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Review

Resistance of Creeping Bentgrass to Biotic and Abiotic Stresses: A Model System for Grass Stress Biology

by
Zhuang Ren
1,†,
Xinbo Sun
2,*,†,
Yalin Chen
1,*,†,
Yaxi Zhang
2,
Meng Yuan
1,
Mengyu Li
1,
Xiaopeng Ren
1 and
Xiaodong Wang
1,*
1
State Key Laboratory of North China Crop Improvement and Regulation, College of Plant Protection, Hebei Agricultural University, Baoding 071000, China
2
College of Agronomy, Hebei Agricultural University, Baoding 071000, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2025, 15(12), 2761; https://doi.org/10.3390/agronomy15122761
Submission received: 13 October 2025 / Revised: 13 November 2025 / Accepted: 25 November 2025 / Published: 29 November 2025
(This article belongs to the Special Issue Grass and Forage Diseases: Etiology, Epidemic and Management)
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Abstract

Agrostis stolonifera L., commonly known as creeping bentgrass, is an important cool-season turfgrass used in landscaping and sports fields. However, creeping bentgrass is prone to various diseases, including dollar spot, brown patch, and bacterial yellowing, during its maintenance, leading to significant degradation in turf quality, esthetics, and greening functions, resulting in substantial losses in turfgrass production and management. On the other hand, extreme environmental conditions such as high temperatures, drought, and salinity have also caused a decline in the quality of creeping bentgrass. Moreover, creeping bentgrass has a moderately sized genome and is easy to genetically transform, making it an ideal model system for studying grass stress biology. This article provides an overview of the major diseases and stressors in the management of creeping bentgrass and proposes future research directions for the disease resistance and stress tolerance of creeping bentgrass.

1. Introduction

Creeping bentgrass (Agrostis stolonifera L.) is a perennial grass belonging to the Poaceae family, and it is an important cool-season turfgrass. Creeping bentgrass thrives in cold and humid climates and exhibits strong cold resistance and drought tolerance. However, during hot summers, the tips of its leaves may turn yellow, affecting its greening effect. It also has a certain shade tolerance and can grow well in shaded environments. Due to its strong spreading ability and fast establishment, creeping bentgrass can quickly cover the ground, forming dense turf that is resilient to frequent mowing. It is suitable for high-quality and high-intensity turfgrass planting in venues such as golf courses and sports fields. It is also widely used in conventional urban areas, courtyards, parks, and highway greening projects.
Due to the shallow root system and dense turf texture of creeping bentgrass, it has poor disease resistance and is susceptible to various pathogens [1]. Dollar spot, brown patch, bacterial yellowing, rust, and other diseases are the most common diseases affecting creeping bentgrass worldwide. These diseases tend to occur in hot and humid environments and often lead to significant degradation in turf quality, esthetics, and greening functions, resulting in substantial losses in turfgrass production and management.
On the other hand, creeping bentgrass is not tolerant to high temperatures. When the temperature exceeds 30 °C, it disrupts the physiological metabolism of the turfgrass, leading to a decline in its apparent quality and increased susceptibility to diseases [2]. The turfgrass may enter a period of dormancy, turn yellow, or even die, thereby affecting its visual appeal and performance for recreational activities. Typically, plants respond to non-biological stressors through morphological adaptations, maintaining hormone homeostasis, and increasing biosynthesis rates [3]. There are complex cross-reactions among different plant hormones and reactive oxygen species under non-biological stress, with both inhibitory and stimulatory effects on each other, and their changes are not consistent [4]. Exogenous substances can regulate the hormone metabolism of turfgrass and the expression of downstream genes, altering its physiological pathways, thereby delaying aging, improving stress tolerance, and enhancing turfgrass quality [5,6].
Creeping bentgrass has a moderately sized genome (2n = 4x = 28, 2.7 Gb) and is easy to genetically transform [7], making it an ideal model system for studying disease resistance and stress tolerance in grass plants. Currently, a method combining Agrobacterium-mediated transformation and thiophosphate screening has enabled the large-scale production of single-copy transgenic plants in creeping bentgrass, achieving stable inheritance of high-proportion single-copy insertions. This holds significant potential for the improvement of resistance in turfgrass species [8]. Based on recent research on stress biology of creeping bentgrass, this article introduces the main symptoms of diseases, stressors, and corresponding control measures, as well as potential molecular mechanism controlling the resistance of creeping bentgrass to these biotic and abiotic stresses, aiming to provide effective recommendations for disease resistance and stress tolerance in creeping bentgrass.

2. Research on Disease Resistance of Creeping Bentgrass

2.1. Dollar Spot Disease

Dollar spot disease, caused by Clarireedia spp., is one of the most important diseases affecting creeping bentgrass [9]. It occurs severely in countries such as Norway, Spain, Argentina, Sweden, and the United States. The first report of dollar spot disease in China was in the late 1990s, mainly in southern China. In late May 2009, China officially reported the occurrence of dollar spot disease in creeping bentgrass [10]. The symptoms of this disease include sunken, straw-colored/bleached patches with red/brown margins (Figure 1). Infected patches later merge into larger ones. On golf courses, irregular and sunken dead turfgrass reduces the esthetic value of the course, affects ball rolling, and has a negative impact on playability [11].
One strategy for controlling dollar spot is the use of tolerant cultivars, which typically take longer to develop symptoms and have smaller lesion centers compared to more susceptible cultivars. Based on the observed continuous distribution of phenotypes and super-progeny segregation in genetic population from contrasted hybridization, it is believed that the resistance to dollar spot disease in creeping bentgrass is controlled by quantitative genetics [12]. Major-effect QTL markers can be directly utilized in molecular breeding, significantly enhancing the efficiency of disease-resistant cultivar development and providing a genetic foundation for reducing pesticide dependency. Chakraborty et al. first identified a major-effect QTL for resistance to leaf spot disease (located on linkage group 7.1) in creeping bentgrass. The associated marker, 3.AW10.650, demonstrated stable phenotypic variance explanation ranging from 14% to 36% across multiple environments, with a heritability of 0.88. Additionally, several environment-specific, minor-effect QTLs were detected [13]. Newly released cultivars such as Declaration, Kingpin, Benchmark DSR, 007, and experimental selections including 13M, HTM, and HTL developed through an intensive dollar spot breeding program typically sustain less disease than cultivars not intentionally selected for dollar spot resistance [14].
Fungicide is the main measure used to prevent and control the dollar spot of creeping bentgrass (Table 1). The mitigation of dollar spot can be achieved through the removal of morning dew and the reduction in leaf dampness duration. Daily removal of dew, coupled with an increase in lawn mowing frequency under conditions of elevated dew coverage, prolongs the efficacy of fungicide application for controlling dollar spot [15,16]. Green et al. simulated the method of combining sand topdressing and rolling on the golf course, and the results showed that this method could reduce the incidence of dollar spot disease by 50% at the highest, which could reduce the use of fungicides [17]. Oztur et al. showed through greenhouse and field experiments that the use of soil conditioners would not be a recommended practice for dollar spot when disease pressure is high but rolling could be included as a management practice to suppress dollar spot [18].
Hsiang et al., through many laboratory and field experiments, concluded that applying ferrous sulfate (21% a.i.) used at 250 g per 100 m2 or ferric sulfate (84.5% a.i.) used at 300 g per 100 m2 applied in 10 L of water per 100 m2 on a weekly basis can enable the inhibition of dollar spot on creeping bentgrass during low-to-moderate disease pressure, which is equivalent to standard fungicide control and the toxicity can subside by itself [19]. Miller et al. showed that the application of paclobutrazol with fungicide could reduce the severity of dollar spot. Short-term phytotoxicity (bronze discoloration) was observed in plots treated with triadimefon or paclobutrazol with fungicide [20]. Kaminski et al. applied a single dose of 9.2 kg a.i. per ha chlorothalonil and three doses of 2.4 kg a.i. per ha triadimenol from May to September to mitigate the impact of leaf spot disease on creeping bentgrass [52]. Fidanza et al. demonstrated through field trials that the combined use of fungicides (such as propiconazole, chlorothalonil, and azoxystrobin) and plant growth regulators (PGRs) like paclobutrazol, anti-lodging agents, or their combinations resulted in superior disease control in creeping bentgrass during the late growth season [53].
Significant studies have been made in the exploration and identification of biological control agents (BCAs) for the management of dollar spot disease. Marvin et al. evaluated BCAs and synthetic fungicides at reduced rates for their efficacy controlling dollar spot. The results show that the combination of Bacillus licheniformis and azoxystrobin + propiconazole can maintain adequate dollar spot control and visual turfgrass quality ratings [21]. In greenhouse experiments, Patrick et al. have successfully demonstrated the efficacy of the fungal protein Efe-AfpA, which is produced during the infection of creeping bentgrass florets by Epichloë festucae, in alleviating the severe symptoms caused by dollar spot. This protein shows great potential as a viable alternative or complementary approach to fungicides for managing the specific disease affecting creeping bentgrass [54]. Pan et al. found that glucosinolates, a secondary compound of mustard seed meal, can be converted into fungicidal isothiocyanates in humid environment. The field test results showed that mustard seed meal completely inhibited the mycelial growth of S. homoeocarpa at a high rate, and the application of mustard seed meal in the control of dollar spot can greatly reduce the dependence on fungicides [22]. Lu et al. conducted a study to investigate the changes in transcriptional and metabolic responses in creeping bentgrass following colonization by Trichoderma virens, with the aim of enhancing the grass’s resistance to dollar spot disease [24]. Duraisamy et al. evaluated the disease control efficacy of a combination of stereoisomers of a bacterial volatile compound, 2,3-butanediol (BDO), which was found to induce plant resistance, and commercial fungicides against turfgrass fungal diseases in both growth room and fields [55]. Results showed that 2,3-BDO significantly increased the disease control efficacy against dollar spot and summer patch disease, thereby reducing the use of chemical fungicides.
Fertilization is also intensively associated with disease resistance of creeping bentgrass to dollar spot. Jiang et al. concluded that calcium fertilizer could significantly increase the root-shoot ratio, thus enhancing the tolerance of creeping bentgrass to dollar spot [25]. Townsend et al. conducted a field experiment, and the results showed that higher nitrogen application rate could reduce the severity of dollar spot disease, and the economic loss could be reduced by controlling the amount of nitrogen fertilizer, but the amount of nitrogen fertilizer needed to control the disease was too large, so it was unrealistic to control dollar spot disease by nitrogen fertilizer at present [26].

