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Review

Global Research Trends and Hotspots in White Clover (Trifolium repens L.) Responses to Drought Stress (1990–2024)

by
Xiaolin Deng
1,†,
Xiangtao Wang
2,†,
Yuting Yang
2,
Junqin Li
2,
Yang Gao
1,*,
Haiyan Huang
2,
Yu Zhang
1,
Jing Du
1 and
Puchang Wang
2,*
1
School of Karst Science, Guizhou Normal University, Guiyang 550025, China
2
School of Life Sciences, Guizhou Normal University, Guiyang 550025, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Sustainability 2025, 17(5), 1883; https://doi.org/10.3390/su17051883
Submission received: 25 December 2024 / Revised: 16 February 2025 / Accepted: 20 February 2025 / Published: 22 February 2025
(This article belongs to the Section Sustainable Agriculture)
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Abstract

:
White clover (Trifolium repens L.) is cultivated worldwide as a forage crop, green manure, and turfgrass, valued for its adaptability and broad distribution. Although numerous studies have investigated the adverse effects of drought stress on white clover growth and yield, a comprehensive bibliometric review has been lacking. To address this gap, we analyzed relevant publications from the Web of Science Core Collection (1990–2024) using VOSviewer (1.6.19.0) and R (4.3.1) software. Our findings reveal a consistent annual increase in research outputs, indicating sustained scholarly efforts to enhance white clover’s drought tolerance. China, New Zealand, Australia, the United States, and France lead in publication volume and maintain active international collaborations. Keyword co-occurrence analysis underscores the importance of phenotypic, physiological, and molecular mechanisms linked to drought resistance, particularly regarding plant growth and yield. Emerging directions include further exploration of transgenic technologies and molecular pathways to bolster white clover’s resilience under water-limited conditions. Overall, these insights offer a theoretical foundation for future research and provide a valuable reference for advancing sustainable agricultural practices in arid and semi-arid environments.

1. Introduction

Global climate change has led to more frequent and prolonged drought events, posing significant risks to agricultural productivity and ecosystem stability worldwide [1,2,3]. Among the most severe abiotic stresses, drought can drastically reduce plant growth and yield, particularly in regions already facing water scarcity [4]. According to recent predictions, such water deficits will become even more pronounced as temperatures continue to rise, thus expanding arid zones across many parts of the world [5]. Addressing the global challenge of drought stress is therefore imperative for ensuring food security, protecting natural habitats, and maintaining economic vitality. Consequently, understanding the mechanisms underlying drought resistance in plants has become a major objective in plant biology, agronomy, and ecology [6,7,8].
Drought stress restricts plants’ access to adequate water, impairing their ability to maintain vital physiological and metabolic functions [6]. Under water-deficit conditions, plants often experience lowered leaf water potential, reduced stomatal conductance, impaired photosynthesis, and decreased biomass accumulation [9,10,11]. At the cellular level, oxidative stress intensifies when reactive oxygen species (ROS), including superoxide anions and hydrogen peroxide, accumulate in plant tissues [12,13]. This build-up of ROS can damage membranes, proteins, and nucleic acids, eventually triggering cell death if not managed effectively [14,15]. To survive and reproduce under water-limited scenarios, many plant species display a suite of adaptive strategies, ranging from morphological adjustments—such as reduced leaf area or increased root-to-shoot ratios—to metabolic modifications, including osmotic regulation and antioxidant defense [15,16,17,18]. Additionally, molecular responses, such as the upregulation of drought-related genes, the activation of transcription factors, and the production of osmoprotectants, enable plants to endure prolonged periods of water scarcity [19].
White clover (Trifolium repens L.) is widely recognized as both an agriculturally and ecologically significant species. Although originally endemic to Europe, it is now cultivated worldwide for its high-quality forage attributes, nitrogen-fixing capabilities, and ease of establishment [20]. Its versatility has made it a preferred choice for multiple applications, including forage production, green manure, and urban turfgrass, reflecting its ability to thrive across diverse habitats [21]. From an economic perspective, white clover supports more sustainable livestock operations due to its rich nutritional profile, thereby enhancing both the quantity and quality of forage-based livestock products [22]. Ecologically, the plant’s symbiotic relationship with rhizobacteria reduces the need for synthetic nitrogen fertilizers, mitigating environmental pollution and improving soil health [23,24]. Despite these benefits, white clover exhibits notable limitations when confronted with severe drought. Its creeping stolons and relatively shallow root system make it more susceptible to water deficits than deep-rooted species, resulting in substantial yield reductions and, in extreme cases, plant mortality [25].
Given the increasing frequency of drought events under climate change scenarios, research on white clover’s drought tolerance has intensified. Although numerous studies have examined the plant’s phenotypic and physiological responses—such as reduced leaf photosynthesis, antioxidant enzyme activation, and alterations in root morphology—a comprehensive analysis integrating findings from molecular genetics, stress physiology, and agronomic practice remains lacking [25,26,27,28,29]. The scarcity of an up-to-date bibliometric review on white clover’s drought responses hampers efforts to identify overarching themes, emerging research frontiers, and critical knowledge gaps. Such insights are vital for guiding future experimental research and for informing policies aimed at enhancing agricultural sustainability in arid and semi-arid regions.
To address this gap, the present study conducts a comprehensive bibliometric analysis of publications focusing on white clover’s drought tolerance between 1990 and 2024. Specifically, we examine global publication trends, collaborating countries and institutions, prevalent research themes, and the evolution of keywords related to drought resistance mechanisms. By synthesizing both quantitative (e.g., publication counts, citation metrics) and qualitative (e.g., keyword networks, co-citation clusters) findings, this study aims to identify key research hotspots and developmental trajectories, providing a theoretical foundation for future research on white clover drought resilience. Ultimately, these insights will support the advancement of sustainable agricultural practices in arid and semi-arid regions, where drought poses a growing threat to agricultural productivity.

