resistant crops [3,4]. The latest report shows that the planting area of genetically modified crops has increased from 1.7 million hectares in 1996 to 202.2 million hm2 in 2022, a growth of about 112 times, significantly enhancing global crop productivity [5].
Genetically modified crops, while bringing significant economic benefits, have increasingly attracted attention for their potential environmental safety issues. Whether their cultivation affects soil microorganisms has become one of the hot topics in recent studies. Soil microbial communities are a major component of the soil ecosystem [6], such as plant roots harboring a large number of microorganisms, primarily dominated by bacterial communities in their surrounding environment [7]. These rhizosphere bacteria, from plant pathogens to beneficial bacteria, significantly impact host plants, regulating nutrient uptake and host immunity [8,9]. Based on their different effects on plants, rhizosphere bacteria can be categorized into three types: beneficial, harmful, and neutral. Among these, there is a group of bacteria that have special interactions with plant roots and can promote plant growth; these are commonly known as plant rhizosphere probiotics (plant growth-promoting rhizobacteria, PGPR). PGPR have strong colonization capabilities in plant roots [10], inhibiting pathogens in the root zone, and can be used to control fungal, bacterial, and viral diseases [11]. They also promote plant growth, significantly increase seed germination rates, enhance root growth, and increase plant weight and yield [12,13]. PGPR mainly include Bacillus spp., Pseudomonas spp., Enterobacter spp., Klebsiella spp., Azotobacter spp., and others [12,14,15,16,17].
Transgenic crops, from planting to the end of their entire growth period, see the proteins expressed by exogenous genes in the plant body enter the soil ecosystem through pathways such as root secretion, making the soil ecosystem a significant site for the release of exogenous gene expression products [18]. To date, some studies have examined the impact of transgenic crops on rhizosphere microbial communities, but most have not found significant effects [19,20,21,22]. However, some studies show that compared to non-transgenic crops, there are notable changes in the rhizosphere microbial communities of transgenic crops [23,24]. An increasing number of scientists believe that scientific assessments of whether transgenic crops significantly affect soil microorganisms should follow the “case-by-case principle” [25], systematically analyzing changes in soil microbial diversity at different stages for specific varieties to determine their impact on soil microbial diversity.
Cry1Ah is an insecticidal gene from the Bt subspecies, with independent intellectual property rights in China. The Cry1Ah protein exhibits significant toxicity to Lepidoptera insects, showing markedly higher insecticidal efficiency compared to Cry1Ab and Cry1Ac, but relatively lower toxicity to economic insects such as silkworms [26]. Using the Cry1Ah gene, the insect-resistant corn HGK60 was obtained, which has clear molecular characteristics, single-point insertion, and genetic stability. Years of multi-site field trials have demonstrated that its resistance to field pests like corn borers and cotton bollworms is significantly better than that of conventional corn varieties. This study focuses on the insect-resistant corn HGK60 with the Cry1Ah gene and its control variety Zheng 58, examining the impact of planting Cry1Ah insect-resistant corn HGK60 on rhizosphere soil bacteria. The aim is to provide more detailed data to support the environmental safety assessment of Cry1Ah insect-resistant corn HGK60 and contribute to the healthy development of biosafety management.

2. Materials and Methods

2.1. Overview of the Research Area

The experimental site is located in the Langfang International Agricultural High-Tech Industrial Park (116°36′34″ E, 39°36′10″ N) in Hebei Province, characterized by a warm temperate continental monsoon climate with distinct monsoon features. The average annual temperature is approximately 11.9 °C, and the average annual precipitation is 554.9 mm, with most rainfall concentrated in summer. The average annual sunshine duration is about 2660 h, and the soil types are mainly sandy loam and clay loam.

2.2. Test Materials and Experimental Design

The Cry1Ah-transferred insect-resistant corn HGK60 (referred to as “HGK60”) and its control conventional corn Zheng 58 (referred to as “Zheng 58”) were provided by the Institute of Biotechnology, Chinese Academy of Agricultural Sciences (Beijing, China). The study employed a randomized block design. Both treatments, HGK60 and Zheng 58, were set up with six replicates (10 m × 10 m) planted in three consecutive seasons: early May 2019, 2020, and 2021. A 1-m isolation zone was established between different materials, and corn was sown using a one-hole-one-seed or one-hole-two-seeds method, maintaining a row spacing of 60 cm and a plant spacing of 25 cm. Field management practices, including irrigation, were consistent with local conventional corn cultivation methods. No chemical fertilizers or insecticides were applied during the growth period of the corn. Corn planting maintained a scientifically reasonable distance from other crops, ensuring that there were no wild relatives within the isolation zone.