2.2. Brown Patch

Brown patch is a leaf disease of cool-season turfgrass, which is caused by Rhizoctonia solani and usually occurs in warm and humid weather [27]. The standard symptom is patches with brown or tan color on the leaves (Figure 2). The damage caused by the outbreak of brown patch reduces the esthetic value of amenity turf. In the environment of golf course, the thinned damaged turf area will destroy the ball lie and roll characteristics, thus negatively affecting the playability [56]. Practice shows that measures such as regulating fertility, limiting leaf humidity, selecting less sensitive varieties and applying fungicides prophylactically will affect the severity of brown patch [57].
Peacock et al. determined that air flow generated by fans can reduce the incidence of brown patch by changing the micro-environment of the canopy surface, reducing canopy temperature and leaf wetting duration, and improving lawn quality [28]. Liu et al. showed that the 2,3-butanediol can induce resistance of creeping bentgrass to brown patch and change the cell structure. The mesophyll cell size and chloroplast number of upper and lower epidermal cells of leaves are positively correlated with the resistance [1]. King et al. studied the inhibitory effect of tobacco phylloplanins on brown patch of creeping bentgrass in vitro (hyphal extension) and in vivo. The results showed that the symptom remission rates of T- and S-phylloplanins on brown patch of creeping bentgrass were 94% and 100%, respectively, which could be used as exogenous or endogenous antifungal agents to protect creeping bentgrass [29]. Coelho et al. showed that antagonistic microorganism Trichoderma atroviride produced by organic compost from agricultural-industrial wastes had a good inhibitory effect on Rhizoctonia solani as a potential biological control microorganism in lawn management [30].
In controlled environment repeated in vitro and in vivo experiments, Penaeidin4-1 transgenic plants exhibited significantly enhanced resistance against both brown patch and dollar spot disease in creeping bentgrass [31]. Cho et al. introduced pepper esterase (PepEST) gene into creeping bentgrass by Agrobacterium-mediated transformation, and purified recombinant PepEST proteins could inhibit the growth of R. solani and S. homoeocarpa [32].

2.3. Bacterial Etiolation

Bacterial etiolation of creeping bentgrass was first discovered in 2009. The disease is caused by Acidovorax avenae subsp. [33], and may also be caused by other bacteria, such as Xanthomonas translucens and Pantoea ananatis [34,35]. When the temperature exceeds the optimum temperature for the growth of creeping bentgrass (30~40 °C), bacterial etiolation is easy to occur [36]. The visual symptom of this disease is initially a small piece (30 cm) on the turf, which seems to have changed color and can quickly spread to the whole green, fairway or other turf areas of golf courses. Leaf tip necrosis, wilting, chlorosis, and stem etiolation are easy to observe after infection, which reduces the appearance and function of turf and causes serious damage to creeping bentgrass, especially on the green of golf course [37]. Physiological symptoms of plants include increased electrolyte leakage from leaves and roots, decreased chlorophyll content and decreased root activity, and there are no known anti-bacterial varieties. In addition, there is no known management strategy to prevent or reduce disease symptoms of bacterial etiolation [38].
The accumulation of different gibberellic acid (GA) subtypes produced by A. avenae may lead to the severity of the disease increasing [39]. The contents of two GA isoforms (GA1 and GA4), salicylic acid (SA) and abscisic acid (ABA) in A. avenae-infected tissue were higher than those in normal tissue, while indole-3-acetic acid (IAA) content was lower than that in normal tissue [40]. Liu et al. tested the prevention and control effects of pretreatment of creeping bentgrass with jasmonic acid (JA) and SA on bacterial etiolation through hydroponic growth chamber research [41]. The results showed that at the optimum temperature, spraying either JA or SA reduced the bacterial etiolation symptoms.
Roberts et al. conducted a series of studies to evaluate the efficacy of chemical reagents in controlling bacterial etiolation in creeping bentgrass. Their findings showed that the application of oxytetracycline and acibenzolar-S-methyl plus chlorothalonil (ASM+C) effectively maintained lawn quality while reducing bacterial etiolation over multiple years [34]. In contrast, treatment with biostimulants did not have a significant impact on etiolation caused by either A. avenae or X. translucens. However, the use of trinexapac-ethyl (TE) reduced etiolation caused by X. translucens but increased etiolation caused by A. avenae [42].

2.4. Microdochium Patch

Microdochium patch, also called pink snow mold, is caused by the fungus Microdochium nivale and is a major disease in most cool-season turfgrass species [11]. When it is in cold and humid weather for a long time, the damaged lawn will appear circular patches [43]. If there is no snow, the lesion starts as a small water-stained plaque with a diameter less than 5 cm, then immediately turns orange-brown to black-red-brown, and finally turns light-gray or brown. Because the spores are scattered with the lawn mower, the smaller red spots may be linearly distributed. The lesions will expand immediately, but their size will always be limited to less than 20 cm in diameter. The annular lesions will occur on the low-mowed lawn, and the outer ring of the lesions will have a waterlogged gray-black edge. Covered with snow or in a very humid area, thin fluffy white mycelium will appear on the gray leaves. When the snow melts, the lesion formed by the damaged leaves turns brown or bleached white, and the outer edge of the lesion may turn pink, and the mycelium is white, but a large number of pink molds will be produced under sunlight [11].
Significant efforts have been dedicated to the chemical and biological control of microdochium patch disease. Dempsey et al. assessed the initial defense responses of turfgrasses infected with M. nivale to determine the effects of phosphite treatment on these responses and symptom inhibition. Phosphite treatment led to increases in the total phenol and hydrogen peroxide contents, and when it was applied to greenhouse plants in sequence or alone, it led to a significant decrease in the symptoms of microdochium patch [44]. Stone K showed that ferric sulfate had inhibitory effect on M. nivale, but the inhibitory effect was inconsistent in three field experiments. When the concentration of ferric sulfate was too high, the creeping bentgrass would turn black as phytotoxicity [45].
Stricker et al. showed that the resistance activator Civitas + Harmonizer had inhibitory effect on M. nivale at 400 ppm and 800 ppm of CO2 [46]. Aamlid et al. tested the control effect of biological agents Gliocladium catenulatum and Streptomyces spp. on M. nivale, and the results showed that low temperature might reduce the efficacy of G. catenulatum. Because M. nivale is active in the cool and humid period of the growing season, G. catenulatum may be able to alleviate the disease stress in summer and early autumn. However, Streptomyces spp. may be able to reduce disease stress in growing season and low temperature in late autumn [58].