2. Materials and Methods

2.1. Data Sources

The Web of Science Core Collection is one of the most widely used citation databases for bibliometric analysis, covering high-impact journals, conference proceedings, and books across multiple disciplines. Recent studies [30,31] in Scientometrics have highlighted its comprehensive nature and robust indexing criteria. Unlike other databases, Web of Science applies strict inclusion standards, ensuring high-quality and influential publications in scientific research. This database is frequently used in bibliometric studies for analyzing research trends and collaboration networks [32,33]. The Web of Science Core Collection comprises six key citation indexes: SSCI (1956–present), SCI-Expanded (1990–present), A&HCI (1975–present), CPCI-S (1991–present), CPCI-SSH (1991–present), and ESCI (2015–present). Recent studies in Scientometrics [30,31,32,33] emphasize the relevance of Web of Science in assessing global research output and scientific collaboration. By using this database, we ensure comprehensive coverage of the peer-reviewed literature relevant to white clover drought stress research.
Bibliometric analysis was conducted using R and VOSviewer, two widely recognized tools for quantitative analysis of the scientific literature. According to recent studies in Scientometrics [30,31,32,33]. R’s ’Bibliometrix’ package provides robust statistical functions for bibliometric data, while VOSviewer excels in network visualization of co-citation, co-authorship, and keyword co-occurrence relationships. By employing these tools, we provide a comprehensive and data-driven assessment of research trends in white clover drought stress studies. The database literature of Web of Science from Guizhou Normal University library, which is selected in this paper, is from the year of 1985 to the year of 2024 [34]. The advanced retrieval method was used multiple times to retrieve and compare topics. The topics were used as follows: TI = (“Trifolium repens” OR “White Clover”) AND (“Water deficiency” OR “drought tolerance” OR “moisture stress” OR “tolerance to drought” OR “water stress” OR “drought resistance” OR “drought-tolerant” OR “drought stress”), and the language was “English”, with the time span being “1990–2024” (Figure 1).

2.2. Data Analysis

Bibliometric analysis of the published studies on the effects of drought stress on white clover was conducted using R and VOSviewer visualization tools. The aim was to identify research hotspots and emerging frontiers. R software facilitates a variety of analyses of documents from Web of Science databases, including statistical analysis, data preprocessing, co-occurrence matrix construction, co-citation analysis, coupling analysis, co-word analysis, and cluster analysis [35,36,37]. The “Bibliometrix” package in R was primarily used to generate maps illustrating yearly publication trends and analyze keyword topic trends. The following steps were undertaken in R 4.3.1: (1) Install the “Bibliometrix” package; (2) Load the package with library (bibliometrix); (3) Use the “Biblioshiny” interface; and (4) Import BibTeX or plain text files, and set parameters to visualize data on publication volume, thematic keyword analysis, and country/journal/author relationships (e.g., Sankey diagrams).
VOSviewer, a widely used bibliometric analysis tool, was employed for additional keyword co-occurrence analysis, as well as for analyzing collaborations between countries, authors, institutions, and funding agencies. It was also used for co-citation analysis of journals and references. VOSviewer generates three types of visual maps: network visualization, coverage visualization, and density visualization [38,39]. For this study, VOSviewer (version 1.6.19) was used to perform network analysis (of countries, authors, institutions, and journals) and keyword clustering analysis. The process in VOSviewer was as follows: (1) Create bibliographic data; (2) Read data from bibliographic files; (3) Import plain text or tab-delimited text data; and (4) Set parameters to generate visualization results. The generated visual maps consist of nodes and connecting lines. Nodes represent selected entities, such as organizations or keywords, and the size of the nodes reflects the frequency of occurrence, with larger nodes indicating higher frequency. The connecting lines illustrate relationships, such as cooperation or keyword co-occurrence, and the density of the lines represents the strength of these relationships. Denser lines indicate higher frequency or stronger cooperation.

3. Results

3.1. Analysis of the Number of Publications and Citations

A total of 447 papers on the effects of drought stress on white clover were identified from 1990 to 2024. Figure 2 presents trends in the number of publications and the average citations per paper. Overall, the publication output shows an increasing trajectory, peaking in 2024 (23 papers), followed by secondary peaks in 2020 and 2022. In addition, Figure 2 illustrates fluctuations in the average number of citations per paper. Notably, 1996 recorded the highest average citations per article within the Web of Science (WoS) database.

