Plant Resistance to Fungal Pathogens: Bibliometric Analysis and Visualization

Plants are susceptible to fungal pathogen infection, threatening plant growth and development. Researchers worldwide have conducted extensive studies to address this issue and have published numerous articles on the subject, but they lack a scientometric evaluation. This study analyzed international research on the topic “Plant resistance to fungal pathogens” between 2008 and 2021, using the core database of the Web of Science (WoS). By searching the subject words “Plants”, “Disease Resistance”, and “Fungal Pathogens”, we received 6687 articles. Bibliometric visualization software analyzes the most published countries, institutions, journals, authors, the most cited articles, and the most common keywords. The results show that the number of articles in the database has increased year by year, with the United States and China occupying the core positions, accounting for 46.16% of the total published articles worldwide. The United States Department of Agriculture (USDA) is the main publishing organization. Wang Guoliang is the author with the most published articles, and the Frontiers in Plant Science ranks first in published articles. The research on plant anti-fungal pathogens is booming, and international exchanges and cooperation need to be further strengthened. This paper summarizes five possible research ideas, from fungal pathogens, gene editing technology, extraction of secondary metabolites from plants as anti-fungal agents, identification of related signal pathways, fungal molecular databases, and development of nanomaterials, to provide data for related research.


Introduction
There are millions of different types of fungal infections, many of which represent a serious threat to plant health. Although long recognized, fungi were not acknowledged as the cause of plant diseases until the 1850s [1]. Cranberry blight caused by Stagonosporopsis cucurbitacearum [2,3], blueberry grey mold produced by Botrytis cinerea, streak disease caused by Drechslera avenaceous [4], and leaf anthracnose of tea plants caused by the Colletotrichum [5] are some examples of diseases and pathogens feared as much as human diseases and war.
Fungal pathogens colonize plants in different ways to obtain nutrients. Biotrophic fungi feed only in living plant tissues. They do not kill the host, preventing cell death and manipulating plant metabolism by secreting effector molecules. Necrotrophic fungi infect living tissues, continuously produce hydrolytic enzymes, and secrete toxins to kill plant cells and acquire nutrients [6]. Hemibiotrophs initially extract nutrients from living tissues before switching to a necrotrophic phase.
Plants cannot move like animals and are more likely to be infected by multiple fungal pathogens. In response to the stress of fungal pathogens, plants resist the invasion of fungal pathogens through innate or acquired systemic immunity. For example, fungal pathogens invade the cell wall, the first line of defense of the plant host, by autophagy of plant cells against necrotrophic fungal pathogens [7], secretion of phytohormones, such as salicylic

Data Collection
This study focuses on the scientometric analysis of plant resistance to fungal pathogens from 2008 to 2021. All the literature data are from the Clarivate Analytics WoS core collection database (https://www.webofscience.com/wos/woscc/basic-search, accessed on 18 October 2022). The data retrieval time is 27 September 2022. The following keywords are entered to search: "plant", "disease resistance", and "fungal pathogen", excluding conference papers, book chapters, duplicate literature, etc. A total of 6687 papers are retrieved for further study after collecting and screening domestic and international literature on plant resistance to fungal pathogens research.