2.3. Sample Collection

Samples of the rhizosphere soil were collected over six growth stages: pre-sowing, seedling stage, trumpet mouth stage, tasseling stage, full maturity stage, and post-harvest. Avoiding potential influencing factors such as roads, the sampling method followed the five-point method. After removing surface weeds, the corn plants were completely extracted, and their rhizomes were collected using the “shake root method” [27]. The samples were then stored at −80 °C and 4 °C for high-throughput sequencing.

2.4. Full-Length Sequencing of 16S rDNA Amplification

(1) DNA extraction: The FastDNA ® SPIN Kit for soil (MP Biomedicals, Santa Ana, CA, USA) was used to extract the total DNA of maize rhizosphere soil microorganisms.
(2) PCR amplification. Region: V1 to V9 full length; template: diluted genomic DNA; Primers: 8F (5′-AGAGTTTGATCCTGGCTCAG-3′), 1509R (5′-GNTACCTTGTTACGACTT-3′); enzyme and buffer from TransStart® FastPfu DNA Polymerase (TransGen Biotech, Beijing, China); PCR reaction system (50 μL): 1 μL Trans Fastpfu,10 μL 5 × buffer, 5 μL 5 × StimuLate, 5 μL dNTPs (2.5 × 10−3 mol/L each), 2 μL primer mix (1 μmol/L), 1 μL gDNA, 26 μL NFW. PCR reaction conditions: pre-denaturation at 98 °C (2 min), denaturation at 95 °C (30 s), annealing at 60 °C (45 s), extension at 72 °C (90 s), followed by 35 cycles, then 10 min at 72 °C for final extension. After mixing samples, electrophoresis was performed using agarose gel (1 × TAE concentration 2%) to purify the PCR product, and the target band was recovered by gel cutting. The reagent kit used was the QIAquick@Gel Extraction Kit gel recovery kit (Qiagen, Düsseldorf, Germany).
(3) High-throughput sequencing: The library was constructed using the SMRTbellTM Template Prep Kit (Pacific Biosciences, Menlo Park, CA, USA). The fragment size was quantified by Qubit and detected by FEMTO Pulse. After qualification, 16S full-length rDNA sequencing was performed. This research was assisted by Beijing Novogene Bioinformatics Technology Co., Ltd. (Beijing, China).

2.5. Statistical Analysis of Diversity and Structure of Bacterial Communities

The alpha diversity index can effectively reflect the number, abundance, and distribution of species in a community. Common indices of alpha diversity include the Shannon index, Simpson’s index, PD index, coverage index, etc.

2.6. Data Processing and Analysis

(1) Sequencing data processing: After the data were downloaded, CCS (SMRT Link v7.0) was used to correct the sequences, perform SSR filtering, and remove primers to obtain the final valid data. (2) OTU Clustering and Species Annotation: The obtained valid data were clustered using Uparse software (Uparse v7.0.1001) with 97% identity to generate OTUs (operational taxonomic units). Species annotations for each OTU were performed using the Mothur method at various taxonomic levels, and normalization was applied to each sample based on minimum data volume. (3) Sample complexity analysis (alpha diversity): Dilution curves were plotted using R software (Version 2.15.3); alpha diversity indices were calculated using Qiime software (Version 1.9.1). (4) Comparative analysis of multiple samples (beta diversity): Principal coordinate analysis (PCoA), similarity analysis (analysis of similarities, Anosim), and non-weighted group average analysis based on the Bray–Curtis distance (unweighted pair group method with arithmetic mean, UPGMA) were all carried out using R software (Version 2.15.3).

3. Results

High-throughput sequencing was performed on 216 soil samples, clustering them into 10,673 OTUs with 97% identity. The corn rhizosphere soil samples were annotated to 51 phyla, 60 classes, 119 orders, 221 families, and 549 genera. Both the dilution curve (Figure 1) and the abundance rank curve (Figure 2) showed gradual flattening as the sequencing volume increased, indicating uniform species distribution and progressively reasonable data volumes, suitable for subsequent scientific analysis. In 2019, the number of OTUs shared between HGK60 and Zheng 58 was 3315; HGK60 had 1659 OTUs, and Zheng 58 had 1699 OTUs. In 2020, the number of OTUs shared between HGK60 and Zheng 58 was 3713; HGK60 had 1904 OTUs, and Zheng 58 had 1938 OTUs. In 2021, the number of OTUs shared between HGK60 and Zheng 58 was 3227; HGK60 had 1688 OTUs, and Zheng 58 had 1736 OTUs (Figure 3).