3.2. Distribution of Countries and Institutions

Figure 3 displays the publication output and collaborative relationships among countries in the research on white clover drought stress. Cluster 1 is centered around Australia and New Zealand, with a high volume of publications and close collaboration. Cluster 2 is led by China and the United States, taking the lead in publication volume and significant cooperation. In Cluster 3, France, the United Kingdom, and Spain are active in research and have tight collaborative ties. Cluster 4 is dominated by Germany, contributing to the research field. In Cluster 5, Switzerland has the highest publication output but weaker collaborative links. Overall, China stands out in terms of publication volume and international collaboration, consistent with the results shown in Table 1, highlighting its significant role in scientific research in this field.
Table 1 presents the distribution of publications by country. China ranks first globally with 82 papers (25.5% of total publications), followed by New Zealand (56 papers), Australia (51), the United States (49), and France (32), which contribute 17.4%, 15.8%, 15.2%, and 10% of global publications, respectively. Although France has fewer publications, it holds the highest average citation rate (45.63), closely followed by Switzerland (45.10). In terms of total citations, China ranks second (1923), just behind the United States (2019). France (1460), New Zealand (1285), and Australia (1130) also feature among the top five in total citations.
Figure 4 illustrates the volume of publications and collaborations among institutions in the study of white clover response under drought stress. The analysis shows that there are 115 institutions with more than 2 publications, forming three main clusters centered on Sichuan University, Massey University, and the University of Lincoln. These three institutions not only ranked in the top three in terms of the number of publications but also had the closest collaborations with other institutions, highlighting their important contributions in this research field.
Table 2 provides a comprehensive statistical analysis of the top ten research institutions in the Web of Science database based on the number of publications. Sichuan Agricultural University led the list with 43 articles and 1142 total citations, followed by Massey University and Lincoln University, which made significant contributions to the drought resistance research of white clover, highlighting the academic influence and importance of their research results. In addition, the University of Caen ranked first with an average citation rate of 62.71 citations per article, demonstrating the high recognition of its research in the international academic community.
Funding agencies play a critical role in supporting research and facilitating publication. As shown in Figure 5, the National Natural Science Foundation of China (NSFC) is the leading funding organization, supporting 20 studies (30.77%). Among the top funding agencies, six are based in China, two in Australia, and one each from New Zealand and the European Union. This distribution of funding underscores China’s significant dominance in this research area, reflecting the country’s robust investment in scientific research and financial backing.

3.3. Main Journals and Most Impacting Papers

Figure 6 displays a co-citation knowledge map of journals publishing white clover drought research. The thickness of connecting lines denotes the frequency and intensity of co-citation. Plant Physiology emerges as the largest node, reflecting its high citation rate in this field—a result that underscores the journal’s influence and the volume of published articles. Within the red cluster, Plant Physiology, Crop Science, and Plant and Soil demonstrate particularly strong co-citation links. The blue cluster features top-tier journals in nature, science, and ecology, indicating robust scholarly exchanges. The green cluster focuses on crops and turfgrass, centering on Crop Science and Turfgrass Science. Finally, the yellow cluster highlights soil environment research, with Plant and Soil and the Australian Journal of Agricultural Research exhibiting strong co-citation relationships. These findings emphasize the interdisciplinary nature of white clover drought research.
Figure 7 depicts the flow of publications among countries, journals, and authors. Crop and Pasture Science ranks first in this domain, featuring a concentrated collaboration network and major contributions from author Williams W.M. In contrast, Environmental and Agricultural Experiments and Functional Plant Biology show more dispersed collaboration patterns. Australia stands out as the primary contributing country, although its international collaboration network is not centralized. In the Frontiers in Plant Science cluster, author Li Z has the highest number of publications, ranking first.
Among the highly cited papers, those on physiological and molecular mechanisms account for three papers each, indicating that research in these areas remains central to white clover drought resistance research (Table 3) [40,41,42,43,44,45]. There were two papers related to enhancing drought resistance through technology (Table 3) [46,47], and one paper each on breeding and morphological responses (Table 3) [23]. These works cover multiple levels of investigation—from physiology and molecular biology to applied technology—demonstrating the breadth and complexity of drought tolerance research in white clover. Notably, the paper titled “Peroxide and lignification in relation to the intensity of water-deficit stress in white clover” [40] holds the highest average annual citation frequency at 11.53, significantly higher than the other papers. Its local citation score (LCS)—the number of citations within the currently selected dataset—is also the highest, indicating its strong relevance to current research in the field. Additionally, its high total citation count reflects its widespread recognition by the global scientific community.

3.4. Research Hotspots and Evolution Trend Analysis

3.4.1. Topic Keyword Mapping and Hotspot Evolutionary Trends

Keywords are central to capturing the essence of the content and themes in the academic literature, offering valuable insights into emerging research trends. In this study, we conducted a keyword cluster analysis of the literature on white clover’s drought stress research. Keyword co-occurrence analysis and keyword cluster analysis are effective methods to detect hot topics and research frontiers in specific academic fields. The results of keyword co-occurrence analysis, conducted using VOSviewer, are shown in Figure 8.
The co-occurrence of keywords offers valuable insights into the intrinsic connections, research hotspots, and potential future directions within a field. Table 4 highlights the top 20 most frequently occurring keywords in white clover drought tolerance research. Notably, “drought stress” and “white clover” are the most dominant keywords, followed by “growth”, “yield”, and “nitrogen”. This indicates the significant impact of drought on both the growth and yield of white clover, suggesting that understanding the drought–growth–yield relationship is foundational to research in this area.
The keyword co-occurrence network diagram (Figure 8) identifies five pivotal clusters in white clover drought resistance research: (1) The Red Cluster focuses on molecular and physiological responses to stress, including protein synthesis and gene interactions. (2) The Green Cluster emphasizes physiological responses to stress, such as protein synthesis interactions. (3) The Blue Cluster centers on molecular responses to stress, including DNA methylation and gene interactions. (4) The Yellow Cluster examines photosynthesis and leaf morphology adaptations to drought stress. (5) The Purple Cluster investigates the relationship between white clover and microorganisms, as well as variety selection.

