Bacillus thuringiensis pesticidal toxins: A global analysis based on scientometric study (1980 – 2021)

doi:10.21203/rs.3.rs-1499179/v1

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Systematic Review

Bacillus thuringiensis pesticidal toxins: A global analysis based on scientometric study (1980 – 2021)

https://doi.org/10.21203/rs.3.rs-1499179/v1

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published 31 Jul, 2023

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Background: Several studies have been conducted on Bacillus thuringiensis (Bt) pesticidal toxins due to their successful environmentally friendly biopesticide activity against various insect pest orders, protozoa, mites, and nematodes. However, no existing study has systematically examined the trends and evolution of research on Bt pesticidal toxins from a scientometric perspective. This study aimed to analyze the trends and hotspots of global research in this field.

Methodology: 5757 publications on Bt pesticidal toxins were extracted from the Web of Science Core Collection (WoS) from 1980 to 2021. Statistical and scientometric analyses were performed using Excel, CiteSpace and VOSviewer visualisation tools to evaluate the contributions of different countries, institutions, highly influential references, and most used keywords.

Results: Out of the 5757 publications, the USA contributed the most, with 1562 publications, 72,754 citations, and 46.58 average citations per paper (ACPP); however, Belgium had the highest (106.43) ACPP among the top 20 contributing countries. The Chinese Academy of Agricultural Sciences is the leading institution with 298 publications and 21.20 ACPP. The Pasteur Institute is ranked first (90.04) in terms of ACPP. Keywords analyses revealed that recent studies are inclined towards the evolution of insect resistance against Bt toxins.

Conclusion: In future, studies related to the development of resistance mechanisms by insects against Bt pesticidal toxins and ways to overcome them will likely receive more attention.

Agricultural Engineering

General Microbiology

Bacteriology

Plant Molecular Biology and Genetics

Bacillus thuringiensis

Cry protein

CiteSpace

VOSviewer

Biopesticide

Scientometric

Toxin

Bacillus thuringiensis (Bt) is a Gram-positive, rod-shaped, motile, and aerobic or facultative anaerobic bacterium that produces insecticidal crystal inclusions, known as δ-endotoxins or Cry proteins, during its sporulation phase of growth. These Cry proteins have been proven to be effective against important crop pests, and also against mosquitoes that are vehicles of serious human diseases such as malaria and dengue [1].

Bt is known as the most successful environmentally friendly insecticidal microbe which acts against different orders of insect pests, such as Lepidoptera, Coleoptera, Diptera, Homoptera, Hymenoptera, Mallophaga and Orthoptera [2]. Also, certain Bt strains have revealed activity against protozoa, mites, and nematodes [3–5]. Unfortunately, there are still many insect pests that have shown poorly controlled or no susceptibility to the known Cry proteins [5]. Furthermore, the emergence of insect resistance to Bt crops in the field, which represents a major threat for using the Cry toxins, have been reported for at least five different insect species [6–10]. Therefore, discovering novel Cry toxin proteins in nature or through in vitro genetic evolution of them to enhance their toxicity against specific pests insects is of utmost importance [11–13]. During the past decade, a considerable number of studies on B. thuringiensis have been published so far, and pesticidal Cry proteins were the subject of intensive research [2, 14, 15]. These efforts have yielded large literature and plentiful data about the Cry proteins’ structure, mechanism of action, genetics, ecological role, performance in agricultural and other natural settings, and the evolution of resistance mechanisms in target pests [1, 2, 16, 17]. Given the importance of Cry proteins, many scholars and academic journals have focused on specific subfields of Cry proteins (which are mentioned above), with conclusions being drawn from systematic reviews or descriptive analysis. However, to our knowledge, there is no existing study that has systematically examined this field from a scientometric perspective.

Scientometric is a branch of informatics that combines information visualization technology and mathematical methods to quantitatively analyze scientific literature and understand emerging trends and the knowledge structure of a scientific research field [18, 19]. It evaluates the contributions of authors, institutions, countries, and journals in specific fields; and primarily it concentrates on the quantification properties of literature, such as publication numbers, citation frequency, and cooperative relationships [20]. Therefore, a scientometric study can help researchers to identify core entities and development trends in a research domain or a specific subject and provide new insights and directions for future research [20, 21]. Currently, an array of science mapping and visualization tools, including CiteSpace, HistCite, VOSviewer, and R-bibliometrix [22–25], are made freely available for scientometric analysis, and they have been widely applied in various scientific fields [26–29]. In this study, scientometric analysis was employed on published Bt pesticidal toxins’ literature (from 1980 to 2021) using CiteSpace and VOSviewer servers. This study aims to summarize the knowledge structure and identify emerging trends, leading countries and organizations/institutions, the main research directions, and potential hotspots in this area in order to provide insights and guide further studies.

Source of data and search strategy

A sum of 5819 documents ranging from the period 1980 to 2021 was selected from the Web of Science Core Collection on December 21, 2021. The data acquisition strategy which reflects studies related to Bt biopesticide toxins was executed as follows: (TS=("Bacillus thuringiensis" OR "B. thuringiensis")) AND TS=("cry protein*" OR "cry toxin*" OR "cry gene*" OR "crystal gene*" OR "crystal protein*" OR "crystal toxin*" OR "cyt toxin*" OR "cyt protein*" OR "cyt gene*" OR "cytolytic toxin*" OR "delta endotoxin*" OR "insecticidal protein*" OR "insecticidal gene*" OR "pesticidal gene*" OR "pesticidal protein*" OR "biological insecticide*" OR "biopesticide*" OR "bioinsecticide*"). TS in WOS represents Topic Search, and it executes a search of the query provided within a bibliographic record in the fields of Title, Abstract, Author Keywords, and Keywords Plus. The wildcard asterisk (*) indicates that any string of character(s) should be considered, for example, cry protein* can find cry proteins, biopesticide* finds biopesticides, etc. Quotation marks are used to enclose terms that are phrases (e.g., “delta endotoxin*”). The document types were refined to include only articles and reviews, thus, book chapters, proceedings papers, early access, retracted publications, and data papers were exempted. Full record and cited references of the documents were imported in plain text format into CiteSpace (version 5.8.R3) and VOSviewer (version 1.6.17) for further analysis.