3. Research on Abiotic Stress Tolerance of Creeping Bentgrass

3.1. Heat Stress

Under high temperature stress, many cool-season turfgrasses, especially creeping bentgrass with low cutting height, will suffer from growth inhibition, leaf senescence, shoot and root death, etc. Heat stress injury may be related to many physiological factors [47]. Elevated temperatures induce thermal instability in photosystem II (PSII), leading to compromised photosynthetic efficiency. Under heat stress, creeping bentgrass exhibits leaf curling, impaired root development, and reduced overall growth rates. Additionally, heat-triggered accumulation of reactive oxygen species (ROS) results in membrane lipid peroxidation and compromised plasma membrane integrity [59,60].
During heat stress, a high carbohydrate utilization rate, especially glucose and sucrose, is an important physiological characteristic of creeping bentgrass related to heat stress tolerance [48]. Larkindale et al. studied the changes in membrane lipid composition and saturation level in leaves and roots during high-temperature acclimation and heat stress. The results showed that there may be some relationship between the saturation of membrane lipid in leaves before heat stress and the ability of plants to limit heat-induced damage during stress. The lipid composition or saturation of roots may be an important factor to control plant heat tolerance [49].
Heat stress injury may be related to the inhibition of root cytokinin biosynthesis. Exogenous application of zeatin riboside (ZR) improved the negative effects of heat stress, which showed that it inhibited or delayed leaf senescence of creeping bentgrass. Cytokinin may be helpful to alleviate heat stress injury, possibly by slowing down the action of protease and inducing or up-regulating genes encoding heat shock protein [51]. Liu et al. studied whether the application of synthetic cytokinin ZR in root zone could improve the tolerance of creeping bentgrass to heat stress. The results showed that the heat stress injury of creeping bentgrass could be reduced by applying 1 or 10 μmol ZR in root zone [61].
Other chemical reagents have also been screened for their ability to induce resistance to heat stress in creeping bentgrass. McCann et al. demonstrated that foliar application of the plant growth regulator trinexapac-ethyl (TE) as a pretreatment in creeping bentgrass confers robust resilience to combined heat-drought stress. TE significantly enhanced turf quality (sustained ratings of 6.5~7.0) while stabilizing leaf relative water content (85~90% vs. 50% in controls) and photosynthetic efficiency [62]. Foliar application of orthosilicic acid (0.32 mL/m2) also enhances creeping bentgrass thermodrought tolerance through coordinated physiological modulation [63]. In addition, the Ascophyllum nodosum-derived biostimulant Utilize® (58 μL/m2 biweekly foliar application) enhances creeping bentgrass thermodrought resilience through coordinated nitrogen metabolism potentiation [64]. In addition, exogenous application of cysteine, serine, and aspartic acid protease inhibitors demonstrated significant mitigation of heat stress-induced foliar senescence in creeping bentgrass under prolonged thermal exposure (35 °C/30 °C day/night cycle for 35 days) [65].
Xu et al. elucidated shared molecular mechanisms in creeping bentgrass under combined heat and drought stress through RNA sequencing. A cohort of 1482 co-regulated genes (670 up-regulated/812 down-regulated) was identified during the 21-day stress exposure. Up-regulated transcripts predominantly mediated oxylipin biosynthesis (antioxidant defense) and proline metabolism (osmoregulation), while down-regulated genes were enriched in thiamine metabolism and photosynthetic apparatus organization [66]. The thermo-tolerance of cool-season turfgrass is governed by a synergistic multi-pathway regulatory framework. Heat shock proteins (HSPs) and transcription factors (HSFs) collectively maintain cellular homeostasis through protein stabilization and degradation retardation. Antioxidant enzymes (SOD/CAT/APX) efficiently scavenge ROS, while photosynthetic regulators (RCAβ/ATPα) and chlorophyll metabolism genes (NYC1/SGR) safeguard carbon metabolic equilibrium. Genomic stability is preserved via cell cycle regulators (SCF/CDC6) and DNA-binding proteins (HMGB7), concurrently with membrane integrity enhancement through lipid metabolism genes (FAD/LOX) that modulate membrane lipid composition. Secondary metabolism pathways (PAL/CYP) reinforce antioxidative defenses via phenolic compound biosynthesis, establishing an integrated molecular network orchestrating heat stress adaptation [67].
A series of studies have been conducted on the genetic improvement of creeping bentgrass for tolerance to heat stress. Li et al. cloned the SUMO E3 ligase gene OsSIZ1 from rice and transformed it into creeping bentgrass. They found that its overexpression significantly enhanced plant resistance to drought, heat, and low-phosphorus stress. The transgenic plants regulated the expression of heat shock proteins (such as ApHSP26.8) and phosphorus uptake-related pathways by increasing SUMO modification levels [68]. Li et al. demonstrated that ectopic expression of cyanobacterial Flavodoxin (Fld) in creeping bentgrass profoundly alters its developmental architecture (manifested as increased tillering coupled with reduced biomass) while conferring multistress tolerance to oxidative, drought, thermal, and nitrogen deprivation challenges. Mechanistic analyses revealed Fld’s broad-spectrum stress resilience is achieved through coordinated enhancement of cellular membrane integrity, modulation of heat shock protein dynamics, maintenance of thioredoxin redox homeostasis, and activation of nitrogen transport/assimilation pathways (NRT/NiR), thereby establishing a comprehensive stress-adaptation framework [69]. Zhao et al. developed a multi-resistance transgenic creeping bentgrass by combining the Arabidopsis vacuolar pyrophosphatase gene AVP1, rice SUMO E3 ligase gene OsSIZ1, and the cyanobacterium flavodoxin gene Fld. Under normal conditions, the plants exhibited a 45% increase in biomass, while simultaneously acquiring resistance to salt (sodium compartmentalization), drought (osmotic regulation), heat (membrane stability), and nutrient stress. Mechanistically, the three genes enhanced ion transport, protein SUMOylation, and photosynthetic electron transport, which collectively activated 6034 differentially expressed genes, thereby reconstructing networks for antioxidant defense, nutrient transport, and stress signaling [70].
Family members of small heat shock proteins have shown great potential in protecting creeping bentgrass from heat stress. Sun et al. constructed transgenic Arabidopsis thaliana overexpressing creeping bentgrass small heat shock protein AsHSP17 and found that this protein significantly reduced plant tolerance to high-temperature and salt stress. Molecular mechanism analysis revealed that AsHSP17 operates through dual pathways: on one hand, it suppresses the expression of photosynthesis-related genes such as PSAF and RCA, and on the other, it modulates the ABA signaling pathway—down-regulating the key ABA biosynthesis gene NCED3 and ABA-responsive genes like ABI4, while up-regulating the catabolic gene CYP707A3 [60]. Another gene encoding a small heat shock protein, AsHSP26.8a, in creeping bentgrass negatively regulates the plant’s resistance to multiple stresses by integrating ABA signaling, heat shock transcription factors (HSFB2a/HSFC1), and calcium signaling networks. Transgenic Arabidopsis experiments confirmed that overexpression of this gene significantly reduced tolerance to heat (40 °C), salt (125~150 mM), and ABA stress [59].