3.4.2. Identification of Research Frontiers

Figure 9 illustrates the thematic analysis of keywords in white clover drought research, highlighting major research areas and trends.
First Quadrant (Top Right)–Active Topics: Contains keywords such as “abscisic acid” and “hydrogen peroxide”. These are actively researched areas due to their importance in agricultural productivity and ecosystem health, reflecting a well-established research base and international relevance.
Second Quadrant (Top Left)—Specialized/Niche Topics: Includes highly specialized topics, such as “transcription factor gene”. While niche, these topics represent areas of in-depth specialization in white clover research, particularly in improving drought tolerance and exploring novel drought-resistant applications.
Third Quadrant (Bottom Left)—Emerging or Fading Themes: Features themes like “herbage”, indicating shifting research interests or emerging new directions.
Fourth Quadrant (Bottom Right)—Basic Themes: Focuses on core topics like “drought stress”, “growth”, “yield”, and “nitrogen”. These foundational themes are central to research on abiotic stress responses in white clover and are closely linked to other research areas.

4. Discussion

Drought stress is widely recognized as one of the most severe abiotic challenges facing agricultural systems in the era of escalating climate change [48]. Rising temperatures and declining precipitation in many regions have exacerbated water deficits, placing immense pressure on both staple and forage crops. In this global context, white clover (Trifolium repens L.) has emerged as a focal species due to its multifaceted roles in agriculture: it serves as high-quality forage, an effective nitrogen fixer for soil enrichment, and a valuable turfgrass in urban landscapes [23]. However, these benefits can be rapidly undermined by drought conditions, which reduce white clover’s productivity and thereby threaten the stability and sustainability of agricultural outputs and ecosystem services. Building on an expanding body of literature investigating the phenotypic, physiological, and molecular responses of white clover to drought [49,50,51], the present study offers a comprehensive bibliometric analysis spanning more than three decades (1990–2024). Unlike earlier reviews that centered on experimental methodologies or single aspects of drought tolerance—such as antioxidant enzyme activities or morphological traits—this work synthesizes publication trends, keyword co-occurrence networks, and collaboration analyses to present a panoramic view of the evolving research landscape. Such an integrative overview is critical not only for identifying existing knowledge gaps but also for guiding future research toward more comprehensive and sustainable approaches.

4.1. Response Mechanism of White Clover to Drought Stress

4.1.1. Effects of Drought Stress on Yield

Achieving both high yield and stress tolerance remains a core challenge in plant science. White clover is globally recognized as a valuable leguminous forage crop for its excellent forage quality and high yield potential; however, its creeping growth habit and shallow fibrous root system render it particularly susceptible to drought [52,53]. Additionally, white clover often exhibits lower water-use efficiency, exacerbating its vulnerability to water scarcity [54]. Numerous studies have identified drought and high temperatures as primary environmental factors constraining white clover yield. Under unirrigated conditions, growth declines significantly, with both stolon number and overall biomass severely affected by drought stress. Conversely, irrigation can substantially improve yields—especially during summer drought—by mitigating soil moisture deficits and promoting stolon production [55,56]. While white clover typically reproduces vegetatively under favorable conditions, severe drought can prompt seedling recruitment to ensure population survival.
In mixed plantings with perennial ryegrass, water stress substantially inhibits white clover growth, whereas ryegrass produces more dry matter under the same conditions [57]. As water stress intensifies, both above-ground and below-ground dry matter, along with stem and leaf biomass, decrease markedly [58]. Under severe water scarcity, white clover performs worse than it does in monoculture, likely due to a smaller root system and limited water uptake capacity. Nevertheless, white clover remains a popular choice for crop rotations and organic farming because of its nitrogen-fixing ability, which enhances forage quality, prolongs the grazing season, and improves livestock performance [59].
Subsequent studies have investigated water relations, photosynthesis, respiration, and the accumulation of osmoregulatory compounds in plants. Research before 2000 largely focused on the morphological responses of white clover to drought, examining changes in leaf size, root structure, and growth habits, as well as overall reductions in biomass and yield. During this period, researchers also explored basic physiological traits such as photosynthesis, respiration, water-use efficiency, and the accumulation of osmoregulatory substances. While these studies established a foundational understanding of drought stress at the whole-plant level, they often employed single-factor analyses, overlooking interactions with other environmental variables [51].

4.1.2. Effects of Drought Stress on the Physiology and Biochemistry

Drought stress induces marked oxidative stress in perennial plants like white clover, leading to the accumulation of reactive oxygen species (ROS), including superoxide anions, hydrogen peroxide, and hydroxyl radicals [60]. These ROS can cause extensive oxidative damage, reducing plant growth and yield. Under drought conditions, white clover shows increased electrolyte leakage, elevated malondialdehyde (MDA) levels, and the accumulation of hydrogen peroxide and proline [56]. As a byproduct of lipid peroxidation, MDA serves as a key indicator of oxidative injury [61]. To combat such damage, white clover upregulates antioxidant genes and increases the activity of ROS-scavenging enzymes, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) [62,63,64,65]. While SOD catalyzes the conversion of superoxide radicals into hydrogen peroxide and oxygen, CAT further breaks down hydrogen peroxide into water and oxygen, thereby alleviating drought-induced oxidative stress [66,67].
Drought tolerance varies among white clover genotypes, as illustrated by differences in MDA content and CAT activity [68]. Genotypes with smaller leaves often exhibit lower increases in MDA and higher CAT activity at the onset of drought, indicating stronger intrinsic drought resistance [69]. Drought stress also constrains photosynthesis and growth by damaging cell membranes [70]. In response, white clover undergoes significant physiological, biochemical, and anatomical alterations. For instance, applying luteolin under drought conditions markedly enhances osmoregulation and water-use efficiency, thereby fostering plant growth [71]. Luteolin-treated plants typically show higher chlorophyll content and net photosynthetic rates than untreated controls, underlining its role in stress tolerance.
Plant polyamines (PAs) also play vital roles in mitigating environmental stresses [72]. Exogenous application of PAs can bolster drought tolerance by maintaining ROS homeostasis through the regulation of antioxidant enzymes and gene expression, partly mediated by the calcium-dependent protein kinase (CDPK) pathway [73]. Growth regulators, such as indole-3-acetic acid (IAA), likewise aid plants in coping with drought. Treatments with IAA alleviate dehydration, increase stem dry weight, raise leaf relative water content, and boost total chlorophyll levels [74,75]. Meanwhile, elevated abscisic acid (ABA) concentrations enhance drought tolerance by inducing drought-resistance genes and modulating dehydration stress genes via bZIP transcription factors [76,77,78].
Additionally, drought stress reduces stomatal conductance, thereby limiting transpiration and photosynthesis [79]. This reduced CO2 availability lowers photosynthetic efficiency and rates [80,81,82]. Under severe drought, enzyme activities and photosynthesis-related proteins in chloroplasts are also impaired, further undermining photosynthetic processes [83,84,85].
With the advent of new analytical techniques and methodologies, research from approximately 2000 to 2010 increasingly delved into the physiological and biochemical dimensions of drought stress. This period marked an initial foray into examining cellular structures and organelle functions, including membrane stability under water deficit. Researchers also began identifying drought-responsive proteins, although these efforts were primarily exploratory and limited to specific pathways or mechanisms. Additionally, multi-factor studies emerged, exploring interactions between drought and other environmental variables, thus setting the stage for more holistic approaches [86,87].