3.1. Relative Abundance of Rhizosphere Soil Bacterial Species

At the phylum level, the relative abundance of rhizosphere soil bacteria in each year and reproductive stage was analyzed. Proteobacteria and Acidobacteria accounted for more than 15% in all samples during each period, making them dominant bacterial groups. Next were Firmicutes, Cyanobacteria, Chloroflexi, Bacteroidetes, Actinobacteria, Gemmatimonadetes, Planctomycetes, and Nitrospirae (Figure 4). At the class level, Gammaproteobacteria, Bacilli, unidentified Cyanobacteria, unidentified Acidobacteria, Anaerolineae, Bacteroidia, Acidobacteria, Alphaproteobacteria, unidentified Actinobacteria, and Clostridia were the top 10 species in relative abundance (Figure 4). Overall, the relative abundance of rhizosphere soil bacteria at the phylum and class levels between HGK60 and Zheng 58 during the same growth period of corn in the same season was not significantly different (p > 0.05). Differences at either the phylum or class levels only briefly appeared during a specific growth period and did not recur across multiple growth periods. For example, cyanobacteria showed significant differences between HGK60 and Zheng 58 during the seedling stage and earing stage in 2020 (p < 0.05), but these differences did not appear during the various growth periods in 2019 and 2021 and were not significant after the harvest of three seasons of corn (p > 0.05).
A clustering heatmap of relative abundance was created for the top 35 families (Figure 5), and a species phylogenetic tree was drawn for the top 100 genera (Figure 6). The species abundance of HGK60 and Zheng 58 at the family level and genus level during the same growth period was compared. Overall, there were no significant differences between HGK60 and Zheng 58. The brief differences that appeared did not recur during the survey, such as in the subfamily Microcystis (Leptolyngbyaceae) and the family Digestion Actinomycetes (Peptostreptococcaceae), which showed significant differences only between HGK60 and Zheng 58 during the seedling stage in 2020; the genus Sphingorhabdus only showed a significant difference in 2019 during the trumpet mouth stage, with HGK60 being significantly lower than Zheng 58; the genera Coniobacter (Conexibacter), Parasegetibacter, Luteimonas, and Pseudococcus (Paeniclostridium) only showed significant differences between HGK60 and Zheng 58 during a certain growth period in 2020; and the genus Rhizoctonia (Ralstonia) only showed a significant difference in 2021 during the full maturity stage, with HGK60 being significantly higher than Zheng 58. Although these families or genera experienced significant increases or decreases in relative abundance at some stages, this change did not persist across all growth periods over three consecutive years. It is believed that these brief differences are more likely due to uncontrollable factors in the field rather than the result of planting HGK60.
On the other hand, common plant rhizosphere-promoting bacteria from the top 200 relative abundance genera were screened, mainly including Bacillus, Arthrobacter, Bradyrhizobium, Streptomyces, Herbaspirillum, Flavobacterium, Pseudomonas, and Azospirillum. The relative abundance of rhizosphere-promoting bacteria in the rhizosphere soil microorganisms of HGK60 and Zheng 58 at different growth stages over various years was compared (Figure 7). Bacillus, Rhizobium, and Rhizobium showed no significant differences between HGK60 and Zheng 58 across all growth stages from 2019 to 2021. Actinobacillus showed significant differences between HGK60 and Zheng 58 only during the seedling stage in 2019 and 2021, but in 2019, HGK60 was significantly lower than Zheng 58, while in 2021, it was the opposite. Streptomyces showed a significant advantage for HGK60 over Zheng 58 after harvest in 2019. Bacillus showed significant differences between HGK60 and Zheng 58 before sowing and after harvest in 2019, and during the heading stage in 2021, but in 2019, HGK60 was significantly higher than Zheng 58, and in 2021, it was significantly lower than Zheng 58. Pseudomonas showed a significant advantage for HGK60 over Zheng 58 only during the late growth stage in 2021. Azotobacter showed significant differences between HGK60 and Zheng 58 only during the seedling stage in 2019. Significant differences between HGK60 and Zheng 58 only occurred at certain stages, and there was no consistency or persistence. It was concluded that the planting of HGK60 had no significant effect on rhizosphere probiotics.