3.2. Drought Stress

In summer season, in warm, arid or semi-arid areas, drought and thermal stress often occur simultaneously. The combined stress of drought and high temperature is harmful to turfgrass, especially the cool-season turfgrass. Drought stress induces progressive foliar desiccation in creeping bentgrass, marked by diminished relative water content (RWC) and loss of cellular turgor pressure, culminating in plant wilting. Concurrent stomatal closure restricts CO2 assimilation, thereby suppressing photosynthetic efficiency and disrupting carbon metabolic flux [70,71,72]. Therefore, it is crucial to understand the mechanisms that enhance plant tolerance to summer stress and to develop corresponding management strategies [62].
In various practical studies, several chemical reagents have been discovered to enhance the tolerance of creeping bentgrass to drought stress. The exogenous application of γ-Aminobutyric acid (GABA) effectively mitigated water stress damage in creeping bentgrass by reducing oxidative damage, photoinhibition, and the loss of water and chlorophyll. [73,74]. Exogenous glycine betaine (GB) pretreatment significantly alleviates drought-induced physiological impairment in creeping bentgrass. Mechanistic analyses indicate that GB mitigates oxidative damage by reducing the accumulation of reactive oxygen species (ROS) and malondialdehyde (MDA), while simultaneously enhancing the activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) [75]. The exogenous application of spermidine (Spm) also mitigates growth inhibition, photosynthetic impairment, and oxidative damage caused by water deficit and heat stress in creeping bentgrass by stimulating the activation of endogenous polyamine biosynthesis. [76]. In creeping bentgrass experiencing drought stress, treatments with seaweed extract (SWE) and humic acid (HA) significantly increased leaf water content, biomass, and α-tocopherol concentrations [77]. The ACC deaminase-producing rhizobacterium Paraburkholderia aspalathi “WSF23” confers significant drought resilience and post-stress recuperative capacity in creeping bentgrass. Experimental validation demonstrates that bacterized plants sustained superior turf quality and root growth throughout a 35-day drought, exhibiting accelerated recovery after a 15-day rehydration period. Metabolomic profiling reveals microbial mediation via drought resistance mechanisms—primarily through the activation of osmoregulatory, antioxidant, and nitrogen assimilatory pathways in foliar and root tissues [78].
Xu et al. conducted comparative proteomic analysis of drought-sensitive (‘Penncross’) and drought-tolerant (‘Penn-A4’) creeping bentgrass genotypes under PEG-induced osmotic stress. Both cultivars exhibited coordinated suppression of carbon/nitrogen metabolic proteins. The tolerant genotype uniquely upregulated β-glucan exohydrolase and actin, facilitating cell wall remodeling and cytoskeletal integrity preservation. Antioxidant defense proteins—particularly ascorbate peroxidase and glutathione transferase—accumulated preferentially in Penn-A4, while molecular chaperones (HSC70 and co-chaperonin CPN20) maintained elevated levels compared to Penncross [79].
In the genetic modification of creeping bentgrass to enhance its tolerance to drought stress, Fu et al. introduced the barley LEA3 gene into the creeping bentgrass genome. They observed that the transgenic plants exhibited a significantly reduced degree of wilting [71]. Chen et al. constructed creeping bentgrass microRNA169 (miR169) overexpression and knockdown transgenic plants. They found miR169 establishes an equilibrium network for growth and stress responses by targeting NFYA transcription factor family members (e.g., AsNFYA2/3/5) [80]. Sun et al. revealed the regulatory roles of chloroplast small heat shock protein AsHSP26.8 in creeping bentgrass. Stress analyses showed its bidirectional regulatory effects: it increased sensitivity to heat (40 °C) and salt (250 mM NaCl) stress, leading to ROS accumulation and ion imbalance, and enhanced drought tolerance by activating the ABA/DREB pathways. Molecular mechanism studies indicated that this protein is involved in reprogramming the HSP family gene network and regulating key transcription factors such as HSFA2 [72]. Tan et al. showed that overexpression of AsAFL1 in creeping bentgrass significantly enhanced drought tolerance, comparative transcriptomics analysis and weighted correlation network analysis (WGCNA) indicating the drought resistance mediated by AsAFL1 is related to the transcriptional regulation of genes involved in the biosynthesis and signaling of plant hormones (abscisic acid, auxin, and gibberellin), redox balance, the synthesis of secondary metabolites (lignin, cutin, suberin, and wax), and the transport and mobilization of nutrients [81].
Aswath et al. used transgenic engineering to introduce the cowpea-derived VuNCED1 gene into creeping bentgrass. The transgenic lines showed remarkable stress resilience, with survival rates over 50% after 10 weeks of hypersaline (10 dS/m) and drought (75% water restriction) conditions, while wild-type specimens died [82]. Overexpression of the isopentenyltransferase (IPT) gene also confers drought resilience in creeping bentgrass via transcriptional reprogramming mediated by the bHLH148/MYB4/WRKY transcription factor triad [83].

3.3. Saline-Alkali Stress

Saline-alkali soil is an important reserve land resource. Salinity stress disrupts ionic homeostasis in creeping bentgrass by causing excessive accumulation of Na+ and efflux of K+, thereby impairing root hydraulic conductance and suppressing chlorophyll biosynthesis.
Several microRNAs have been shown to be involved in creeping bentgrass resistance to saline-alkali stress. Transgenic plants overexpressing microRNA319 (miR319) enhance their salt tolerance through the salt exclusion mechanism. The leaves of Osa-miR319a transgenic plants exhibit increased thickness, leaf weight per unit area, and wax content, which is likely to contribute to the reduction in water loss and enhance the plant’s resistance to drought stress. Furthermore, under salt stress conditions, Osa-miR319a transgenic plants demonstrate significantly lower sodium uptake compared to the wild-type control [84,85]. Additionally, during salt treatment, both transgenic lines maintained significantly higher total chlorophyll content compared to the wild-type control, indicating an improved photosynthetic activity in the transgenic lines, which contributes to enhanced salt stress resistance compared to the wild-type control [86]. miR396 also plays an active role in environmental stress responses by regulating functional and regulatory proteins. The enhanced salt tolerance in transgenic creeping bentgrass may be due to miR396-mediated positive regulation of AsSOS1, suppression of AsHKT1 expression, and reducing Na+ accumulation [87]. Under salt stress, the K+:Na+ ratio significantly increases in miR528 transgenic creeping bentgrass because of an enhanced ability to maintain stable K+ acquisition and distribution, which leads to an enhancement in salt tolerance [88].
Besides miRNAs, Li et al. showed that the transgenic expression of the Arabidopsis vacuolar H+-pyrophosphatase gene AVP1 in creeping bentgrass confers salt tolerance. The engineered lines had enhanced vacuolar proton-pumping activity, which increased Na+/H+ antiport efficiency, leading to compartmentalized Na+ accumulation in roots and leaves while maintaining preferential acquisition of K+, Cl−, and phosphorus [89]. Furthermore, Zhao et al. have simultaneously introduced AVP1, OsSIZ1 and Fld in creeping bentgrass, transgenic (TG) plants overexpressing these three genes performed significantly better than wild type controls indicating that multiple stress-resistant genes can work together to enhance plant resistance [69]. A similar strategy can be extended for the use of other beneficial genes in various crop species for trait modifications, enhancing agricultural production.

3.4. Heavy Metal Stress

Heavy metals are a type of potentially harmful pollutant in the soil environment. They can generate excessive ROS either directly or indirectly, causing oxidative stress in plants. This stress leads to lipid peroxidation of cell membranes and oxidative damage to proteins, pigments, enzymes, nucleic acids, and other cellular components in grass species [90]. Gladkov et al. evaluated creeping bentgrass’ sensitivity to cadmium, copper, zinc, and lead in soil. Data showed second generation seeds kept tolerance to these factors, and cross resistance to heavy metals was seen in some cases [91].
Yuan et al. identified key molecular responses of creeping bentgrass to cadmium stress. Mitogen-activated protein kinase kinase kinase 12 (MAPKKK12) had increased expression at both low and high cadmium concentrations, showing its vital role in activating cadmium tolerance [92]. Transgenic creeping bentgrass expressing S599A-PhyA showed remarkable resilience under 20 mM ZnCl2 heavy metal stress. These improvements were accompanied by increased antioxidant enzyme activities (ascorbate peroxidase, catalase, superoxide dismutase, glutathione reductase), better shoot/root biomass allocation, and stable photochemical efficiency (Fv/Fm) [93].
In summary, when faced with abiotic stresses, A. stolonifera triggers a complex set of adaptive responses (Figure 3). Key regulatory nodes governing tolerance to abiotic stresses in A. stolonifera have been identified, including heat shock proteins HSP17 and HSP26.8, as well as the microRNA miR396, which share interconnected downstream regulatory networks.