4.1.3. Effects of Drought Stress on the Molecular

Key proteins involved in drought responses include Rubisco-binding proteins (RBPs), Rubisco-activating proteins (RAs), and heat shock proteins (HSPs), all of which help stabilize and fold proteins under stressful conditions [88]. Although the expression of RAs and Rubisco subunits remains relatively unchanged—reducing their utility as tolerance markers—RBP levels rise significantly in drought-stressed white clover [89]. This upregulation suggests that RBPs are crucial for maintaining protein stability under water scarcity. Additionally, protective molecules that prevent protein aggregation and denaturation form part of the molecular drought-resistance network [22]. Calpains, for instance, degrade damaged or nonfunctional proteins and are notably induced in drought-stressed plants [90], highlighting their potential importance as molecular markers. Understanding these molecular pathways provides a clearer perspective on the regulatory networks underpinning the physiological and biochemical adaptations of white clover to drought, thereby informing the development of drought-tolerant germplasm and sustainable agricultural strategies.
Over the past decade, the focus has increasingly shifted toward elucidating the molecular mechanisms of drought stress. High-throughput sequencing technologies, such as RNA sequencing (RNA-seq), enable comprehensive analyses of gene expression changes and facilitate the identification of key regulatory genes. Proteomic and metabolomic approaches have also revealed complex biochemical and molecular reprogramming—including shifts in hormone signaling, transcription factor networks, and metabolic pathways—under drought conditions [91]. Recent studies emphasize integrated multi-factor analyses that address how drought interacts with additional stressors (e.g., heat, nutrient limitations, competition), offering a more holistic view of white clover’s physiology and productivity under water-limited environments.

4.2. Drought-Resistant Technologies of White Clover

Improving the productivity and ecological functions of white clover under drought conditions is central for its sustainable use, especially in regions prone to water scarcity. Recent studies emphasize the importance of selecting drought-tolerant varieties and employing evidence-based cultivation practices to enhance both adaptability and yield under water-limited conditions [92,93]. While significant progress has been made in identifying drought-tolerant traits, the methods used to assess drought resistance in white clover play a key role in shaping our understanding of its potential for agricultural improvement. The study of drought tolerance in white clover has relied on several experimental approaches, each with its own set of advantages and limitations. Broadly, these methods can be classified into controlled-environment experiments, field-based assessments, and physiological or molecular analyses. Each approach offers valuable insights into how white clover responds to drought stress, but no single method can fully capture the complexity of drought stress responses in natural conditions [94,95].
Controlled-environment experiments, such as greenhouse studies, are among the most frequently used methods for assessing drought tolerance in white clover. These experiments offer precise control over variables such as water availability, temperature, and humidity, enabling researchers to isolate the effects of drought on plant growth and yield [96]. Common techniques include withholding water for predetermined periods to simulate drought, followed by evaluations of plant survival, growth rates, and physiological parameters (e.g., photosynthetic rate, stomatal conductance) [97]. The advantages of controlled-environment experiments include a high level of control over environmental factors, the ability to replicate specific drought scenarios and compare treatments directly, and the capacity to screen large numbers of genotypes in a relatively short time. However, these experiments have limited ecological relevance due to their artificial settings, which fail to capture soil heterogeneity, pest pressures, and interspecies competition [98].
In contrast, field-based studies are essential for evaluating the performance of white clover under real-world drought conditions. Such studies involve growing white clover in its natural environment or in managed agricultural systems, then monitoring drought responses over multiple growing seasons. Field trials may incorporate various soil types, irrigation practices, and co-cultivation with other species (e.g., grasses or other legumes) [99]. The primary advantages of field-based assessments are their real-world relevance and the opportunity for long-term evaluation. Field conditions account for complex environmental interactions—such as soil composition, water availability, and pest pressures—while allowing researchers to assess drought tolerance over extended periods, thus providing a more holistic view of plant resilience [90,91]. Nevertheless, environmental variability in field settings can complicate the replication of results, and these studies often require greater investment in terms of time, land, and resources [100].
Beyond basic growth measurements, physiological analyses are critical for understanding the mechanisms underlying drought tolerance. These analyses may include the measurement of key drought-related traits such as osmotic adjustment, chlorophyll content, stomatal conductance, and leaf water potential [101]. Advances in molecular techniques, including transcriptomics and proteomics, further enable researchers to explore gene expression and protein profiles associated with drought stress [102]. The advantages of physiological and molecular approaches lie in their capacity to offer in-depth insights into the biological mechanisms conferring drought tolerance in white clover, and they can be applied in both controlled-environment and field contexts [41]. However, these methods can be resource-intensive, requiring specialized equipment and expertise, and the resulting data often need to be integrated with field or whole-plant assessments to gain a comprehensive understanding of drought tolerance in real-world environments [103].
To advance research on drought resistance in white clover, a multifaceted strategy that combines controlled-environment studies, field-based assessments, and molecular techniques is crucial. Precision agriculture tools, such as remote sensing, soil moisture sensors, and unmanned aerial vehicles (UAVs), can augment data collection during field trials [104]. Additionally, genomic tools—such as genome-wide association studies (GWAS) and CRISPR/Cas-mediated genome editing—offer new avenues for identifying and modifying drought-tolerant traits [105]. By integrating these complementary methods, researchers can more effectively characterize drought responses and accelerate the development of white clover cultivars better suited to water-limited environments.