3.2. Diversity and Structure of Bacterial Communities

The alpha diversity index can effectively reflect the number, abundance, and distribution of species within a community. Analysis of the Shannon index, Simpson’s index, PD index, and coverage index for root soil bacterial communities at different growth stages of HGK60 and Zheng 58 (Figure 8) shows that there is no significant difference between HGK60 and Zheng 58 in any of these indices (p > 0.05), indicating that the planting of HGK60 has no significant impact on the alpha diversity of root soil bacteria. Beta diversity analysis is mainly used to compare differences in the overall structure of microbial communities across samples. PCoA and Anosim analysis results (Figure 9) show that in 2019, there were significant differences during the seedling stage (R = 0.383, p = 0.002) and the heading stage (R = 0.279, p = 0.011). In 2020, no significant differences were observed throughout the entire growth period. In 2021, only during the trumpet stage (R = 0.397, p = 0.005) did significant differences emerge. After three consecutive years of harvest, no significant differences in community structure between HGK60 and Zheng 58 were observed (p > 0.05). The UPGMA dendrogram based on the Bray–Curtis distance (Figure 10) shows that, except for the trumpet stage in 2021, root soil samples from all growth stages in 2019–2021 clustered together, indicating similar bacterial community structures. On the other hand, clear separation was observed across different growth stages, suggesting that growth stage is a crucial factor influencing the structure of soil bacterial communities, rather than the planting of HGK60.

4. Discussion

The insecticidal proteins released by genetically modified crops can enter the soil through various pathways, such as crop residues and root exudates, altering the soil environment around the crops. This, in turn, affects soil biodiversity and ultimately poses a threat to the soil ecosystem [28]. Currently, many experts have conducted risk assessments of soil ecosystems for different genetically modified crops, but the conclusions vary [4,29], and there is no clear consensus on the environmental safety issues that may arise from planting genetically modified crops.
This study employed third-generation high-throughput sequencing to investigate the impact of HGK60 planting on rhizosphere soil bacteria. Analysis of bacterial relative abundance at different taxonomic levels revealed that, overall, there were no significant differences in the phyla, classes, and orders between the rhizosphere soil bacteria of HGK60 and Zheng 58 during the same growth period. Occasional differences only appeared during certain growth periods and had a short duration, weakening to non-significant levels within a short time frame. This finding is similar to the results reported by Widmer et al. [30,31,32], who concluded that the planting of HGK60 did not have a sustained or significant effect on the relative abundance of rhizosphere soil bacteria. Additionally, this study screened for rhizosphere-promoting bacteria with relatively high abundance in corn rhizosphere soil. The analysis showed that the planting of HGK60 did not cause any significant differences in the abundance of rhizosphere-promoting bacteria such as Bacillus, Rhizobium, and Sinorhizobium. The effects on Rhizobium, Streptomyces, Pseudomonas, Pseudomonas fluorescens, and Azorhizobium were only occasional and lacked persistence and repeatability. It can be said that the planting of insect-resistant maize with the Cry1Ah gene in HGK60 has no significant impact on major rhizosphere-promoting bacteria. Based on current literature reviews, studies on the impact of genetically modified crop planting on rhizosphere-promoting bacteria are relatively scarce. Further research is needed to extend the study duration and broaden the scope to validate our findings.
The results of the sample complexity and comparative analysis show that the alpha diversity index of rhizosphere soil bacteria between HGK60 and Zheng 58 was not significantly different across various growth stages from 2019 to 2021. PCoA and Anosim analyses indicate that the community structure of rhizosphere soil bacteria in HGK60 and Zheng 58 during the same period was relatively similar, with little overall difference. Significant differences only briefly appeared in a certain year and growth stage, and after harvest, the differences between HGK60 and Zheng 58 were not significant. UPGMA analysis also shows that planting HGK60 did not significantly affect the beta diversity of rhizosphere soil bacterial communities [32,33]. These results all indicate that planting HGK60 does not significantly impact the diversity of corn rhizosphere soil bacteria. Although plants can alter their rhizosphere microbial communities by modifying root exudates [34,35,36], the introduction of Cry1Ah exogenous genes did not reach a significant level of influence on the rhizosphere soil bacteria of corn. Some existing research findings corroborate this study’s results, suggesting that genetically modified crops do not significantly affect soil microbial community diversity [37,38]. Fan et al. conducted a two-year trial on insect-resistant genetically modified corn carrying the Cry1le gene and found no significant impact on soil biodiversity [39]; Fazal et al.’ s study on mcry1Ab and mcray2Ab gene-transferred corn showed that its planting had minimal impact on the rhizosphere soil bacterial community, which can be disregarded [40]. In addition, the results of this study show that the growth stage is the primary factor influencing the structure of soil bacterial communities in corn rhizosphere, with significant differences observed across different growth stages, consistent with some existing research findings [32,33]. The enrichment of crop rhizosphere microorganisms is positively correlated with the degree of crop growth and development and interacts with the surrounding environment to gradually form a rhizosphere microenvironment [41]. The differences in soil rhizosphere bacterial community structures at different growth stages of corn may be due to variations in root biomass and hormone levels during different growth and developmental phases, leading to differences in root exudates [42].