CiteSpace

CiteSpace is a java tool designed to analyze and visualize scholarly scientific literature of emerging trends in a knowledge domain [30]. CiteSpace performs Co-Citation Analysis (CA) which is subdivided into Author Co-Citation Analysis (ACA), Document Co-Citation Analysis (DCA), and Journal Co-Citation Analysis (JCA). In this study, CiteSpace was employed to perform documents and keywords co-citation analyses.

VOSviewer

VOSviewer is a software tool that is used to create and visualize maps of bibliographic data to build networks of scientific publications, journals, authors, research institutions, countries, keywords, and terms [31]. In this study, VOSviewer was employed to map and visualize the contributions of countries and organisations/institutions to Bt pesticidal toxins. The default settings of VOSviewer were used in this study. Co-authorships of countries and organizations/institutions are represented by labels and circles. The size of a circle reflects the degree of contribution of a particular country or organization. The colors in the network maps represent a network of clusters of cooperation, and the distance between items represents the strength of the connection.

Document volume and annual growth

After screening the data, 5757 qualified documents related to studies conducted on Bacillus thuringiensis and its biopesticide toxins were selected from the Web of Science Core Collection. The document type and the publication language are shown in Table 1 below. Out of the 5747 documents, 5375 (93.36%) were research articles whilst 382 (6.64%) were review articles. Majority of the documents were published in English (5665, 98.228%), followed by Japanese (20, 0.347%), Portuguese (20, 0.347%), Spanish (19, 0.330%), French (12, 0.208%), Russian (10, 0.174%), Chinese (8, 0,139%), Polish (8, 0.139%), and a document (1, 0.017%) each in Croatian, Czech, German, Italian and Turkish. Most of the documents were research articles published in English.

Table 1

Document type and publication language of studies related to Bt biopesticide toxins.
No.	Document type	Quantity	% of 5757	Publication language	Quantity	% of 5,757
1	Article	5375	93.36	English	5655	98.228
2	Review	382	6.64	Japanese	20	0.347
3				Portuguese	20	0.347
4				Spanish	19	0.330
5				French	12	0.208
6				Russian	10	0.174
7				Chinese	8	0.139
8				Polish	8	0.139
9				Croatian	1	0.017
10				Czech	1	0.017
11				German	1	0.017
12				Italian	1	0.017
13				Turkish	1	0.017

Evolution of Bt pesticidal toxins literature

Figure 2 displays the annual publications on Bt pesticidal toxins from 1980 to 2021. The number of publications from 1980 to 1989 witnessed a slow growth trend with less than 30 articles published per year. With increasing interest and deepening research on toxins produced by Bacillus thuringiensis, the number of publications has grown steadily since 1990. As studies on Bt biocontrol pesticidal toxins gathered pace from 1990, they are reflected in Fig. 3 with heightened annual citation frequency from1991 onwards. Another trend of increasing volatility is witnessed by annual publications exceeding 100 articles from 1994 to 2021. The peak of publications over the 42 years was recorded in 2017 when 254 articles were published. From 2017 to 2021, the average annual citation exceeded 10000, dwarfing the years from 1980 to 1992, where the average annual citation did not reach 1000. This demonstrates the continued growth of studies in this area.

Document Co-Citation analysis

The map of co-cited papers related to pesticidal toxins of Bt was generated in CiteSpace by selecting cited references. The reference citation analysis was employed to determine the quality of academic literature in this field by identifying documents with the most-cited references and the corresponding highly influential authors. In the analysis, time-slicing was set as 6 years per slice from 1980 to 2021 and only the top 50 references of each year slice were included, pathfinder was selected, and merged networks were pruned to reduce network density in order to improve the readability of the network [32], the rest of the parameters were set to default. Figure 4 shows a map of the co-citation network related to publication on Bt pesticidal toxins from 1980 to 2021. The network consisted of 242 nodes and 7883 citation links, which means that 242 authors cooperated through 7883 links. The citation threshold was set to 140 displaying only references with 140 or more citations and their respective author and publication year. The size of a node reflects the importance of a reference in the network, whereas the links connecting the nodes indicate their co-occurrence strength. The purple colors surrounding the nodes indicate node centrality which represents the prominence of a node in connecting other pairs of nodes in the network. Higher thickness indicates higher centrality.

Table 2 highlights the top 20 influential and most cited references on studies related to Bacillus thuringiensis biopesticide toxins, ranked based on the number of times they have been cited. It can be seen from Fig. 4 and Table 2 that the most influential reference is written by Schnepf et al. [2], having the highest citation of 1406. This review paper emphasized extensive topics covering Bt genome, the expression of insecticidal cry genes, the structure and functions of Cry toxins, the mechanism of action of Cry proteins, and insect resistance to Bt Cry toxins. The second most-cited document, written by Höfte & Whiteley [33], is also a review article that focuses on the nomenclature and classification scheme of crystal proteins produced by Bacillus thuringiensis based on the protein structure and effectiveness of their host range. Although Schnepf et al. [2], has the most citation count, the higher betweenness centrality of Höfte & Whiteley (1989) makes it more revolutionary, gives it a higher impact factor, and plays a more important role within the network. The third [4], and the fourth [34], most-cited documents talk about the nomenclature of Bt pesticidal crystal proteins, and the crystal structures of δ-endotoxins respectively. These and other articles in the list were crucial to the early stages of research into Bt pesticidal crystal toxins, and they continue to shape studies in this field today.