4.3. Research Gaps and Challenge

Despite considerable advances in understanding the drought stress responses of Trifolium repens (white clover), several critical research gaps remain. First, while numerous candidate genes and quantitative trait loci (QTL) related to drought tolerance have been identified, the discovery and integration of molecular markers specific to white clover are still in the early stages [86]. The application of these markers in practical breeding programs, particularly within robust marker-assisted selection (MAS) frameworks, has not yet been fully realized [106]. Further development of molecular markers holds significant potential to accelerate the genetic improvement of white clover for enhanced drought tolerance.
Second, transgenic approaches and genome-editing technologies—such as the introduction of drought-tolerant genes from Arabidopsis or Medicago sativa—represent promising strategies for improving drought resilience in white clover [88]. However, the widespread adoption of these technologies is hindered by regulatory complexities, public acceptance concerns, and challenges related to polyploidy and the multi-subgenome systems inherent in white clover. Overcoming these barriers is crucial to advancing the practical application of genetic engineering in this species [107]. Additionally, the ethical and regulatory frameworks governing transgenic crops remain a significant challenge, particularly in countries where public opinion on genetically modified organisms (GMOs) is divided.
Another challenge lies in the over-reliance on controlled-environment or greenhouse experiments, which often fail to capture the full complexity of field conditions. In real-world agricultural settings, factors such as soil heterogeneity, pest pressures, competition with other species in mixed swards, and seasonal variability can significantly influence drought tolerance. Future research should therefore prioritize field-based studies that more accurately reflect the diverse environmental conditions under which white clover is cultivated [108,109].
Moreover, there is a notable underrepresentation of research from arid and semi-arid regions, particularly in Africa and Latin America, where drought stress poses a significant threat to agriculture. Contributing factors include limited infrastructure, funding constraints, and the predominance of research published in non-English journals, which are often overlooked in bibliometric analyses relying on conventional English-language databases, such as Web of Science. This geographical bias distorts the global research landscape, favoring wealthier nations with greater research capacity. To address this limitation, future bibliometric studies should incorporate a wider range of databases, including non-English language publications and open-access platforms, such as Google Scholar. This would provide a more inclusive and comprehensive overview of global research trends in drought tolerance in white clover [28].
Several studies [30,33] suggest that Web of Science primarily indexes English-language journals, leading to the underrepresentation of research published in non-English languages. We acknowledge that our study may not fully capture relevant non-English literature, particularly from regions where white clover research is prominent but published in local languages (e.g., Spanish, Chinese, and Russian). Additionally, Web of Science primarily includes English-language literature, which may result in the omission of funding information from non-English-speaking countries. Some studies indicate that Web of Science does not consistently provide complete funding information, with certain funding acknowledgments either missing or inconsistently reported across different publishers and disciplines [110,111]. Funding details tend to be more comprehensively recorded in STEM fields than in the social sciences and humanities. While Web of Science remains a valuable resource for examining funding trends, these limitations should be considered when interpreting the financial support for white clover drought research.
Recent studies [112,113,114] suggest that Scopus offers broader journal coverage, particularly for non-English publications. In contrast, Web of Science tends to index journals with higher impact factors and more stringent indexing criteria. While both databases are valuable, we relied on Web of Science for this study due to its long-standing use in bibliometric analyses and its well-established citation-based metrics, which are conducive to robust trend analysis in white clover drought research. Nevertheless, we recognize that using Scopus could yield slightly different results, and future studies would benefit from comparative analyses across multiple databases.
It is also worth noting that Web of Science’s focus on high-impact journals may overlook important research published in lower-tier or regional journals, particularly those focusing on applied agricultural research. Furthermore, reports, theses, and non-peer-reviewed publications are not indexed, potentially leaving gaps in the research landscape. Citation-based metrics may also be influenced by self-citations and disciplinary trends, which could over-represent certain regions or research groups. To obtain a more comprehensive view of white clover drought research, future studies could benefit from integrating multiple databases (e.g., Scopus, Google Scholar, Dimensions).
In conclusion, while significant progress has been made in understanding drought stress responses in white clover, critical research gaps remain. Key areas for further exploration include the development of molecular markers, the application of marker-assisted selection, and the advancement of genome-editing technologies. Additionally, more field-based studies are needed to capture real-world environmental conditions, as current research often relies on controlled experiments. Geographic gaps, particularly in arid regions, and the underrepresentation of non-English publications should also be addressed. Overcoming regulatory and public acceptance challenges related to transgenic approaches is crucial. Addressing these gaps will enhance drought tolerance in white clover and contribute to more sustainable agricultural practices in water-scarce environments.