5. Conclusions

The research findings indicate that the planting of insect-resistant corn HGK60 with the Cry1Ah gene had no significant impact on the bacterial communities in the rhizosphere soil. The partial effects were relatively short-lived and did not persist beyond the corn harvest, and there was no reproducibility across different years. Although this study has reached relatively clear conclusions and innovatively examined the impact of insect-resistant corn HGK60 with the Cry1Ah gene from the perspective of rhizosphere probiotics, the environmental safety assessment of genetically modified crops is a long-term process that requires more extensive and in-depth research to ultimately scientifically determine whether GM crops pose any threat to the environment. Of course, differences between species, differences in inserted genes, variations in research methods, field management practices, and uncontrollable climatic factors can all interfere with the ecological safety studies of GM crops. It is essential to fully adhere to the “case-by-case principle” [25] and conduct follow-up studies on resistance varieties obtained through the introduction of different exogenous genes, taking into account external environmental disturbances, to facilitate the rapid development of GM breeding.

Author Contributions

Conceptualization, Y.C. and X.G.; methodology, Y.C.; software, L.P. and Q.W.; validation, X.G. and N.X.; formal analysis, J.Y.; investigation, Y.C. and J.Y.; resources, X.G. and N.X.; data curation, L.P.; writing—original draft preparation, Y.C., J.Y., L.P. and M.L.; writing—review and editing, N.X. and X.G.; visualization, Y.C. and J.Y.; supervision, X.G. and N.X.; project administration, funding acquisition, X.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Science and Technology Major Project of the Ministry of Science and Technology of China, grant number 2016ZX08012005.