Table 2

Top 15 most-cited references of studies related to Bt pesticidal proteins
Rank	Cited reference	Count	Centrality	Year	DOI
1	Schnepf et al. (1998)	1406	0.29	1998	doi.org/10.1128/MMBR.62.3.775-806.1998
2	Höfte & Whiteley (1989)	1247	0.81	1989	doi.org/10.1128/MR.53.2.242-255.1989
3	Crickmore et al. (1998)	559	0.29	1998	doi.org/10.1128/MMBR.62.3.807-813.1998
4	J. Li et al. (1991)	434	0.27	1991	doi.org/10.1038/353815a0
5	Bravo et al. (2007)	403	0.07	2007	doi.org/10.1016/J.TOXICON.2006.11.022
6	Ferré & Van Rie (2002)	368	0.00	2002	doi.org/10.1146/annurev.ento.47.091201.145234
7	Gill et al. (1992)	347	0.02	1992	doi.org/10.1146/annurev.en.37.010192.003151
8	Bravo et al. (2011)	239	0.00	2011	doi.org/10.1016/j.ibmb.2011.02.006
9	Estruch et al. (1996)	326	0.03	1996	doi.org/10.1073/pnas.93.11.5389
10	Tabashnik BE (1994)	322	0.35	1994	doi.org/10.1146/annurev.en.39.010194.000403
11	Grochulski et al. (1995)	292	0.07	1995	doi.org/10.1006/jmbi.1995.0630
12	Gould F (1998)	291	0.31	1998	doi.org/10.1146/annurev.ento.43.1.701
13	Pigott CR (2007)	290	0.02	2007	doi.org/10.1128/MMBR.00034-06
14	Pardo-Lopez L (2013)	284	0.08	2013	doi.org/10.1111/j.1574-6976.2012.00341.x
15	Knowles BH (1987)	261	0.08	1987	doi.org/10.1016/0304-4165(87)90167-X
16	de Maagd RA (2001)	254	0.00	2001	doi.org/10.1016/S0168-9525(01)02237-5
17	Thomas WE (1983)	252	0.07	1983	doi.org/10.1242/jcs.60.1.181
18	Tabashnik BE (1990)	246	0.05	1990	doi.org/10.1093/jee/83.5.1671
19	Gahan LJ (2001)	241	0.37	2001	doi.org/10.1126/science.1060949
20	Hofmann C (1988)	223	1.00	1988	doi.org/10.1073/pnas.85.21.7844

Reference citation burst analysis

Citation burst detection in CiteSpace depends on Kleinburg’s algorithm to estimate an abrupt change of frequency over a period of time [35, 36]. Burst detection is used in this study to determine cited references that received an outstanding degree of attention within a specific time range and to determine the current trend of studies by detecting references that have attracted much attention in recent years. Out of the 5,757 documents, 218 burst items were found. Table 3 lists the top 20 references with the strongest citation burst sorted by the beginning year of burst, with the right columns representing the duration of each burst – beginning of deep green lines represent publication year, and red lines segment represent burst duration. References with the same burst duration are considered to belong to the same group.

Table 3

Top 20 references with the strongest citation bursts from 1980 to 2021
References		Strength	Begin	End	1980–2021
HOFMANN C, 1988, P NATL ACAD SCI USA, V85, P7844, DOI 10.1073/pnas.85.21.7844, DOI	1988	79.04	1988	2003	▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
HOFTE H, 1989, MICROBIOL REV, V53, P242, DOI.org/10.1128/mr.53.2.242-255.1989, DOI	1989	86	1989	2003	▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
VANRIE J, 1990, APPL ENVIRON MICROB, V56, P1378, DOI 10.1128/AEM.56.5.1378-1385.1990, DOI	1990	71.94	1992	2003	▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
VANRIE J, 1989, EUR J BIOCHEM, V186, P239, DOI 10.1111/j.1432 − 1033. 1989.tb15201.x, DOI	1989	68.19	1992	2003	▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
VANRIE J, 1990, SCIENCE, V247, P72, DOI 10.1126/science.2294593, DOI	1990	66.68	1992	2003	▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
FERRE J, 1991, P NATL ACAD SCI USA, V88, P5119, DOI 10.1073/pnas.88.12.5119, DOI	1991	65.13	1992	2003	▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂
Schnepf E, 1998, MICROBIOL MOL BIOL R, V62, P775, DOI 10.1128/MMBR.62.3.775-806.1998, DOI	1998	89.11	1998	2015	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂
GROCHULSKI P, 1995, J MOL BIOL, V254, P447, DOI 10.1006/jmbi.1995.0630, DOI	1995	58.8	1998	2015	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂
Bravo A, 2004, BBA-BIOMEMBRANES, V1667, P38, DOI 10.1016/j.bbamem.2004.08.013, DOI	2004	64.29	2004	2015	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃▂▂▂▂▂▂
Bravo A, 2007, TOXICON, V49, P423, DOI 10.1016/j.toxicon.2006.11.022, DOI	2007	114.92	2010	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃
Pardo-Lopez L, 2013, FEMS MICROBIOL REV, V37, P3, DOI 10.1111/j.1574-6976.2012. 00341.x, DOI	2013	109.76	2013	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃
Bravo A, 2011, INSECT BIOCHEM MOLEC, V41, P423, DOI 10.1016/j.ibmb.2011.02.006, DOI	2011	108.93	2011	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃
Pigott CR, 2007, MICROBIOL MOL BIOL R, V71, P255, DOI 10.1128/MMBR.00034 − 06, DOI	2007	82.15	2010	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃
Sanahuja G, 2011, PLANT BIOTECHNOL J, V9, P283, DOI 10.1111/j.1467-7652.2011. 00595.x, DOI	2011	70.68	2011	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃
Vachon V, 2012, J INVERTEBR PATHOL, V111, P1, DOI 10.1016/j.jip.2012.05.001, DOI	2012	57.61	2012	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃
van Frankenhuyzen K, 2009, J INVERTEBR PATHOL, V101, P1, DOI 10.1016/j.jip.2009.02.009, DOI	2009	54.41	2010	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃▃▃▃▃▃▃
Palma L, 2014, TOXINS, V6, P3296, DOI 10.3390/toxins6123296, DOI	2014	86.08	2016	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃
Tabashnik BE, 2013, NAT BIOTECHNOL, V31, P510, DOI 10.1038/nbt.2597, DOI	2013	65.6	2016	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃
Adang MJ, 2014, ADV INSECT PHYSIOL, V47, P39, DOI 10.1016/B978-0-12-800197-4.00002–6, DOI	2014	55.4	2016	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃▃
Tabashnik BE, 2017, NAT BIOTECHNOL, V35, P926, DOI 10.1038/nbt.3974, DOI	2017	55.25	2017	2021	▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▂▃▃▃▃▃

Hofmann et al. (1988), is the first reference to witness citation burst, which started from 1988 to 2003. This reference is related to the specificity of Bt delta-endotoxins to binding sites in the brush border membrane of target insects [37]. A year later a study by Hofte & Whiteley [33], about the classification of Bt toxins started to witness a burst and continued until 2003. However, the top-ranked reference by burst strength is Bravo et al. [38], with a strength of 114.92, which began in 2010 and continues to experience burst. In this paper, Bravo et al.[38], discussed the mode of action of three-domain Cry toxins and cytolytic toxins in selected lepidopteran insects pests and mosquitoes. The second-ranked (Pardo-López et al., 2013) and the third (Bravo et al., 2011) references have close citation burst strengths of 109.76 and 108.93 respectively [1, 39]. These two papers stressed on the mechanism of action of Bt Cry and Cyt toxins but went further to highlight the resistance mechanisms certain insects have developed against these toxins and the strategies to overcome them. 11 out of the top 20 references continue to have burst and we cannot conclude when they will end. Recent papers with references citation bursts are mostly focused on the resistance of insects to Bacillus thuringiensis toxins.