4. Final Considerations and Future Research

This review systematically investigated the disease resistance mechanisms and abiotic stress tolerance strategies in creeping bentgrass, providing novel insights into molecular breeding and integrated turf management. Creeping bentgrass employs multiple systems against biotic and abiotic stresses through genetic, physiological, and agronomic adaptations, which collectively contribute to its ecological resilience in diverse environments.
While this summary advances understanding of creeping bentgrass stress responses, three critical limitations must be addressed: (1) Most molecular findings derive from controlled environments, necessitating field validation under real-world stress combinations. (2) The economic viability of biological control agents (BCAs) in large-scale turf systems remains unproven. (3) Epigenetic regulation and microbiome interactions are largely unexplored dimensions.
The future directions of research on creeping bentgrass disease and stress resistance are highly diverse, covering various aspects such as precise molecular breeding and sustainable field management. Firstly, a precise biotechnology approach can be adopted. This is the most groundbreaking direction at present, aiming to “customize” the grass for precise disease resistance. Secondly, the immune system can be utilized to regulate resistance and tolerance. Besides directly modifying genes, “training” the plants immune system to acquire greater resistance is also an efficient and environmentally friendly strategy, including inducing systemic resistance and studying signaling pathways, etc. Furthermore, comprehensive multi-attribute collaborative breeding is required, including disease resistance, nutritional enhancement, and tolerance to non-biological stress. Finally, it is important to focus on technological integration and sustainable development, seamlessly connecting cutting-edge technologies with practical applications. The main task is to establish an integrated disease management (IDM) system. In the future, it is necessary to integrate measures such as disease-resistant varieties, agricultural management techniques, biological control, and precise chemical control to create an efficient, environmentally friendly, and sustainable disease management plan.
Future research would prioritize the following: (1) Development of multi-trait selection indices incorporating disease resistance and abiotic stress tolerance. (2) Establishment of nanoparticle delivery systems for precision stress mitigation. (3) Investigation of stress memory effects through multi-generational omics analysis. (4) The integration of machine learning for stress phenotyping could accelerate the breeding cycle, particularly for complex traits.

5. Conclusions

Creeping bentgrass remains a cornerstone cool-season turfgrass in landscaping and sports field applications due to its functional and esthetic value. However, its vulnerability to biotic stressors, including dollar spot, brown patch, and bacterial yellowing, and abiotic challenges such as high temperature, drought, and salinity significantly compromises turf quality, visual appeal, and ecological functions, imposing substantial economic and management costs. Paradoxically, these agronomic challenges are precisely what cement its status as a model system for grass biology. Its moderately sized genome and facile genetic transformation capabilities position it as an exemplary model system for elucidating grass stress biology, offering unique advantages for dissecting molecular mechanisms underlying disease resistance and stress tolerance. This review underscores the necessity of integrating multi-omics approaches, molecular breeding, genome editing technologies, and physiological-biochemical analyses to advance our understanding of creeping bentgrass resilience. Future research should prioritize identifying key regulatory genes, pathways, and biomarkers associated with stress adaptation, while exploring practical breeding strategies to develop cultivars with enhanced durability. Prioritizing the identification and validation of master regulatory genes will accelerate the development of novel cultivars with enhanced durability. Such efforts will not only elevate turfgrass management practices but also contribute to sustainable urban greening and agricultural ecosystems, bridging fundamental biological insights with applied agronomic solutions.

Author Contributions

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

Funding

This work was supported by the National Key Research and Development Program of China (2023YFD1201000), the National Natural Science Foundation of China (32471755 and 32502420), the Major Science and Technology Support Program of Hebei (252N6501D), the Key Research and Development Project of Shijiazhuang City for University in Hebei Province (241490012A), the Local Science and Technology Development Fund Projects Guided by the Central Government (236Z6302G), the State Key Laboratory of North China Crop Improvement and Regulation (NCCIR2021ZZ-17), and S&T Program of Hebei (23567601H).