Data Analysis
We used VOSviewer to map the network collaboration of major countries, institutions, authors, journals, etc. Bibliometrics obtained the number of papers published in different years in some countries; the keywords of CiteSpace can also well reflect the keywords in different periods. HistCite created a chronological chart of the top 50 local citation scores (LCS).
VOSviewer is a software developed by the Science and Technology Research Center of Leiden University in the Netherlands. It can draw knowledge maps through the relationship construction and visual analysis of "network data" and visualize the relationship between the structure, evolution, and cooperation of the field [15]. Thomson Reuters developed HistCite, which can only be applied to WoS database files owned by the same company. This paper understands the domestic and foreign attention to this field by analyzing the annual publication volume, major countries, institutions, authors, journals, and other network cooperation maps. Next, we analyzed the keywords in this field to understand the research hotspots and then analyzed the main research in this direction. The examination of the first 50 publications classified according to LCS index gave us an indication on the progress of research and the keystone in the field of resistance of the plant to fungal pathogens ( Figure 2). In 2008, Wan et al. [18], the authors of a paper numbered 61 with an LCS of 75, identified a LysM receptor-like protein required for chitin signaling in Arabidopsis thaliana. In 2009, Simon et al. [16], in the article numbered 345 published in SCIENCE, proposed the wheat gene Lr34 useful to induce resistance to some fungal pathogens. In 2010, studies on the molecular basis of Fusarium pathogenicity were published in NATURE [19]. In 2011, the article with the highest LCS was published in PLANT PHYSIOLOGY [20] and developed an RLP-mediated verticillium wilt resistance signaling model in A. thaliana by transferring the tomato gene encoding Ve1. Matthew et al. [21] reviewed the studies on plant resistance to fungal pathogens, underlined the emergence of plant pathogenic fungi resistant to antifungal drugs, and showed several problems in this field that need to be solved. The examination of the first 50 publications classified according to LCS index gave us an indication on the progress of research and the keystone in the field of resistance of the plant to fungal pathogens ( Figure 2). In 2008, Wan et al. [18], the authors of a paper numbered 61 with an LCS of 75, identified a LysM receptor-like protein required for chitin signaling in Arabidopsis thaliana. In 2009, Simon et al. [16], in the article numbered 345 published in SCIENCE, proposed the wheat gene Lr34 useful to induce resistance to some fungal pathogens. In 2010, studies on the molecular basis of Fusarium pathogenicity were published in NATURE [19]. In 2011, the article with the highest LCS was published in PLANT PHYSIOLOGY [20] and developed an RLP-mediated verticillium wilt resistance signaling model in A. thaliana by transferring the tomato gene encoding Ve1. Matthew et al. [21] reviewed the studies on plant resistance to fungal pathogens, underlined the emergence of plant pathogenic fungi resistant to antifungal drugs, and showed several problems in this field that need to be solved.  [18], Ioannis et al. [17], Simon et al. [16], Justin et al. [22], Ma et al. [19], Emily et al. [20], Chan-Ho Park et al. [23], Aline et al. [24], Joanna et al. [25], Vivianne et al. [26], John et al. [27], and Matthew et al. [21].

Annual Research Analysis
The literature on plant resistance to fungi infections is primarily focused on the years 2008-2021 in the WoS core collection, and the number of papers published after 2008 is rising annually. Figure 3 demonstrates that, as of 2021, the number of articles relating to research on anti-fungal pathogens is continually increasing, growing substantially from 257 in 2008 to 962 in 2021, suggesting that this study area has attracted widespread interest since 2008. There is still great room for progress in the future with increasing attention.    [18], Ioannis et al. [17], Simon et al. [16], Justin et al. [22], Ma et al. [19], Emily et al. [20], Chan-Ho Park et al. [23], Aline et al. [24], Joanna et al. [25], Vivianne et al. [26], John et al. [27], and Matthew et al. [21].

Annual Research Analysis
The literature on plant resistance to fungi infections is primarily focused on the years 2008-2021 in the WoS core collection, and the number of papers published after 2008 is rising annually. Figure 3 demonstrates that, as of 2021, the number of articles relating to research on anti-fungal pathogens is continually increasing, growing substantially from 257 in 2008 to 962 in 2021, suggesting that this study area has attracted widespread interest since 2008. There is still great room for progress in the future with increasing attention.  [18], Ioannis et al. [17], Simon et al. [16], Justin et al. [22], Ma et al. [19], Emily et al. [20], Chan-Ho Park et al. [23], Aline et al. [24], Joanna et al. [25], Vivianne et al. [26], John et al. [27], and Matthew et al. [21].

Annual Research Analysis
The literature on plant resistance to fungi infections is primarily focused on the years 2008-2021 in the WoS core collection, and the number of papers published after 2008 is rising annually. Figure 3 demonstrates that, as of 2021, the number of articles relating to research on anti-fungal pathogens is continually increasing, growing substantially from 257 in 2008 to 962 in 2021, suggesting that this study area has attracted widespread interest since 2008. There is still great room for progress in the future with increasing attention.

Countries Assessment
Articles published by countries included in the WoS database can reflect the research level and importance of countries in this field to a certain extent. The data obtained in this study shows that the sources of articles in the WoS database include 124 countries (for details see Supplementary Table S1), and Table 1 lists the top ten countries, namely the United States, China, Germany, India, Australia, the United Kingdom, France, Canada, Brazil, and Italy, accounting for the 93.48% of the total publication volume in the field. The United States and China issued far more documents than third-ranked Germany. This partially reflects that the two countries have paid more attention to plant resistance to fungal pathogens. The local total citation score (TLCS) and the global total citation score (TGCS) can more scientifically reflect their corresponding academic influence collectively. Table 1 shows that the TLCS and TGCS of the United States are larger than those in other countries. We analyzed the annual publication volume of the top ten countries by publication volume, as shown in       Figure 6 shows a map of cooperation between some countries. It can be seen from the Figure that, except for the close cooperation between the United States and China, and the relatively close cooperation between the United States and Brazil, among the United Kingdom, France, Germany, and Canada there are cooperative relations between countries, but they are not very close.  Figure 6 shows a map of cooperation between some countries. It can be seen from the Figure that, except for the close cooperation between the United States and China, and the relatively close cooperation between the United States and Brazil, among the United Kingdom, France, Germany, and Canada there are cooperative relations between countries, but they are not very close.