Keywords analysis

The keywords co-occurrence analysis function in CiteSpace uses Co-occurring Author Keywords (DE) and KeyWords Plus (ID) in published documents to generate a network map of the most occurring keywords. Keyword analysis was performed to determine viral topics and trends of development in research related to toxins produced by Bt. Clustering analysis of the keywords was further performed to explore the potential hidden congruence between the keywords. Table 4 lists the top 20 co-occurring keywords. Figure 5 displays the map of the keyword co-occurrence network showing keywords with at least 100 appearances. The sizes of the rectangles in the figure are proportional to the frequency of occurrence of their corresponding keywords. The purple colors surrounding the nodes indicate the strength of centrality.

Table 4

Top 20 keywords with their frequency and centrality in pesticidal toxins of Bt research (1980–2021)
Rank	Frequency	Centrality	Year	Keyword
1	2750	0.20	1991	Bacillus thuringiensis
2	1544	0.07	1987	delta endotoxin
3	792	0.03	1990	resistance
4	786	0.18	1987	toxin
5	684	0.00	1991	protein
6	614	0.03	1987	gene
7	598	0.10	1987	crystal protein
8	539	0.07	1991	expression
9	537	0.00	1987	toxicity
10	472	1.00	1991	brush border membrane
11	467	0.42	1991	insect resistance
12	459	0.30	1991	strain
13	442	0.03	1991	lepidoptera
14	421	0.03	1992	Heliothis virescens
15	409	0.13	1991	binding
16	388	0.00	1991	identification
17	385	0.35	1991	Manduca sexta
18	323	0.10	2004	Helicoverpa armigera
19	299	0.07	1991	larvae
20	294	0.07	1991	plant

Categorization of top 20 keywords

From Fig. 5 and Table 4, the top 20 co-occurring keywords are grouped as follows:

The first group of keywords, such as “Bacillus thuringiensis (2,750 appearances in all keywords with a centrality of 0.20), “strain (459, 0.30)”, and “identification (388, 0.00), is related to the identification of Bt strains that produce the insecticidal toxins. In 1901, a Japanese bacteriologist Shigetane Ishiwata discovered the first endospore-forming Bacillus thuringiensis reported it as the causal agent of sotto disease in silkworms following the ingestion of the bacterium by the silkworm larvae [40]. However, Lepidopteran insects (moths and butterflies) were popularly considered the only targets of Bt until the 1970s [41], when Goldberg and Margalit identified a new subspecies of Bt (Bacillus thuringiensis israelensis – Bti) that was active against mosquito and blackfly larvae (Dipteran insects) [42]. Until now, several Bt strains have been isolated throughout the world from various sources such as soil, diseased insects, water, grain dust, and leaf surface of many plants [43, 44]. These strains produce over 300 crystal proteins that demonstrate specific activity against several insect orders including Lepidoptera, Diptera, Coleoptera, Hymenoptera, Homoptera, Orthoptera, Mallophaga [2], and other invertebrates [41].

The keywords “delta endotoxin (1545, 0.070)”, “toxin (787, 0.18)”, “protein (684, 0.00)”, “gene (615, 0.03)”, “crystal protein (599, 0.10)”, and “toxicity (539, 0.00)”, form the second group of keywords and are related to the insecticidal protein toxins produced by Bt and the genes encoding these proteins. When there is a shortage of nutrients to Bacillus thuringiensis, it forms a dormant spore or large parasporal crystalline inclusions. These crystal inclusions are oftentimes referred to as δ-endotoxins (delta endotoxins), and they contain insecticidal Cry proteins that are deadly when ingested by specific susceptible insects [45]. These protein toxins are coded by a family of genes called cry genes [2, 4, 46].

The third group of keywords consists of, “expression (539, 0.07)”, “brush border membrane (472, 1.00)”, and “binding (388, 0.00). This group of keywords is related to the mechanism of action of Bacillus thuringiensis insecticidal toxins which involves the expression of certain cry genes such as cry1Ab, cry1F, cry9C etc. [47], by binding to the brush border membrane vesicles of specific insects. The crystal proteins of Bt consist of inactive protoxins. Upon ingestion, the crystals are solubilized under the alkaline conditions of the susceptible insect midgut and protoxins are processed by the proteases of the midgut to become activated [2]. The activated crystal toxin binds to a specific receptor on the brush border membrane of midgut microvillae. This causes pore formation in the insect midgut, cell lyses, and the eventual death of the insect [2, 48].

The fourth group of keywords are “resistance (792, 0.03)”, and “insect resistance (467, 0.42), which are related to the evolution of insect resistance to certain Bt toxins. Due to the coevolution of Bt and insects, there were optimisms in the past that insects would not develop resistance against Bt toxins. However, several insect species displaying different levels of resistance to Bt Cry proteins by laboratory selection experiments, using insects collected from wild populations or laboratory-reared insects have been reported, starting in the mid-1980s [2, 49, 50]. Several studies have reported different levels of field-evolved resistance to Bt toxins by different major insect pests [51–54].

The last group of keywords comprise “lepidoptera (442, 0.03)”, “Heliothis virescens (409, 0.13)”, “Manduca sexta (385, 0.35)”, “Helicoverpa armigera (323, 0.10)”, and “larvae (299, 0.07)”, is related to some major insect pests which Bt toxins have been deployed against.

Timeline clusters of keywords

Keywords are clustered and visualized in the “timeline” mode to generate a map depicting the relationship between a cluster of keywords and the lifespan of most co-occurring keywords in a cluster. Frequently co-occurring keywords are firstly clustered in CiteSpace and an appropriate cluster label is designated to each cluster. Nodes of the same cluster are aligned on the same horizontal line in accordance with the timespan, displaying the historical accomplishment of a cluster [55]. Keywords with a higher frequency of occurrence show that those keywords were Bt toxin research-related hotspots within that period. CiteSpace utilized the clustering modularity index (Q value) and silhouette index (S value) to compute the clustering efficacy of the map. Q value ranges from 0–1, Q > 0.3 indicates a significant network structure. A network with a mean silhouette value above 0.5 is considered rational, and if it is closer to 1, it indicates higher homogeneity of the network [35, 56]. Thus, the Q value of 0.8083, and S value of 0.9675 denote reasonable divided keywords into loose clusters and a higher degree of consistency among members in a cluster.