Data Availability Statement

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

Acknowledgments

During the preparation of this manuscript/study, the authors used Wenxin 4.5 Turbo AI tool for the purposes of grammar checking and language editing. The authors have reviewed and edited the output and take full responsibility for the content of this publication.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Liu, N.; Lin, S.; Huang, B. Differential effects of glycine betaine and spermidine on osmotic adjustment and antioxidant defense contributing to improved drought tolerance in creeping bentgrass. J. Am. Soc. Hortic. Sci. 2017, 142, 20–26. [Google Scholar] [CrossRef]
  2. DiPaola, J.; Beard, J. Physiological effects of temperature stress. Turfgrass 1992, 32, 231–267. [Google Scholar]
  3. Bita, C.E.; Gerats, T. Plant tolerance to high temperature in a changing environment: Scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci. 2013, 4, 273. [Google Scholar] [CrossRef] [PubMed]
  4. Xia, X.-J.; Zhou, Y.-H.; Shi, K.; Zhou, J.; Foyer, C.H.; Yu, J.-Q. Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J. Exp. Bot. 2015, 66, 2839–2856. [Google Scholar] [CrossRef] [PubMed]
  5. Jespersen, D.; Yu, J.; Huang, B. Metabolite responses to exogenous application of nitrogen, cytokinin, and ethylene inhibitors in relation to heat-induced senescence in creeping bentgrass. PLoS ONE 2015, 10, e0123744. [Google Scholar] [CrossRef]
  6. Li, Z.; Zhou, H.; Peng, Y.; Zhang, X.; Ma, X.; Huang, L.; Yan, Y. Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul. 2015, 76, 71–82. [Google Scholar] [CrossRef]
  7. Yu, T.; Skinner, D.; Liang, G.; Trick, H.; Huang, B.; Muthukrishnan, S. Agrobacterium-mediated transformation of creeping bentgrass using GFP as a reporter gene. Hereditas 2001, 133, 223–229. [Google Scholar] [CrossRef]
  8. Luo, H.; Hu, Q.; Nelson, K.; Longo, C.; Kausch, A.; Chandlee, J.; Wipff, J.; Fricker, C. Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Rep. 2004, 22, 645–652. [Google Scholar] [CrossRef]
  9. Bonos, S.A.; Casler, M.D.; Meyer, W.A. Plant responses and characteristics associated with dollar spot resistance in creeping bentgrass. Crop Sci. 2004, 44, 1763–1769. [Google Scholar] [CrossRef]
  10. Lv, C.; Hsiang, T.; Li, J.; Luo, L. First report of dollar spot of Agrostis stolonifera, Poa pratensis, Festuca arundinacea and Zoysia japonica caused by Sclerotinia homoeocarpa in China. New Dis. Rep. 2011, 23, 2044-0588. [Google Scholar] [CrossRef]
  11. Vargas, J.M. Management of Turfgrass Diseases; Routledge: Abingdon-on-Thames, UK, 2018. [Google Scholar]
  12. Bonos, S.A. Gene action of dollar spot resistance in creeping bentgrass. J. Phytopathol. 2011, 159, 12–18. [Google Scholar] [CrossRef]
  13. Chakraborty, N.; Curley, J.; Warnke, S.; Casler, M.; Jung, G. Mapping QTL for dollar spot resistance in creeping bentgrass (Agrostis stolonifera L.). Theor. Appl. Genet. 2006, 113, 1421–1435. [Google Scholar] [CrossRef] [PubMed][Green Version]
  14. Bonos, S.A.; Clarke, B.B.; Meyer, W.A. Breeding for disease resistance in the major cool-season turfgrasses. Annu. Rev. Phytopathol. 2006, 44, 213–234. [Google Scholar] [CrossRef] [PubMed]
  15. Williams, D.; Powell, A.; Vincelli, P.; Dougherty, C. Dollar spot on bentgrass influenced by displacement of leaf surface moisture, nitrogen, and clipping removal. Crop Sci. 1996, 36, 1304–1309. [Google Scholar] [CrossRef]
  16. Delvalle, T.C.; Landschoot, P.J.; Kaminski, J.E. Effects of dew removal and mowing frequency on fungicide performance for dollar spot control. Plant Dis. 2011, 95, 1427–1432. [Google Scholar] [CrossRef]
  17. Green, T.O.; Rogers, J.N.; Crum, J.R.; Vargas, J.M.; Nikolai, T.A. Effects of rolling and sand topdressing on dollar spot severity in fairway turfgrass. HortTechnology 2019, 29, 394–401. [Google Scholar] [CrossRef]
  18. Oztur, E.D. Integrated Management of Dollar Spot Disease of Creeping Bentgrass Using Soil Conditioners. Ph.D. Thesis, University of Guelph, Guelph, ON, Canada, 2020. [Google Scholar]
  19. Hsiang, T.; Stone, K.; Rudland, M.; Chen, J. Non-conventional fungicides to control dollar spot disease. Int. Turfgrass Soc. Res. J. 2022, 14, 831–834. [Google Scholar] [CrossRef]
  20. Miller, G. Effect of watered-in demethylation-inhibitor fungicide and paclobutrazol applications on foliar disease severity and turfgrass quality of creeping bentgrass putting greens. Crop Prot. 2016, 79, 64–69. [Google Scholar] [CrossRef]
  21. Marvin, J.W.; Kerr, R.A.; McCarty, L.B.; Bridges, W.; Martin, S.B.; Wells, C.E. Curative evaluation of biological control agents and synthetic fungicides for Clarireedia jacksonii. HortScience 2020, 55, 1622–1625. [Google Scholar] [CrossRef]
  22. Pan, X.; Earlywine, D.T.; Smeda, R.J.; Teuton, T.C.; English, J.T.; Sams, C.E.; Xiong, X. Effect of oriental mustard (Brassica juncea) seed meal for control of dollar spot on creeping bentgrass (Agrostis stolonifera) Turf. Int. Turfgrass Soc. Res. J. 2017, 13, 166–174. [Google Scholar] [CrossRef]
  23. Ünal, F.; Aşkın, A.; Koca, E.; Yıldırır, M. Identification, Genetic Diversity and Biological Control of Dollar Spot Disease Caused by Sclerotinia homoeocarpa on Golf Courses in Turkey. Int. J. Agric. For. Life Sci. 2021, 5, 147–153. [Google Scholar]
  24. Gan, L.; Yin, Y.; Niu, Q.; Yan, X.; Yin, S. New insights into the mechanism of Trichoderma virens-induced developmental effects on Agrostis stolonifera disease resistance against Dollar spot infection. J. Fungi 2022, 8, 1186. [Google Scholar] [CrossRef] [PubMed]
  25. Jiang, M.; Kaluwasha, W.; Xiong, X. Influence of calcium and nitrogen fertilizer on creeping bentgrass infected with dollar spot under cool temperatures. Int. Turfgrass Soc. Res. J. 2022, 14, 931–939. [Google Scholar] [CrossRef]
  26. Townsend, R.; Millican, M.D.; Smith, D.; Nangle, E.; Hockemeyer, K.; Soldat, D.; Koch, P.L. Dollar spot suppression on creeping bentgrass in response to repeated foliar nitrogen applications. Plant Dis. 2021, 105, 276–284. [Google Scholar] [CrossRef]
  27. Fidanza, M.A.; Dernoeden, P.H. Brown patch severity in perennial ryegrass as influenced by irrigation, fungicide, and fertilizers. Crop Sci. 1996, 36, 1631–1638. [Google Scholar] [CrossRef]
  28. Peacock, C.H.; Lyford, P.R. Use of fans and their effects on the turf microenvironment and disease development. Int. Turfgrass Soc. Res. J. 2022, 14, 1088–1091. [Google Scholar] [CrossRef]
  29. King, B.; Williams, D.; Wagner, G. Phylloplanins reduce the severity of gray leaf spot and brown patch diseases on turfgrasses. Crop Sci. 2011, 51, 2829–2839. [Google Scholar] [CrossRef]
  30. Coelho, L.; Reis, M.; Guerrero, C.; Dionísio, L. Use of organic composts to suppress bentgrass diseases in Agrostis stolonifera. Biol. Control 2020, 141, 104154. [Google Scholar] [CrossRef]
  31. Zhou, M.; Hu, Q.; Li, Z.; Li, D.; Chen, C.-F.; Luo, H. Expression of a novel antimicrobial peptide Penaeidin4-1 in creeping bentgrass (Agrostis stolonifera L.) enhances plant fungal disease resistance. PLoS ONE 2011, 6, e24677. [Google Scholar] [CrossRef][Green Version]
  32. Cho, K.C.; Han, Y.J.; Kim, S.J.; Lee, S.S.; Hwang, O.J.; Song, P.S.; Kim, Y.S.; Kim, J.I. Resistance to Rhizoctonia solani AG-2-2 (IIIB) in creeping bentgrass plants transformed with pepper esterase gene PepEST. Plant Pathol. 2011, 60, 631–639. [Google Scholar] [CrossRef]
  33. Giordano, P.; Vargas Jr, J.; Detweiler, A.; Dykema, N.; Yan, L. First report of a bacterial disease on creeping bentgrass (Agrostis stolonifera) caused by Acidovorax spp. in the United States. Plant Dis. 2010, 94, 922. [Google Scholar] [CrossRef]