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. Ramankutty, N.; Mehrabi, Z.; Waha, K.; Jarvis, L.; Kremen, C.; Herrero, M.; Rieseberg, L.H. Trends in global agricultural land use: Implications for environmental health and food security. Annu. Rev. Plant Biol. 2018, 69, 789–815. [Google Scholar] [CrossRef]
  2. Catacora-Vargas, G.; Binimelis, R.; Myhr, A.I.; Wynne, B. Socio-economic research on genetically modified crops: A study of the literature. Agric. Hum. Values 2018, 35, 489–513. [Google Scholar] [CrossRef]
  3. Anderson, J.A.; Ellsworth, P.C.; Faria, J.C.; Head, G.P.; Owen, M.D.K.; Pilcher, C.D.; Shelton, A.M.; Meissle, M. Genetically engineered crops: Importance of diversified integrated pest management for agricultural sustainability. Front. Bioeng. Biotechnol. 2019, 7, 24. [Google Scholar] [CrossRef] [PubMed]
  4. Kumar, K.; Gambhir, G.; Dass, A.; Tripathi, A.K.; Singh, A.; Jha, A.K.; Yadava, P.; Choudhary, M.; Rakshit, S. Genetically modified crops: Current status and future prospects. Planta 2020, 251, 91. [Google Scholar] [CrossRef] [PubMed]
  5. Li, H.; Lui, C.; Zhang, H.; Wang, X.; Tang, Q. Global Genetically Modified Crop Industrialization Trends in 2022. J. Agric. Sci. Technol. 2023, 25, 6–16. [Google Scholar]
  6. Berendsen, R.L.; Pieterse, C.M.; Bakker, P.A. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012, 17, 478–486. [Google Scholar] [CrossRef]
  7. Rahman, M.K.U.; Zhou, X.G.; Wu, F.Z. The role of root exudates, CMNs, and VOCs in plant–plant interaction. J. Plant Interact. 2019, 14, 630–636. [Google Scholar] [CrossRef]
  8. Bai, Y.C.; Chang, Y.Y.; Hussain, M.; Lu, B.; Pei, D. Soil chemical and microbiological properties are changed by long-term chemical fertilizers that limit ecosystem functioning. Microorganisms 2020, 28, 694. [Google Scholar] [CrossRef]
  9. Trivedi, P.; Leach, J.E.; Tringe, S.G.; Sa, T.; Singh, B.K. Plant–microbiome interactions: From community assembly to plant health. Nat. Rev. Microbiol. 2020, 18, 607–621. [Google Scholar] [CrossRef]
  10. Ryu, C.M.; Farag, M.A.; Hu, C.H.; Reddy, M.S. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA 2003, 100, 4927–4932. [Google Scholar] [CrossRef]
  11. Gao, X.; Yao, S.; Joachim, V.; Wang, J. Analysis of Antibacterial Substances Produced by Bacillus subtilis B2 Strain. Chin. J. Biol. Control 2003, 19, 175–179. [Google Scholar]
  12. Kloepper, J.W.; Ryu, C.M.; Zhang, S. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 2008, 94, 1259–1266. Phytopathology 2008, 94, 1259–1266. [Google Scholar] [CrossRef]
  13. Shao, J.H.; Xu, Z.H.; Zhang, N.; Shen, Q.R.; Zhang, R.F. Contribution of indole-3-acetic acid in the plant growth promotion by the rhizospheric strain Bacillus amyloliquefaciens SQR9. Biol. Fertil. Soils 2015, 51, 321–330. [Google Scholar] [CrossRef]
  14. Kuklinsky-Sobral, J.; Araújo, W.L.; Mendes, R.; Geraldi, I.O.; Pizzirani-Kleiner, A.A.; Azevedo, J.L. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 2004, 6, 1244–1251. [Google Scholar] [CrossRef]
  15. Bhattacharyya, P.N.; Jha, D.K. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World J. Microbiol. Biotechnol. 2012, 28, 1327–1350. [Google Scholar] [CrossRef]
  16. Thokchom, E.; Kalita, M.C.; Talukdar, N.C. Isolation, screening, characterization, and selection of superior rhizobacterial strains as bioinoculants for seedling emergence and growth promotion of Mandarin orange (Citrus reticulata Blanco). Can. J. Microbiol. 2014, 60, 85–92. [Google Scholar] [CrossRef] [PubMed]
  17. Haiyambo, D.H.; Chimwamurombe, P.M.; Reinhold-Hurek, B. Isolation and screening of rhizosphere bacteria from grasses in east Kavango Region of Namibia for plant growth promoting characteristics. Curr. Microbiol. 2005, 71, 566–571. [Google Scholar] [CrossRef] [PubMed]
  18. Saxena, D.; Flores, S.; Stotzky, G. Bt Toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events. Soil Biol. Biochem. 2002, 34, 133–137. [Google Scholar] [CrossRef]
  19. Khan, M.S.; Ahmad, H.; Ullah, M.; Ahmed, M.Z. Allelopathic assessment for the environmental biosafety of the transgenic oilseed rape lines harboring the antifungal synthetic chitinase (NiC) gene. Pak. J. Bot. 2019, 51, 1465–1472. [Google Scholar] [CrossRef] [PubMed]
  20. Li, P.; Li, Y.C.; Shi, J.L.; Yu, Z.B.; Pan, A.H.; Tang, X.M.; Ming, F. Impact of transgenic Cry1Ac+ CpTI cotton on diversity and dynamics of rhizosphere bacterial community of different root environments. Sci. Total Environ. 2018, 637, 233–243. [Google Scholar] [CrossRef]
  21. Tang, T.; Chen, G.M.; Liu, F.X.; Bu, C.P.; Liu, L.; Zhao, X.X. Effects of transgenic glufosinate-tolerant rapeseed (Brassica napus L.) and the associated herbicide application on rhizospheric bacterial communities. Physiol. Mol. Plant Pathol. 2019, 106, 246–252. [Google Scholar] [CrossRef]
  22. Canfora, L.; Sbrana, C.; Avio, L.; Felici, B.; Scatà, M.C.; Neri, U.; Benedetti, A. Risk management tools and the case study Brassica napus: Evaluating possible effects of genetically modified plants on soil microbial diversity. Sci. Total Environ. 2014, 493, 983–994. [Google Scholar] [CrossRef] [PubMed]
  23. 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]
  24. Zhang, M.J.; Feng, M.C.; Xiao, L.J.; Song, X.Y.; Ding, G.W.; Yang, W.D. Persistence of Cry1Ac protein from transgenic Bt cotton cultivation and residue returning in fields and its effect on functional diversity of soil microbial communities. Pedosphere 2019, 29, 114–122. [Google Scholar] [CrossRef]