Figure 6 shows timeline visualization of keywords co-citation analysis, divided into 11 timelines of clusters by the Log-Likelihood Ratio (LLR) clustering method. High-frequency keywords usually appeared between 1990–1992. The largest cluster (#0 bacillus thuringiensis subsp. israelensis) has 15 members and a Mean Silhouette value of 0.936. Keywords in this cluster were hotspots in 1990, but the timeline expired around 1992. The second (#1 insecticidal toxin) and the third (#2 biological control) largest clusters have 14 members of keywords each, with a Mean Silhouette value of 1.00 each and these timelines lasted until around 2008 and 2016 respectively. This means that the keywords related to these clusters appeared early and had great influence in those periods, their popularity has declined recently.

Also, “#2 biological control”, “#3 helicoverpa armigera”, and “#4 field-evolved resistance are three highly connected clusters. The significant overlap of keywords in these clusters can be partly attributed to the detection of field-evolved resistance mechanisms in Helicoverpa armigera to certain Bt toxins (Cry1Ac) in Bt cotton fields [57]. The timelines of “#4 field-evolved resistance”, “#5 bacillus thuringiensis delta-endotoxin”, and “#6 plutella xylostela” are still active to this day. Thus, research related to keywords in these clusters has been ongoing since their emergence and they are still popular today, indicating the current research focus.

Top twenty active countries

VOSviewer was used to examine and visualize the contributions and collaborations of different countries in Bt pesticidal toxins related research. Only countries with a minimum of 5 documents were included. Out of the 105 countries involved, 63 met the threshold, and the visualization result is illustrated in Fig. 7. The size of a node represents the number of documents published by a particular country and the nodal linkage denote the degree of cooperation. Articles co-authored by authors from more than one country were not ignored.

As shown in Table 5, the United States of America is the leading country in terms of the number of published articles on studies related to Bt pesticidal toxins. Articles published by researchers from the United States have been cited 72754 times, with an average citation of 46.58 per article.

Table 5

Top 20 influential countries in Bt pesticidal toxin-related research from 1980–2021
Rank	Country	Documents	Citations	Mean citation/document
1	United States of America	1562	72754	46.58
2	Peoples Republic of China	933	16760	17.96
3	India	449	6583	14.66
4	Mexico	308	9986	32.42
5	Brazil	290	4740	16.34
6	England	289	17737	61.37
7	France	284	15280	53.80
8	Canada	283	10703	37.82
9	Japan	249	4945	19.86
10	Spain	245	8578	35.01
11	Germany	131	4257	32.50
12	Tunisia	123	1746	14.20
13	Switzerland	122	5320	43.61
14	Australia	113	5089	45.04
15	South Korea	111	1835	16.53
16	Pakistan	109	1243	11.40
17	Thailand	102	1463	14.34
18	Belgium	99	10537	106.43
19	Italy	98	2383	24.31
20	Turkey	79	796	10.07

The Peoples Republic of China had the second-highest published articles (933), with a mean citation of 17.96 per paper. This is followed by India (449), Mexico (308), and Brazil (290), with an average citation of 14.66, 32.42, 16.34 per paper respectively. Although Belgium is ranked eighteenth (99 documents) regarding the number of publications, it has the highest (106.43) average citation per document among the top 15 most contributing countries. This shows the quality and relative importance of articles published by researchers from Belgium in this field.

Top twenty prolific institutions

The data used contain 2899 institutions that have contributed to research publications on Bacillus thuringiensis pesticidal toxins from 1980 to 2021. Out of the 2899 institutions, 66 of them have published at least 25 documents. The number of published documents and the average citation number per document of an institution reflect the influence of an institution in this field. Figure 8 shows the network map of co-cited institutions with at least 25 publications.

Table 6

Top 20 institutions/organisations with the most published articles in Bt related research from 1980–2021
Rank	Institution	Documents	Citations	Mean Citation/document
1	Chinese Academy of Agricultural Sciences	298	6317	21.20
2	National Autonomous University of Mexico	177	8244	46.58
3	Huazhong Agricultural University	161	3141	19.51
4	University of Valencia	150	5524	36.83
5	University of California, Riverside	145	6932	47.81
6	The United States Department of Agriculture (USDA)	134	5451	40.68
7	University of Georgia	112	5578	49.80
8	University of Arizona	92	4171	45.34
9	University of Cambridge	89	5893	66.21
10	Mahidol University	85	1288	15.15
11	French National Research Institute of Agriculture (INRA)	82	4084	49.80
12	Chinese Academy of Sciences	81	1426	17.60
13	Agricultural Research Services (ARS)	79	2903	36.75
14	Cornell University	78	4411	56.55
15	Monsanto Company	76	4676	61.53
16	Ohio State University	75	5865	78.20
17	Pasteur Institute	73	6573	90.04
18	Kyushu University	70	1365	19.50
19	Iowa State University	67	2967	44.28
20	Nanjing Agricultural University	62	1739	28.04

Table 6 shows the top 20 institutions/organisations that have published the most documents on Bt pesticidal toxins related studies from 1980 to 2021. The Chinese Academy of Agricultural Sciences is ranked first with 298 publications and an average citation of 21.20 per document. The subsequent institutions are the National Autonomous University of Mexico, Huazhong Agricultural University, and University of Valencia, with 177, 161, and 150 publications, and average citations of 46.58, 19.51, and 36.83 per document respectively. Among the top 20 institutions, the Pasteur Institute in France, Ohio State University in the United States, and the University of Cambridge in England had the highest average citation per document of 90.04, 78.20, and 66.21 respectively. This signifies the contribution of these institutions to quality published documents on Bt pesticidal toxins related studies.