Institutions Analysis
The articles on plant anti-fungal pathogens included in the WoS database involved a total of 4987 institutions (for information on the remaining institutions, see Table S2 in Supplementary Materials). The top ten are listed in Table 2. The institutions that published the most articles were the USDA from the United States (251 articles) and China (231 articles). Although the number of papers published by these two institutions is not much different, the TLCS and TGCS of the USDA are significantly higher than those of Chinese Acad Agr Sci. Six of the top ten institutions are from China, three are from the United States, and one is from Canada.
Analysis and research institutions can quickly find teams with greater scientific influence in the field, providing quick references for data acquisition and cooperation. In general, the cooperation and exchanges between institutions are relatively close, and the

Institutions Analysis
The articles on plant anti-fungal pathogens included in the WoS database involved a total of 4987 institutions (for information on the remaining institutions, see Table S2 in Supplementary Materials). The top ten are listed in Table 2. The institutions that published the most articles were the USDA from the United States (251 articles) and China (231 articles). Although the number of papers published by these two institutions is not much different, the TLCS and TGCS of the USDA are significantly higher than those of Chinese Acad Agr Sci. Six of the top ten institutions are from China, three are from the United States, and one is from Canada.
Analysis and research institutions can quickly find teams with greater scientific influence in the field, providing quick references for data acquisition and cooperation. In general, the cooperation and exchanges between institutions are relatively close, and the institutions that publish more articles have closer exchanges with other institutions (Figure 7). institutions that publish more articles have closer exchanges with other institutions (Figure 7).   Figure 8 shows the network relationship graph of author cooperation and co-occurrence involved in studies on plant resistance to fungal pathogens (detailed author information is provided in Supplementary Table S4). Wang Guoliang, Oliver Richard p, Friesen, etc., are the most important researchers. In addition, our data show that many researchers are engaged in this research and have a cooperative relationship.  Figure 8 shows the network relationship graph of author cooperation and co-occurrence involved in studies on plant resistance to fungal pathogens (detailed author information is provided in Supplementary Table S4). Wang Guoliang, Oliver Richard p, Friesen, etc., are the most important researchers. In addition, our data show that many researchers are engaged in this research and have a cooperative relationship.  Table 3 shows the top ten journals in terms of publishing volume (see Supplementary  Table S3 for complete information), their impact factor (IF), country of publication, and total citations. As can be seen from Table 3 Table 3 shows the top ten journals in terms of publishing volume (see Supplementary  Table S3 for complete information), their impact factor (IF), country of publication, and total citations. As can be seen from Table 3 Figure 9 and Table 4 shows a network co-occurrence diagram of plant resistance to fungal pathogens (details are provided in Supplementary Table S5). According to the statistics, the most often appearing terms from 2008 to 2021 are resistance, disease resistance, identification, expression, disease, Arabidopsis, genes, infection, S.A., and wheat.  Figure 9 and Table 4 shows a network co-occurrence diagram of plant resistance to fungal pathogens (details are provided in Supplementary Table S5). According to the statistics, the most often appearing terms from 2008 to 2021 are resistance, disease resistance, identification, expression, disease, Arabidopsis, genes, infection, S.A., and wheat.   Resistance  1308  12  Gene-expression  405  3  Identification  724  13  Growth  388  4  Expression  637  14  Plants  371  5  Disease  547  15  Powdery-mildew  370  6  Arabidopsis  538  16  Plant  363  7  Gene  537  17  Biological-control  349  8  Infection  533  18  Defense-Responses  338  9  Salicylic-acid  480  19  Arabidopsis-thaliana  336  10  Wheat  430  20 Botrytis-cinerea 329  We conducted visual analysis in the three time periods of: 2008-2012, 2013-2018, and 2019-2021, to fully comprehend the dynamic changes of keywords. We discovered that biological control was a prominent topic, and that resistance and disease resistance were not the only key phrases that persisted in these three periods with the highest frequency ( Figure 10). From 2008 to 2018, powdery mildew was a relatively hot topic, but from 2019 onwards, its popularity dropped significantly. Wheat was the main research object in 2008-2012, and the research interest in 2013-2018 dropped significantly, but the research interest in 2019-2021 is also the word gene. As can be seen from the graph, research on Arabidopsis has increased significantly since 2013.