  34. Roberts, J.A. Investigating the Cause and Developing Management Options to Control Bacterial Etiolation in Creeping Bentgrass Putting Greens; North Carolina State University: Raleigh, NC, USA, 2014. [Google Scholar]
  35. Roberts, J.A.; Ma, B.; Tredway, L.P.; Ritchie, D.F.; Kerns, J.P. Identification and pathogenicity of bacteria associated with etiolation and decline of creeping bentgrass golf course putting greens. Phytopathology 2018, 108, 23–30. [Google Scholar] [CrossRef]
  36. Giordano, P.R. Identification and Characterization of a New Bacterial Disease of Creeping Bentgrass (Agrostis stolonifera L.) Caused by Acidovorax avenea subsp. Avenae; Michigan State University: East Lansing, MI, USA, 2014. [Google Scholar]
  37. Mitkowski, N.; Browning, M.; Basu, C.; Jordan, K.; Jackson, N. Pathogenicity of Xanthomonas translucens from annual bluegrass on golf course putting greens. Plant Dis. 2005, 89, 469–473. [Google Scholar] [CrossRef] [PubMed][Green Version]
  38. Giordano, P.R.; Chaves, A.M.; Mitkowski, N.A.; Vargas, J.M., Jr. Identification, characterization, and distribution of Acidovorax avenae subsp. avenae associated with creeping bentgrass etiolation and decline. Plant Dis. 2012, 96, 1736–1742. [Google Scholar] [CrossRef] [PubMed][Green Version]
  39. Liu, S.; Vargas, J.; Merewitz, E. Phytohormones associated with bacterial etiolation disease in creeping bentgrass. Environ. Exp. Bot. 2017, 133, 35–49. [Google Scholar] [CrossRef]
  40. Liu, S.; Vargas, J.; Merewitz, E. Temperature and hormones associated with bacterial etiolation symptoms of creeping bentgrass and annual bluegrass. J. Plant Growth Regul. 2019, 38, 249–261. [Google Scholar] [CrossRef]
  41. Liu, S.; Vargas, J.; Merewitz, E. Jasmonic and salicylic acid effects on bacterial etiolation and decline disease of creeping bentgrass. Crop Prot. 2018, 109, 9–16. [Google Scholar] [CrossRef]
  42. Roberts, J.A.; Kerns, J.P.; Ritchie, D.F. Bacterial etiolation of creeping bentgrass as influenced by biostimulants and trinexapac-ethyl. Crop Prot. 2015, 72, 119–126. [Google Scholar] [CrossRef]
  43. Dwyer, P.J., Jr.; Horvath, B.; Kravchenko, A.; Vargas, J.M., Jr. Predicting Microdochium patch on creeping bentgrass. Int. Turfgrass Soc. Res. J. 2017, 13, 139–144. [Google Scholar] [CrossRef]
  44. Dempsey, J.J.; Wilson, I.; Spencer-Phillips, P.T.; Arnold, D.L. Phosphite-mediated enhancement of defence responses in Agrostis stolonifera and Poa annua infected by Microdochium nivale. Plant Pathol. 2022, 71, 1486–1495. [Google Scholar] [CrossRef]
  45. Stone, K. Efficacy of Non-Conventional Fungicides for Control of the Plant Pathogens Clarireedia jacksonii and Microdochium nivale. Ph.D. Thesis, University of Guelph, Guelph, ON, Canada, 2019. [Google Scholar]
  46. Stricker, S.; Hsiang, T.; Bertrand, A. Reaction of bentgrass cultivars to a resistance activator and elevated CO2 levels when challenged with Microdochium nivale, the cause of Microdochium Patch. Int. Turfgrass Soc. Res. J. 2017, 13, 229–232. [Google Scholar] [CrossRef]
  47. Liu, X.; Huang, B. Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 2000, 40, 503–510. [Google Scholar] [CrossRef]
  48. Liu, X.; Huang, B. Carbohydrate accumulation in relation to heat stress tolerance in two creeping bentgrass cultivars. J. Am. Soc. Hortic. Sci. 2000, 125, 442–447. [Google Scholar] [CrossRef]
  49. Larkindale, J.; Huang, B. Changes of lipid composition and saturation level in leaves and roots for heat-stressed and heat-acclimated creeping bentgrass (Agrostis stolonifera). Environ. Exp. Bot. 2004, 51, 57–67. [Google Scholar] [CrossRef]
  50. Xu, Q.; Huang, B. Lowering soil temperatures improves creeping bentgrass growth under heat stress. Crop Sci. 2001, 41, 1878–1883. [Google Scholar] [CrossRef]
  51. Veerasamy, M.; He, Y.; Huang, B. Leaf senescence and protein metabolism in creeping bentgrass exposed to heat stress and treated with cytokinins. J. Am. Soc. Hortic. Sci. 2007, 132, 467–472. [Google Scholar] [CrossRef]
  52. Kaminski, J.E.; Dernoeden, P.H. Dead spot severity, pseudothecia development, and overwintering of Ophiosphaerella agrostis in creeping bentgrass. Phytopathology 2006, 96, 248–254. [Google Scholar] [CrossRef]
  53. Fidanza, M.; Wetzel Iii, H.; Agnew, M.; Kaminski, J. Evaluation of fungicide and plant growth regulator tank-mix programmes on dollar spot severity of creeping bentgrass. Crop Prot. 2006, 25, 1032–1038. [Google Scholar] [CrossRef]
  54. Fardella, P.A.; Tian, Z.; Clarke, B.B.; Belanger, F.C. The Epichloë festucae antifungal protein Efe-AfpA protects creeping bentgrass (Agrostis stolonifera) from the plant pathogen Clarireedia jacksonii, the causal agent of dollar spot disease. J. Fungi 2022, 8, 1097. [Google Scholar] [CrossRef]
  55. Duraisamy, K.; Ha, A.; Kim, J.; Park, A.R.; Kim, B.; Song, C.W.; Song, H.; Kim, J.-C. Enhancement of disease control efficacy of chemical fungicides combined with plant resistance inducer 2, 3-butanediol against turfgrass fungal diseases. Plant Pathol. J. 2022, 38, 182. [Google Scholar] [CrossRef]
  56. Settle, D.; Fry, J.; Tisserat, N. Effects of irrigation frequency on brown patch in perennial ryegrass. Int. Turfgrass Soc. Res. J. 2001, 9, 710–714. [Google Scholar]
  57. Smiley, R.W.; Dernoeden, P.; Clarke, B. Compendium of Turfgrass Diseases, 3rd ed.; APS Press: St. Paul, MN, USA, 2005. [Google Scholar]
  58. Aamlid, T.S.; Espevig, T.; Tronsmo, A. Microbiological products for control of microdochium nivale on golf greens. Crop Sci. 2017, 57, 559–566. [Google Scholar] [CrossRef]
  59. Sun, X.; Zhu, J.; Li, X.; Li, Z.; Han, L.; Luo, H. AsHSP26. 8a, a creeping bentgrass small heat shock protein integrates different signaling pathways to modulate plant abiotic stress response. BMC Plant Biol. 2020, 20, 184. [Google Scholar] [CrossRef] [PubMed]
  60. Sun, X.; Sun, C.; Li, Z.; Hu, Q.; Han, L.; Luo, H. AsHSP17, a creeping bentgrass small heat shock protein modulates plant photosynthesis and ABA-dependent and independent signalling to attenuate plant response to abiotic stress. Plant Cell Environ. 2016, 39, 1320–1337. [Google Scholar] [CrossRef]
  61. Liu, X.; Huang, B.; Banowetz, G. Cytokinin effects on creeping bentgrass responses to heat stress: I. Shoot and root growth. Crop Sci. 2002, 42, 457–465. [Google Scholar] [CrossRef]
  62. McCann, S.E.; Huang, B. Effects of trinexapac-ethyl foliar application on creeping bentgrass responses to combined drought and heat stress. Crop Sci. 2007, 47, 2121–2128. [Google Scholar] [CrossRef]
  63. Zhang, X.; Goatley, M.; Wang, K.; Goddard, B.; Harvey, R.; Brown, I.; Kosiarski, K. Silicon Improves Heat and Drought Stress Tolerance Associated with Antioxidant Enzyme Activity and Root Viability in Creeping Bentgrass (Agrostis stolonifera L.). Agronomy 2024, 14, 1176. [Google Scholar] [CrossRef]
  64. Zhang, X.; Taylor, Z.; Goatley, M.; Wang, K.; Brown, I.; Kosiarski, K. Photosynthetic rate and root growth responses to Ascophyllum nodosum extract–based biostimulant in creeping bentgrass under heat and drought Stress. HortScience 2023, 58, 917–921. [Google Scholar] [CrossRef]
  65. Rossi, S.; Huang, B. Protease inhibitors suppressed leaf senescence in creeping bentgrass exposed to heat stress in association with inhibition of protein degradation into free amino acids. Plant Growth Regul. 2024, 102, 65–75. [Google Scholar] [CrossRef]
  66. Xu, Y.; Huang, B. Comparative transcriptomic analysis reveals common molecular factors responsive to heat and drought stress in Agrostis stolonifera. Sci. Rep. 2018, 8, 15181. [Google Scholar] [CrossRef]