In this study, data of global scientific research publications on Bt pesticidal toxins from 1980 to 2021 were extracted from the Web of Science Core Collection and analyzed using CiteSpace and VOSviewer scientometric visualization tools. After refining the data, 5757 documents were extracted. The results showed that researchers from 2,899 institutions in 105 countries contributed to studies on Bt biopesticide toxins. The United States of America was the leading country in this field, followed by the People’s Republic of China, and India. The most influential institutions were the Chinese Academy of Agricultural Sciences, the National Autonomous University of Mexico, and the Huazhong Agricultural University.

Also, Schepf et al. (1998), Höfte & Whiteley (1989), and Crickmore et al. (1998) were the most influential references based on the number of times they have been cited. Documents related to these references have contributed immensely to shaping research trends in this field. These references focused on topics such as the structure and functions of Cry proteins, nomenclature and classification of Cry toxins, expression and mode of action of Cry toxins in insects, and the evolution of resistance to Cry toxins in insects. Reference burst citation analysis revealed the most influential references and current references that are receiving the most attention [2, 4, 33]. Bravo et al. [38], had the highest citation burst of 115.06, followed by Pardo-López et al. [39] and Bravo et al. [1] with citation burst strengths of 109.83 and 109.03 respectively. Out of the top 20 references with the strongest citation burst, 11 of them are still receiving attention to this day. Most of these references are related to research on the evolution of insect resistance to Bt pesticidal toxins.

Keyword co-occurrence analysis revealed the most frequently occurring keywords. After the analysis, some of the most highly occurring keywords were Bacillus thuringiensis, delta endotoxin, resistance, toxin, protein, gene, crystal protein etc. In addition, cluster and timeline visualization of the keywords showed that keywords related to cluster labels such as field-evolved resistance, Bacillus thuringiensis delta endotoxin, and Plutella xylostella are the current active hotspots. In general, the current trend of research in this field is more focused on the evolution of resistance among pest insects against Bt toxins.

Research hotspots in recent years have mainly focused on the development of resistance among certain insects against Bacillus thuringiensis pesticidal toxins. With the latest development of research on Bt toxins, researchers should concentrate more on understanding the mechanisms of resistance among certain insects and put in an effort to discover novel pesticidal toxins that are effective against these pest insects.

Limitations

This scientometric study utilized CiteSpace and VOSviewer to analyze data on Bacillus thuringiensis pesticidal toxins’ publications from 1980–2021, based on the Web of Science Core Collection database. The data used in this study were extracted from only one database. Although Web of Science consists of many journals, it is difficult to achieve full coverage of all documents on Bt pesticidal toxins, especially those in other databases such as Scopus, PubMed, etc. Also, data used in this study were restricted to only research and review articles, and the query terms used to search the articles. Future studies can broaden the data collection to include publication types such as book chapters, proceedings papers, early access etc., and include search terms such as parasporins, vegetative insecticidal protein (Vip) toxins, binary (Bin) toxins etc.

Competing interests: The authors have declared that no competing interest exists.