  25. Liu, B.; Han, J.; Xue, K. Progress in the environmental monitoring of transgenic plants. Acta Ecol. Sin. 2016, 36, 2490–2496. [Google Scholar] [CrossRef]
  26. Li, X.Y.; Lang, Z.H.; Zhang, J.; He, K.L.; Zhu, L.; Huang, D.F. Acquisition of insect-resistant transgenic maize harboring a truncated cry1Ah gene via Agrobacterium-mediated transformation. J. Integr. Agric. 2014, 13, 937–944. [Google Scholar] [CrossRef]
  27. Teixeira, L.C.R.S.; Peixoto, R.S.; Cury, J.C.; Sul, W.J.; Pellizari, W.H.; Tiedje, J.; Rosado, A.S. Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J. 2010, 4, 989–1001. [Google Scholar] [CrossRef]
  28. Mandal, A.; Sarkar, B.; Owens, G.; Thakur, J.K.; Manna, M.C.; Niazi, N.K.; Jayaraman, S.; Patra, A.K. Impact of genetically modified crops on rhizosphere microorganisms and processes: A review focusing on Bt cotton. Appl. Soil Ecol. 2020, 148, 103492. [Google Scholar] [CrossRef]
  29. Singh, A.K.; Dubey, S.K. Current trends in Bt crops and their fate on associated microbial community dynamics: A review. Protoplasma 2016, 253, 663–681. [Google Scholar] [CrossRef]
  30. Liu, B.; Zeng, Q.; Yan, F.M.; Xu, H.G.; Xu, C.R. Effects of transgenic plants on soil microorganisms. Plant Soil 2005, 271, 1–13. [Google Scholar] [CrossRef]
  31. Widmer, F. Assessing effects of transgenic crops on soil microbial communities. In Green Gene Technology; Springer: Berlin/Heidelberg, Germany, 2007; pp. 207–234. [Google Scholar]
  32. Chen, Y.; Li, J.; Yan, B.; Guan, X.; Tao, J. Impact of Transgenic Insect-Resistant Maize HGK60 with Cry1AhGene on Biodiversity in the Fields. Res. Environ. Sci. 2021, 34, 964–975. [Google Scholar]
  33. Li, X.; Liu, B.; Xu, W.; Cao, W.; Fang, Z.; Liu, D.; He, Z.; Han, Z. Effect of Transgenic Bt Cotton on Biodiversity of Soil Microbial Community. J. Ecol. Rural Environ. 2011, 27, 17–22. [Google Scholar]
  34. Badri, D.V.; Vivanco, J.M. Regulation and function of root exudates. Plant Cell Environ. 2010, 32, 666–681. [Google Scholar] [CrossRef]
  35. Hamid, M.I.; Hussain, M.; Wu, Y.; Zhang, X.; Xiang, M.; Liu, X. Successive soybean-monoculture cropping assembles rhizosphere microbial communities for the soil suppression of soybean cyst nematode. FEMS Microbiol. Ecol. 2017, 93, fiw222. [Google Scholar] [CrossRef] [PubMed]
  36. Li, C.X.; Tian, Q.; Rahman, M.K.; Wu, F.Z. Effect of anti-fungal compound phytosphingosine in wheat root exudates on the rhizosphere soil microbial community of watermelon. Plant Soil 2020, 456, 223–240. [Google Scholar] [CrossRef]
  37. Filion, M. Do transgenic plants affect rhizobacteria populations? Microb. Biotechnol. 2008, 1, 463–475. [Google Scholar] [CrossRef]
  38. Sun, C.S.; Geng, L.L.; Wang, M.L.; Shao, G.X.; Liu, Y.F.; Shu, C.L.; Zhang, J. No adverse effects of transgenic maize on population dynamics of endophytic Bacillus subtilis strain B916-gfp. Microbiol. Open 2016, 6, e00404. [Google Scholar]
  39. Fan, C.; Wu, F.C.; Dong, J.Y.; Wang, B.F.; Song, X.Y. No impact of transgenic cry1Ie maize on the diversity, abundance and composition of soil fauna in a 2-year field trial. Sci. Rep. 2019, 9, 10333. [Google Scholar] [CrossRef]
  40. Fazal, A.; Wen, Z.L.; Lu, Y.T.; Hua, X.M.; Yang, M.K.; Yin, T.M.; Han, H.W.; Lin, H.Y.; Wang, X.M.; Lu, G.H.; et al. Assembly and shifts of the bacterial rhizobiome of field grown transgenic maize line carrying mcry1ab and mcry2Ab genes at different developmental stages. Plant Growth Regul. Int. J. Nat. Synth. Regul. 2020, 91, 113–126. [Google Scholar] [CrossRef]
  41. Du, K.; Li, J.; Wang, T.; Zhang, J.; Wang, M.; Wang, Y. Physicochemical properties and fungal community diversity in rhizosphere soil of transgenie glyphosate resistant Brassica napus. Chin. J. Ecol. 2024, 43, 1082–1091. [Google Scholar]
  42. Houlden, A.; Timms-Wilson, T.M.; Day, M.J.; Bailey, M.J. Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol. Ecol. 2008, 65, 193–201. [Google Scholar] [CrossRef]
Figure 1. Rarefaction curve.
Figure 1. Rarefaction curve.
Microorganisms 13 01892 g001
Figure 2. Rank abundance.
Figure 2. Rank abundance.
Microorganisms 13 01892 g002
Figure 3. Venn diagrams. A: HGK60, B: Zheng 58. The same below.
Figure 3. Venn diagrams. A: HGK60, B: Zheng 58. The same below.
Microorganisms 13 01892 g003
Figure 4. The relative abundance of the top 10 soil bacteria. 1: Pre-planting stage, 2: Seeding stage, 3: Bell stage, 4: Heading stage, 5: Fully ripe stage, 6: Post-harvest stage. The same below.
Figure 4. The relative abundance of the top 10 soil bacteria. 1: Pre-planting stage, 2: Seeding stage, 3: Bell stage, 4: Heading stage, 5: Fully ripe stage, 6: Post-harvest stage. The same below.
Microorganisms 13 01892 g004
Figure 5. Cluster heatmap of the relative abundance of bacteria at the family level.
Figure 5. Cluster heatmap of the relative abundance of bacteria at the family level.
Microorganisms 13 01892 g005
Figure 6. The phylogenetic tree at the genus level.
Figure 6. The phylogenetic tree at the genus level.
Microorganisms 13 01892 g006
Figure 7. The relative abundance of rhizosphere-promoting bacteria.
Figure 7. The relative abundance of rhizosphere-promoting bacteria.
Microorganisms 13 01892 g007
Figure 8. Alpha diversity analysis.
Figure 8. Alpha diversity analysis.
Microorganisms 13 01892 g008
Figure 9. Principal coordinate analysis.
Figure 9. Principal coordinate analysis.
Microorganisms 13 01892 g009
Figure 10. UPGMA clustering tree based on Bray–Curtis distance.
Figure 10. UPGMA clustering tree based on Bray–Curtis distance.
Microorganisms 13 01892 g010
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