4.4. Perspectives on Drought Tolerance in White Clover

Given these gaps and uncertainties, several research directions appear particularly promising. First is the integration of advanced omics approaches. Employing transcriptomics, proteomics, and metabolomics can deepen our understanding of drought-responsive pathways in white clover, revealing unexplored layers of regulation, including epigenetic modifications and post-translational protein dynamics [20,106,115]. Second, genome-editing tools such as CRISPR/Cas offer the potential to target specific drought-responsive genes or regulators. Validating the functions of candidate genes (e.g., NAC, DREB, bZIP) could enable breeders to develop more precise and efficient strategies for improving drought tolerance [116]. Third, the development of hybrids and sustainable cultivation practices continues to hold significant potential. Crosses with related clover species (e.g., Trifolium ambiguum) or advanced backcross lines may produce germplasm that combines a deeper root system with white clover’s nitrogen-fixing capabilities [117]. Concurrently, refining soil management through mulching, organic amendments, or reduced tillage, as well as optimizing irrigation intervals, can help mitigate drought impacts [118]. Finally, climate modeling and ecological simulations using crop models (e.g., DSSAT, APSIM) and regional climate forecasts can reveal how shifting temperature and precipitation patterns might shape white clover distribution and productivity. Such simulations could also inform adaptive management strategies, including cultivar selection tailored to future climate scenarios.

5. Conclusions

Research on the drought tolerance of white clover (Trifolium repens L.) has steadily increased over the past few decades. Leading contributors—namely China, New Zealand, Australia, the United States, and France—have consistently produced the largest volume of publications and maintained extensive international collaborations, highlighting the economic and ecological importance of white clover research. Notably, Sichuan Agricultural University stands out with 43 articles and 1142 citations, indicating its prominent role in advancing the understanding of drought tolerance in white clover. In terms of journal co-citation patterns, Plant Physiology, Crop Science, Plant Soil, and New Phytologist exhibit close co-citation relationships with other journals. This interconnectedness reflects not only their high publication volumes but also their considerable influence within the field. Furthermore, analyses of the most cited articles, coupled with keyword mapping, reveal that investigations into the phenotypic, physiological, and molecular mechanisms underpinning white clover’s drought tolerance have been a focal point of research in the last decade. Overall, this study provides a strong theoretical foundation for future research on white clover’s drought resistance, informing both adaptive crop management and breeding programs. By deepening our understanding of the plant’s stress-response mechanisms, researchers and practitioners can more effectively develop white clover varieties that thrive under increasingly volatile climatic conditions, thereby sustaining forage production and enhancing agroecosystem services worldwide.

Author Contributions

Conceptualization, X.D. and P.W.; methodology, P.W.; validation, X.W., J.L., Y.Y. and Y.G.; formal analysis, H.H., Y.Z. and J.D.; data curation, X.D.; writing—original draft preparation, X.D. and X.W.; writing—review and editing, P.W., X.W., J.L., Y.Y. and Y.G.; visualization, H.H., Y.Z. and J.D.; funding acquisition, P.W. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Natural Science Foundation of China (32260351) and the Guizhou Province Science and Technology Foundation of China (Qiankehepingtairencai-GCC [2022]022-1, Qiankehejichu-zk [2025]254).