Bravo A, Likitvivatanavong S, Gill SS, Soberón M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem Mol Biol. Pergamon; 2011;41:423–31.
Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, et al. Bacillus thuringiensis and Its Pesticidal Crystal Proteins. Microbiol Mol Biol Rev [Internet]. American Society for Microbiology; 1998 [cited 2021 Aug 1];62:775–806. Available from: https://journals.asm.org/journal/mmbr
Wei J-Z, Hale K, Carta L, Platzer E, Wong C, Fang S-C, et al. Bacillus thuringiensis crystal proteins that target nematodes. Natl Acad Sci [Internet]. 2003 [cited 2022 Jan 23];100:2760–5. Available from: https://www.pnas.org/content/100/5/2760.short
Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van Rie J, Lereclus D, et al. Revision of the Nomenclature for the Bacillus thuringiensis Pesticidal Crystal Proteins. Microbiol Mol Biol Rev [Internet]. American Society for Microbiology; 1998 [cited 2021 Dec 31];62:807–13. Available from: https://journals.asm.org/doi/abs/10.1128/MMBR.62.3.807-813.1998
De Maagd RA, Bravo A, Crickmore N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. Elsevier Current Trends; 2001;17:193–9.
Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW. Field-Evolved Resistance to Bt Maize by Western Corn Rootworm. PLoS One [Internet]. Public Library of Science; 2011 [cited 2022 Jan 23];6:e22629. Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0022629
Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, et al. Discovery and Characterization of Field Resistance to Bt Maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol [Internet]. Oxford Academic; 2010 [cited 2022 Jan 23];103:1031–8. Available from: https://academic.oup.com/jee/article/103/4/1031/2199574
Bagla P. Hardy cotton-munching pests are latest blow to GM crops. Science (80-) [Internet]. American Association for the Advancement of Science; 2010 [cited 2022 Jan 23];327:1439. Available from: https://www.science.org/doi/abs/10.1126/science.327.5972.1439
Tabashnik BE, Gassmann AJ, Crowder DW, Carrière Y. Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 2008 262 [Internet]. Nature Publishing Group; 2008 [cited 2022 Jan 23];26:199–202. Available from: https://www.nature.com/articles/nbt1382
van Rensburg JBJ. First report of field resistance by the stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. 101080/02571862200710634798 [Internet]. Taylor & Francis Group; 2013 [cited 2022 Jan 23];24:147–51. Available from: https://www.tandfonline.com/doi/abs/10.1080/02571862.2007.10634798
Yılmaz S, Babiker Idris A, Ayvaz A, Çetin A, Ülgen F, Çetin M, et al. New Insights into Molecular Basis Identification of Three Novel Strains of the Bacillus Subtilis Group Produce Cry Proteins Isolated from Soil Samples in Adana, Turkey. biorxiv.org [Internet]. 2021 [cited 2022 Jan 23]; Available from: https://www.biorxiv.org/content/10.1101/2021.12.24.474129.abstract
Bravo A, Gómez I, Porta H, García-Gómez BI, Rodriguez-Almazan C, Pardo L, et al. Evolution of Bacillus thuringiensis Cry toxins insecticidal activity. Microb Biotechnol. 2013;6:17–26.
Pardo-López L, Muñoz-Garay C, Porta H, Rodríguez-Almazán C, Soberón M, Bravo A. Strategies to improve the insecticidal activity of Cry toxins from Bacillus thuringiensis. Peptides. Elsevier; 2009;30:589–95.
Nair K, Al-Thani R, Al-Thani D, Al-Yafei F, Ahmed T, Jaoua S. Diversity of Bacillus thuringiensis strains from Qatar as shown by crystal morphology, δ-Endotoxins and Cry gene content. Front Microbiol. Frontiers Media S.A.; 2018;9:708.
Rabha M, Sharma S, Acharjee S, Sarmah BK. Isolation and characterization of Bacillus thuringiensis strains native to Assam soil of North East India. 3 Biotech [Internet]. Springer Verlag; 2017 [cited 2022 Jan 23];7:1–9. Available from: https://link.springer.com/article/10.1007/s13205-017-0935-y
Pinos D, Andrés-Garrido A, Ferré J, Hernández-Martínez P. Response Mechanisms of Invertebrates to Bacillus thuringiensis and Its Pesticidal Proteins. Microbiol Mol Biol Rev. American Society for Microbiology; 2021;85.
Peng Q, Yu Q, Song F. Expression of cry genes in Bacillus thuringiensis biotechnology. Appl Microbiol Biotechnol. Springer Verlag; 2019;103:1617–26.
Chen C, Hu Z, Liu S, Tseng H. Emerging trends in regenerative medicine: a scientometric analysis in CiteSpace. https://doi.org/101517/147125982012674507 [Internet]. Taylor & Francis; 2012 [cited 2022 Jan 23];12:593–608. Available from: https://www.tandfonline.com/doi/abs/10.1517/14712598.2012.674507
Rizzi L, Aventurato ÍK, Balthazar MLF. Neuroimaging Research on Dementia in Brazil in the Last Decade: Scientometric Analysis, Challenges, and Peculiarities. Front Neurol. Frontiers Media S.A.; 2021;12.
Wu H, Zhou Y, Xu L, Tong L, Wang Y, Liu B, et al. Mapping Knowledge Structure and Research Frontiers of Ultrasound-Induced Blood-Brain Barrier Opening: A Scientometric Study. Front Neurosci. Frontiers Media S.A.; 2021;15:834.
Liu C, Liu Z, Zhang Z, Li Y, Fang R, Li F, et al. A Scientometric Analysis and Visualization of Research on Parkinson’s Disease Associated With Pesticide Exposure. Front Public Heal. Frontiers Media S.A.; 2020;8.
Guo Y, Hao Z, Zhao S, Gong J, Yang F. Artificial Intelligence in Health Care: Bibliometric Analysis. J Med Internet Res 2020;22(7)e18228 https//www.jmir.org/2020/7/e18228 [Internet]. Journal of Medical Internet Research; 2020 [cited 2022 Jan 23];22:e18228. Available from: https://www.jmir.org/2020/7/e18228
van Eck NJ, Waltman L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics [Internet]. Springer Netherlands; 2010 [cited 2022 Jan 23];2:523–38. Available from: https://www.infona.pl//resource/bwmeta1.element.springer-41076c77-7e15-3f8d-9077-d0d050bef548
Ke L, Lu C, Shen R, Lu T, Ma B, Hua Y. Knowledge Mapping of Drug-Induced Liver Injury: A Scientometric Investigation (2010–2019). Front Pharmacol. Frontiers Media S.A.; 2020;11.
Synnestvedt MB, Chen C, Holmes JH. CiteSpace II: Visualization and Knowledge Discovery in Bibliographic Databases. AMIA Annu Symp Proc [Internet]. American Medical Informatics Association; 2005 [cited 2022 Jan 23];2005:724. Available from: /pmc/articles/PMC1560567/
Liu X, Wu X, Tang J, Zhang L, Jia X. Trends and Development in the Antibiotic-Resistance of Acinetobacter baumannii: A Scientometric Research Study (1991–2019). Infect Drug Resist [Internet]. Dove Press; 2020 [cited 2022 Jan 23];13:3195. Available from: /pmc/articles/PMC7502395/
Teles RHG, Moralles HF, Cominetti MR. Global trends in nanomedicine research on triple negative breast cancer: a bibliometric analysis. Int J Nanomedicine [Internet]. Dove Press; 2018 [cited 2022 Jan 23];13:2321. Available from: /pmc/articles/PMC5910795/
Zhao J, Yu G, Cai M, Lei X, Yang Y, Wang Q, et al. Bibliometric analysis of global scientific activity on umbilical cord mesenchymal stem cells: A swiftly expanding and shifting focus. Stem Cell Res Ther [Internet]. BioMed Central Ltd.; 2018 [cited 2022 Jan 23];9:1–9. Available from: https://stemcellres.biomedcentral.com/articles/10.1186/s13287-018-0785-5
Wang Y, Zhao N, Zhang X, Li Z, Liang Z, Yang J, et al. Bibliometrics Analysis of Butyrophilins as Immune Regulators [1992–2019] and Implications for Cancer Prognosis. Front Immunol. Frontiers Media S.A.; 2020;11.