Keyword Analysis
We conducted visual analysis in the three time periods of: 2008-2012, 2013-2018, and 2019-2021, to fully comprehend the dynamic changes of keywords. We discovered that biological control was a prominent topic, and that resistance and disease resistance were not the only key phrases that persisted in these three periods with the highest frequency ( Figure 10). From 2008 to 2018, powdery mildew was a relatively hot topic, but from 2019 onwards, its popularity dropped significantly. Wheat was the main research object in 2008-2012, and the research interest in 2013-2018 dropped significantly, but the research interest in 2019-2021 is also the word gene. As can be seen from the graph, research on Arabidopsis has increased significantly since 2013.   To determine the development of a research frontier, we used CiteSpace's burstness feature. The top 20 keywords with the most powerful citation bursts are displayed in Table 5. The Table shows   purpose of this study is to perform a quantitative analysis of 6687 articles published on plant resistance to fungal pathogens included in the WoS database from 2008 to 2021 to identify some research trends and provide references for future researchers. According to the annual publication volume, the publication volume of this research is continuously increasing year after year, attaining significant growth from zero to even more. The first article on plant resistance to fungal pathogens included in the WoS database was published in ORGANIC LETTERS in 1999, in which the authors described the metabolism and detoxification of destruction and Homodestruxin B by oil crops [28]. In addition, in 2003, PHYTOCHEMISTRY published a second related article on the antitoxin produced by cress under biotic stress [29], and the authors of the first two articles were Pedras. In 2008, Wan et al. pointed out that chitin is a component of fungal cell walls, which can be sensed by plant cells to induce plant cell immunity. They found the receptor protein LysM RLK1 required for chitin signaling in Arabidopsis thaliana [18]; PEN1 syntaxin is a component of barley against Ascomycete powdery mildew fungi [30].  2019) found that a gene (HRC) is a decisive factor in resistance to Fusarium head blight (FHB), and the TaHRC sequence can be manipulated by bioengineering methods to improve FHB resistance of other cereal crops [37]; The UNITE database fungal ITS sequences that can identify fungi have increased and become more powerful [38]. Luo et al. (2021) tried introducing five resistance genes into wheat, four of which were functional, indicating that it was feasible to introduce multiple genes to improve plant durability and spectral resistance [39].
There is a difference of 55 articles between the United States and China, but a difference of 22,134 times in TGCS (Table 1); a difference of 20 articles between the U.S. USDA and Chinese Acad Agr Sci in China, but a difference of 2776 times in TGCS (Table 2); four belonged to the United States and none to China (Table 3). These results indicate that the United States has the most prominent contribution and influence on plant anti-fungal pathogens, followed by China. The national and institutional cooperation network map analysis shows that they all have cooperative relations. For example, the most comprehensive UNITE database of fungi identification is jointly established by Sweden, the United Kingdom, the United States, Germany, and other countries. UNITE is the most commonly used database for comparing fungal taxonomy and annotation after ITS high-throughput sequencing [38].
Visual analysis of keywords shows that the research content of researchers is also more diversified. Due to the long time required for traditional crossbreeding to select virus-resistant varieties, chemical fungicide drug residues will cause serious environmental pollution [40]. Therefore, exploring more effective methods to solve this problem is necessary. Through the analysis of keywords, the current main research can be classified into the following five categories: (1) At the molecular level, research on the transmission route, reproduction mode, regulatory mechanism, and interaction mechanism between virus and host of fungal pathogens, disease resistance genes, and susceptibility diseases, gene mapping, using gene editing technology to target knockout or overexpression of key genes to obtain varieties with strong disease resistance; (2) Extract secondary metabolites secreted by plants with anti-fungal pathogens to make anti-fungal agents for protection, plants are protected from infection by some fungal pathogens; (3) Identify the signaling pathways of fungal pathogens infecting plant hosts, and edit key regulatory factors upstream of the signaling pathways to avoid infection of plant hosts by fungal pathogens; (4) Further improve the established fungal molecular identification database, such as UNITE database (https://unite.ut.ee/, accessed on 18 October 2022) [38], or establish a fungal pathogen identification database; (5) Develop metal nanomaterials to make pesticides and nano herbicides and realize the combination of green chemistry and nanobiotechnology.

Conclusions
Our research shows that articles on plant anti-fungal pathogens are increasing each year. Through bibliometric analysis of the articles included in WoS from 2008 to 2021, the following conclusions are drawn: (1) The top three countries in terms of publication volume are the United States, China, and Germany; among the ten institutions, six are in China, three in the United States, and one in Canada. The top ten journals are from the United States, the United Kingdom, Switzerland, the Netherlands, and Germany; the United States has the strongest comprehensive influence, followed by China; (2) The cooperative relationship between different countries needs to be further strengthened; (3) The systematic omics and comparative omics (informatization) databases should be integrated to facilitate collaborative research; (4) The research has a significant interdisciplinary nature. There are still a lot of issues and challenges in the current research that need to be further solved.