Data Availability Statement

The original contributions presented in the study are included in the article. Further inquiries can be directed to the corresponding authors.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Figure 1. Detailed flowchart steps of the search strategy in screening publications.
Figure 1. Detailed flowchart steps of the search strategy in screening publications.
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Figure 2. Annual changes in white clover drought research publications (1990–2024).
Figure 2. Annual changes in white clover drought research publications (1990–2024).
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Figure 3. Visualization of national publication output. Different colors represent different clusters, the size of the circles indicates the number of publications, and the thickness of the lines represents the strength of connections between countries.
Figure 3. Visualization of national publication output. Different colors represent different clusters, the size of the circles indicates the number of publications, and the thickness of the lines represents the strength of connections between countries.
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Figure 4. Network visualization map of institutional partnerships in white clover in response to drought stress (f ≥ 2), with different colors indicating different clusters, dot size representing the number of postings, and the width of the connecting line indicating the strength of the collaboration, and f representing the number of publications issued by the institution.
Figure 4. Network visualization map of institutional partnerships in white clover in response to drought stress (f ≥ 2), with different colors indicating different clusters, dot size representing the number of postings, and the width of the connecting line indicating the strength of the collaboration, and f representing the number of publications issued by the institution.
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Figure 5. The related funding agencies. Dot size indicates the number of projects funded by the organization.
Figure 5. The related funding agencies. Dot size indicates the number of projects funded by the organization.
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Figure 6. Mapped knowledge domains for journal co-citation in the field of white clover drought tolerance, (f ≥ 20).
Figure 6. Mapped knowledge domains for journal co-citation in the field of white clover drought tolerance, (f ≥ 20).
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Figure 7. Sankey flow diagram of countries, journals, and authors of papers published in the field of white clover response to drought stress.
Figure 7. Sankey flow diagram of countries, journals, and authors of papers published in the field of white clover response to drought stress.
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Figure 8. Keyword co-occurrence network analysis (occurrence frequency ≥ 3). The same color represents the same cluster, with each node representing different keywords. The size of each node is proportional to the frequency of keyword occurrence, and the degree of co-occurrence between keywords is reflected in the strength of their connections.
Figure 8. Keyword co-occurrence network analysis (occurrence frequency ≥ 3). The same color represents the same cluster, with each node representing different keywords. The size of each node is proportional to the frequency of keyword occurrence, and the degree of co-occurrence between keywords is reflected in the strength of their connections.
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Figure 9. Analysis of keyword themes in white clover drought research.
Figure 9. Analysis of keyword themes in white clover drought research.
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Table 1. Top 10 countries in terms of white clover publications.
Table 1. Top 10 countries in terms of white clover publications.
CountryTCAACNP
China192323.4582
New Zealand128522.9556
Australia113022.1651
USA201941.249
France146045.6332
United Kingdom84332.4226
Germany71229.6724
Switzerland90245.120
Spain73941.0618
Canada30925.7512
NP: Number of published papers; TC: Total citations; AAC: Average article citations.
Table 2. Top 10 organizations in terms of white clover publications.
Table 2. Top 10 organizations in terms of white clover publications.
InstitutionCountryNPTCCPP
Sichuan Agriculture UniversityChina43114226.5581
Massey UniversityNew Zealand1740423.7647
Lincoln UniversityNew Zealand1530220.1333
AgresearchNew Zealand1252944.0833
Chonnam national UniversitySouth Korea1053053
Agricultural and Food Research CouncilUnited Kingdom922725.2222
Institute National de la Recherche AgronomiqueFrance848861
Grassland Environment Research InstituteChina834543.125
La Trobe UniversityAustralia727238.8571
Université de Caen NormandieFrench743962.7143
NP: Number of published papers; TC: Total citations; CPP: Citations per paper.
Table 3. Top 10 highly cited papers in the field of white clover drought resistance research, 1990–2024.
Table 3. Top 10 highly cited papers in the field of white clover drought resistance research, 1990–2024.
RankTitleJournalYearIFTCTC per Year
1Peroxide and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.)Journal of Experimental Botany20076.919611.53
2Progress in Breeding Perennial Clovers for Temperate AgricultureJournal of Agricultural Science20052.0985.16
3Responses to Uv-B radiation in Trifolium repens L.—physiological links to plant productivity and water availabilityPlant Cell and Environment20037.3954.52
4Exogenous spermidine improves seed germination of white clover under water stress via involvement in starch metabolism, antioxidant defenses and relevant gene expressionMolecules20144.6858.5
5Metabolic pathways regulated by chitosan contributing to drought resistance in white cloverJournal of Proteome Research201711.67410.57
6The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white cloverEnvironmental and Experimental Botany20165.7739.13
7Exogenous application of gaba improves peg-induced drought tolerance positively associated with gaba-shunt, polyamines, and proline metabolism in white cloverFrontiers in Physiology20174.0699.86
8Indole-3-acetic acid improves drought tolerance of white clover via activating auxin, abscisic acid and jasmonic acid related genes and inhibiting senescence genesBmc Plant Biology20205.36315.75
9Water-deficit accumulates sugars by starch degradation-not by de novo synthesis-in white clover leaves (Trifolium repens)Physiologia Plantarum20086.4613.81
10Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens)American Journal of Botany20163587.25
Table 4. Top 20 keywords by frequency of occurrence.
Table 4. Top 20 keywords by frequency of occurrence.
Keyword PlusClusterOccurrencesLinksTotal Connection Strength
drought stress123982773
white clover220587599
growth211568376
yield211068333
nitrogen24340142
responses33235114
elevated CO24262485
soil4232989
leaves1223182
photosynthesis4213084
salinity1213893
abscisic acid1203496
fungi5201867
hydrogen-peroxide1203195
Arabidopsis1192776
root5162054
lipid-peroxidation1152773
osmotic adjustment1152869
leaf senescence1142661
proline1143161
“Cluster” refers to the grouping of data points based on their similarity, while “Total Connection Strength” represents the aggregate strength of connections within each cluster, calculated by summing the connection strength between each pair of data points in the cluster.
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MDPI and ACS Style

Deng, X.; Wang, X.; Yang, Y.; Li, J.; Gao, Y.; Huang, H.; Zhang, Y.; Du, J.; Wang, P. Global Research Trends and Hotspots in White Clover (Trifolium repens L.) Responses to Drought Stress (1990–2024). Sustainability 2025, 17, 1883. https://doi.org/10.3390/su17051883

AMA Style

Deng X, Wang X, Yang Y, Li J, Gao Y, Huang H, Zhang Y, Du J, Wang P. Global Research Trends and Hotspots in White Clover (Trifolium repens L.) Responses to Drought Stress (1990–2024). Sustainability. 2025; 17(5):1883. https://doi.org/10.3390/su17051883

Chicago/Turabian Style

Deng, Xiaolin, Xiangtao Wang, Yuting Yang, Junqin Li, Yang Gao, Haiyan Huang, Yu Zhang, Jing Du, and Puchang Wang. 2025. "Global Research Trends and Hotspots in White Clover (Trifolium repens L.) Responses to Drought Stress (1990–2024)" Sustainability 17, no. 5: 1883. https://doi.org/10.3390/su17051883

APA Style

Deng, X., Wang, X., Yang, Y., Li, J., Gao, Y., Huang, H., Zhang, Y., Du, J., & Wang, P. (2025). Global Research Trends and Hotspots in White Clover (Trifolium repens L.) Responses to Drought Stress (1990–2024). Sustainability, 17(5), 1883. https://doi.org/10.3390/su17051883

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