Chen C. CiteSpace II: Detecting and visualizing emerging trends and transient patterns in scientific literature. J Am Soc Inf Sci Technol [Internet]. John Wiley & Sons, Ltd; 2006 [cited 2021 Dec 19];57:359–77. Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/asi.20317
Eck N Van, Leiden LW-LU, 2013 undefined. VOSviewer manual. vosviewer.com [Internet]. 2020 [cited 2021 Dec 20]; Available from: https://www.vosviewer.com/download/f-33t2.pdf
Li X, Guo D, Cheng J. Study on Map Knowledge Domains of Transgenic Maize: Based on Citespace. World Scientific Pub Co Pte Lt; 2016;618–24.
Hofte H, Whiteley HR. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev [Internet]. American Society for Microbiology; 1989 [cited 2021 Dec 31];53:242–55. Available from: https://journals.asm.org/doi/abs/10.1128/mr.53.2.242-255.1989
Li J, Carroll J, Nature DE-, 1991 undefined. Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution. nature.com [Internet]. 1991 [cited 2021 Dec 31]; Available from: https://www.nature.com/articles/353815a0
Chen C. The citespace manual. Coll Comput Informatics. 2014;1–84.
Sohrabi B, Vanani IR, Mohammad S, Jalali J, Abedin E, Jalali J. Evaluation of research trends in knowledge management: a hybrid analysis through burst detection and text clustering. World Sci [Internet]. World Scientific Publishing Co. Pte Ltd; 2020 [cited 2022 Jan 2];18. Available from: https://www.worldscientific.com/doi/abs/10.1142/S0219649219500436
Hofmann C, Vanderbruggen H, Hofte H, Van Rie J, Jansens S, Van Mellaert H. Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc Natl Acad Sci [Internet]. National Academy of Sciences; 1988 [cited 2022 Jan 5];85:7844–8. Available from: https://www.pnas.org/content/85/21/7844
Bravo A, Gill SS, Soberón M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon. Pergamon; 2007;49:423–35.
Pardo-López L, Soberón M, Bravo A. Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev [Internet]. Oxford Academic; 2013 [cited 2022 Jan 3];37:3–22. Available from: https://academic.oup.com/femsre/article/37/1/3/557757
Ishiwata S. On a kind of severe flacherie (sotto disease). ci.nii.ac.jp [Internet]. 1901 [cited 2022 Mar 12];114:1–5. Available from: https://sci-hub.ren/https://ci.nii.ac.jp/naid/10006296301/
Sanchis V. From microbial sprays to insect-resistant transgenic plants: history of the biospesticide Bacillus thuringiensis. A review. Agron Sustain Dev 2010 311 [Internet]. Springer; 2011 [cited 2022 Mar 13];31:217–31. Available from: https://link.springer.com/article/10.1051/agro/2010027
Goldberg LJ, Margalit J. A bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegypti and Culex pipiens. Mosq News [Internet]. 1977 [cited 2022 Mar 13];37:355–8. Available from: https://sci-hub.ren/https://www.cabdirect.org/cabdirect/abstract/19782902995
Martin PAW, Travers RS. Worldwide abundance and distribution of Bacillus thuringiensis isolates. Appl Environ Microbiol. 1989;55:2437–42.
Khachatourians GG. Insecticides, Microbial. Encycl. Microbiol. Saskatoon; Jan p. 95–109.
Knowles BH. Mechanism of Action of Bacillus thuringiensis Insecticidal δ-Endotoxins. Adv In Insect Phys. 1994;24:275–308.
Ibrahim M, Griko N, Junker M, bugs LB-B, 2010 undefined. Bacillus thuringiensis: a genomics and proteomics perspective. Taylor Fr [Internet]. 2010 [cited 2021 Dec 12];1:31–50. Available from: https://www.tandfonline.com/doi/abs/10.4161/bbug.1.1.10519
Hua G, Masson L, Jurat-Fuentes JL, Schwab G, Adang MJ. Binding analyses of Bacillus thuringiensis Cry δ-endotoxins using brush border membrane vesicles of Ostrinia nubilalis. Appl Environ Microbiol [Internet]. American Society for Microbiology; 2001 [cited 2022 Jan 11];67:872–9. Available from: https://journals.asm.org/doi/abs/10.1128/AEM.67.2.872-879.2001
Ferré J, Van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annu Rev Entomol [Internet]. Annu Rev Entomol; 2002 [cited 2021 Dec 31];47:501–33. Available from: https://pubmed.ncbi.nlm.nih.gov/11729083/
Tabashnik BE. Evolution of Resistance to Bacillus Thuringiensis.
http://dx.doi.org/101146/
annurev.en39010194000403 [Internet]. Annual Reviews 4139 El Camino Way, P.O. Box 10139, Palo Alto, CA 94303-0139, USA; 1994 [cited 2021 Dec 31];39:47–79. Available from: https://www.annualreviews.org/doi/abs/10.1146/annurev.en.39.010194.000403
Ferré J, Escriche B, Bel Y, van Rie J. Biochemistry and genetics of insect resistance to Bacillus thuringiensis insecticidal crystal proteins. FEMS Microbiol Lett [Internet]. Oxford Academic; 1995 [cited 2022 Mar 24];132:1–7. Available from: https://academic.oup.com/femsle/article/132/1-2/1/902913
Tabashnik BE. ABCs of Insect Resistance to Bt. PLOS Genet [Internet]. Public Library of Science; 2015 [cited 2022 Mar 28];11:e1005646. Available from: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005646
Tabashnik BE, Brévault T, Carrière Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 2013 316 [Internet]. Nature Publishing Group; 2013 [cited 2022 Jan 5];31:510–21. Available from: https://www.nature.com/articles/nbt.2597
Zhang H, Tian W, Zhao J, Jin L, Yang J, Liu C, et al. Diverse genetic basis of field-evolved resistance to Bt cotton in cotton bollworm from China. Proc Natl Acad Sci U S A. 2012;109:10275–80.
Monnerat R, Martins E, Macedo C, Queiroz P, Praça L, Soares CM, et al. Evidence of field-evolved resistance of Spodoptera frugiperda to Bt corn expressing Cry1F in Brazil that is still sensitive to modified Bt toxins. PLoS One. Public Library of Science; 2015;10.
Wu J, Wu X, Zhang J. Development Trend and Frontier of Stormwater Management (1980–2019): A Bibliometric Overview Based on CiteSpace. Water 2019, Vol 11, Page 1908 [Internet]. Multidisciplinary Digital Publishing Institute; 2019 [cited 2022 Jan 12];11:1908. Available from: https://www.mdpi.com/2073-4441/11/9/1908/htm
Liu H, Tan W, Li H, Wu X, Han T, Xu Y, et al. Analysis on Research Frontiers and Hotspots of “Artificial Intelligence Plus Education” in China --Visualization Research Based on Citespace V. IOP Conf Ser Mater Sci Eng [Internet]. IOP Publishing; 2019 [cited 2022 Jan 15];569:052073. Available from: https://iopscience.iop.org/article/10.1088/1757-899X/569/5/052073
Gunning R V., Dang HT, Kemp FC, Nicholson IC, Moores GD. New resistance mechanism in Helicoverpa armigera threatens transgenic crops expressing Bacillus thuringiensis Cry1Ac toxin. Appl Environ Microbiol [Internet]. Appl Environ Microbiol; 2005 [cited 2022 Jan 26];71:2558–63. Available from: https://pubmed.ncbi.nlm.nih.gov/15870346/

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published 31 Jul, 2023

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Bacillus thuringiensis pesticidal toxins: A global analysis based on scientometric study (1980 – 2021)

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Abstract

Figures

Background

Materials And Methods

Source of data and search strategy

CiteSpace

VOSviewer

Results And Discussion

Document volume and annual growth

Document Co-Citation analysis

Categorization of top 20 keywords

Timeline clusters of keywords

Top twenty active countries

Top twenty prolific institutions

Conclusions

Limitations

Declarations

References

Status:

Journal Publication

Version 1