Chen, Y.; Yang, J.; Pan, L.; Liu, M.; Wang, Q.; Xiao, N.; Guan, X. Effects of Transgenic Insect-Resistant Maize HGK60 on Rhizosphere Soil Bacterial Communities. Microorganisms 2025, 13, 1892. https://doi.org/10.3390/microorganisms13081892

AMA Style

Chen Y, Yang J, Pan L, Liu M, Wang Q, Xiao N, Guan X. Effects of Transgenic Insect-Resistant Maize HGK60 on Rhizosphere Soil Bacterial Communities. Microorganisms. 2025; 13(8):1892. https://doi.org/10.3390/microorganisms13081892

Chicago/Turabian Style

Chen, Yanjun, Junyi Yang, Libo Pan, Meng Liu, Qiuming Wang, Nengwen Xiao, and Xiao Guan. 2025. "Effects of Transgenic Insect-Resistant Maize HGK60 on Rhizosphere Soil Bacterial Communities" Microorganisms 13, no. 8: 1892. https://doi.org/10.3390/microorganisms13081892

APA Style

Chen, Y., Yang, J., Pan, L., Liu, M., Wang, Q., Xiao, N., & Guan, X. (2025). Effects of Transgenic Insect-Resistant Maize HGK60 on Rhizosphere Soil Bacterial Communities. Microorganisms, 13(8), 1892. https://doi.org/10.3390/microorganisms13081892

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