  67. Rossi, S.; Huang, B. Research advances in molecular mechanisms regulating heat tolerance in cool-season turfgrasses. Crop Sci. 2025, 65, e21339. [Google Scholar] [CrossRef]
  68. Li, Z.; Hu, Q.; Zhou, M.; Vandenbrink, J.; Li, D.; Menchyk, N.; Reighard, S.; Norris, A.; Liu, H.; Sun, D. Heterologous expression of Os SIZ 1, a rice SUMO E 3 ligase, enhances broad abiotic stress tolerance in transgenic creeping bentgrass. Plant Biotechnol. J. 2013, 11, 432–445. [Google Scholar] [CrossRef] [PubMed]
  69. Li, Z.; Yuan, S.; Jia, H.; Gao, F.; Zhou, M.; Yuan, N.; Wu, P.; Hu, Q.; Sun, D.; Luo, H. Ectopic expression of a cyanobacterial flavodoxin in creeping bentgrass impacts plant development and confers broad abiotic stress tolerance. Plant Biotechnol. J. 2017, 15, 433–446. [Google Scholar] [CrossRef] [PubMed]
  70. Zhao, G.; Liu, Y.; Li, L.; Che, R.; Douglass, M.; Benza, K.; Angove, M.; Luo, K.; Hu, Q.; Chen, X. Gene pyramiding for boosted plant growth and broad abiotic stress tolerance. Plant Biotechnol. J. 2024, 22, 678–697. [Google Scholar] [CrossRef] [PubMed]
  71. Fu, D.; Huang, B.; Xiao, Y.; Muthukrishnan, S.; Liang, G.H. Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Rep. 2007, 26, 467–477. [Google Scholar] [CrossRef]
  72. Sun, X.; Huang, N.; Li, X.; Zhu, J.; Bian, X.; Li, H.; Wang, L.; Hu, Q.; Luo, H. A chloroplast heat shock protein modulates growth and abiotic stress response in creeping bentgrass. Plant Cell Environ. 2021, 44, 1769–1787. [Google Scholar] [CrossRef]
  73. Tang, M.; Li, Z.; Luo, L.; Cheng, B.; Zhang, Y.; Zeng, W.; Peng, Y. Nitric oxide signal, nitrogen metabolism, and water balance affected by γ-aminobutyric acid (GABA) in relation to enhanced tolerance to water stress in creeping bentgrass. Int. J. Mol. Sci. 2020, 21, 7460. [Google Scholar] [CrossRef]
  74. Li, Z.; Tang, M.; Cheng, B.; Han, L. Transcriptional regulation and stress-defensive key genes induced by γ-aminobutyric acid in association with tolerance to water stress in creeping bentgrass. Plant Signal. Behav. 2021, 16, 1858247. [Google Scholar] [CrossRef]
  75. Gan, L.; Zhang, X.; Liu, S.; Yin, S. Mitigating effect of glycinebetaine pretreatment on drought stress responses of creeping bentgrass. HortScience 2018, 53, 1842–1848. [Google Scholar] [CrossRef]
  76. Li, Z.; Cheng, B.; Wu, X.; Zhang, Y.; Feng, G.; Peng, Y. Spermine-mediated metabolic homeostasis improves growth and stress tolerance in creeping bentgrass (Agrostis stolonifera) under water or high-temperature stress. Front. Plant Sci. 2022, 13, 944358. [Google Scholar] [CrossRef]
  77. Zhang, X.; Schmidt, R. Hormone-containing products’ impact on antioxidant status of tall fescue and creeping bentgrass subjected to drought. Crop Sci. 2000, 40, 1344–1349. [Google Scholar] [CrossRef]
  78. Errickson, W.; Huang, B. Rhizobacteria-enhanced drought tolerance and post-drought recovery of creeping bentgrass involving differential modulation of leaf and root metabolism. Physiol. Plant. 2023, 175, e14004. [Google Scholar] [CrossRef]
  79. Xu, C.; Huang, B. Differential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars differing in stress tolerance. J. Plant Physiol. 2010, 167, 1477–1485. [Google Scholar] [CrossRef] [PubMed]
  80. Chen, X.; Chen, Z.; Fiorentino, A.; Kuess, M.; Tharayil, N.; Kumar, R.; Leonard, E.; Noorai, R.; Hu, Q.; Luo, H. MicroRNA169 integrates multiple factors to modulate plant growth and abiotic stress responses. Plant Biotechnol. J. 2024, 22, 2541–2557. [Google Scholar] [CrossRef] [PubMed]
  81. Tan, Z.; Wang, Y.; Liu, Y.; Jiang, H.; Li, Y.; Zhong, X.; Zhuang, L.; Yang, Z.; Zhang, X.; Huang, B. Transcriptional Regulation Mechanisms in AsAFL1-mediated Drought Tolerance for Creeping Bentgrass (Agrostis stolonifera). Physiol. Plant. 2025, 177, e70225. [Google Scholar] [CrossRef] [PubMed]
  82. Aswath, C.R.; Kim, S.H.; Mo, S.Y.; Kim, D.H. Transgenic plants of creeping bent grass harboring the stress inducible gene, 9-cis-epoxycarotenoid dioxygenase, are highly tolerant to drought and NaCl stress. Plant Growth Regul. 2005, 47, 129–139. [Google Scholar] [CrossRef]
  83. Xu, Y.; Huang, B. Transcriptional factors for stress signaling, oxidative protection, and protein modification in ipt-transgenic creeping bentgrass exposed to drought stress. Environ. Exp. Bot. 2017, 144, 49–60. [Google Scholar] [CrossRef]
  84. Zhou, M.; Luo, H. Role of microRNA319 in creeping bentgrass salinity and drought stress response. Plant Signal. Behav. 2014, 9, 1375–1391. [Google Scholar] [CrossRef]
  85. Zhou, M.; Li, D.; Li, Z.; Hu, Q.; Yang, C.; Zhu, L.; Luo, H. Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 2013, 161, 1375–1391. [Google Scholar] [CrossRef]
  86. Zhao, J.; Yuan, S.; Zhou, M.; Yuan, N.; Li, Z.; Hu, Q.; Bethea, F.G., Jr.; Liu, H.; Li, S.; Luo, H. Transgenic creeping bentgrass overexpressing Osa-miR393a exhibits altered plant development and improved multiple stress tolerance. Plant Biotechnol. J. 2019, 17, 233–251. [Google Scholar] [CrossRef]
  87. Yuan, S.; Zhao, J.; Li, Z.; Hu, Q.; Yuan, N.; Zhou, M.; Xia, X.; Noorai, R.; Saski, C.; Li, S. MicroRNA396-mediated alteration in plant development and salinity stress response in creeping bentgrass. Hortic. Res. 2019, 6, 48. [Google Scholar] [CrossRef]
  88. Yuan, S.; Li, Z.; Li, D.; Yuan, N.; Hu, Q.; Luo, H. Constitutive expression of rice microRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping bentgrass. Plant Physiol. 2015, 169, 576–593. [Google Scholar] [CrossRef]
  89. Li, Z.; Baldwin, C.M.; Hu, Q.; Liu, H.; Luo, H. Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant Cell Environ. 2010, 33, 272–289. [Google Scholar] [CrossRef]
  90. Xie, Y.; Sun, X.; Ren, J.; Fan, J.; Lou, Y.; Fu, J.; Chen, L. Genetic diversity and association mapping of cadmium tolerance in bermudagrass [Cynodon dactylon (L.) Pers.]. Plant Soil 2015, 390, 307–321. [Google Scholar] [CrossRef]
  91. Gladkov, E.; Gladkova, O.; Glushetskaya, L. Estimation of heavy metal resistance in the second generation of creeping bentgrass (Agrostis solonifera) obtained by cell selection for resistance to these contaminants and the ability of this plant to accumulate heavy metals. Appl. Biochem. Microbiol. 2011, 47, 776–779. [Google Scholar] [CrossRef]
  92. Yuan, J.; Bai, Y.; Chao, Y.; Sun, X.; He, C.; Liang, X.; Xie, L.; Han, L. Genome-wide analysis reveals four key transcription factors associated with cadmium stress in creeping bentgrass (Agrostis stolonifera L.). PeerJ 2018, 6, e5191. [Google Scholar] [CrossRef] [PubMed]
  93. Gururani, M.A.; Ganesan, M.; Song, I.-J.; Han, Y.; Kim, J.-I.; Lee, H.-Y.; Song, P.-S. Transgenic turfgrasses expressing hyperactive Ser599Ala phytochrome A mutant exhibit abiotic stress tolerance. J. Plant Growth Regul. 2016, 35, 11–21. [Google Scholar] [CrossRef]
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Figure 1. Pathological manifestations of dollar spot disease and hyphal morphology of Clarireedia spp. (a–c) Advanced progression of dollar spot disease, presenting pronounced leaf dwarfism and apical stunting, with coalescing white necrotic lesions extending across the entire foliar surface; (d) Morphological characterization of S. homoeocarpa colonies cultured on potato dextrose agar (PDA) medium; (e) Visualization of S. homoeocarpa hyphal architecture under microscopic examination. (Source: Original figure created by the authors for this review).
Figure 1. Pathological manifestations of dollar spot disease and hyphal morphology of Clarireedia spp. (a–c) Advanced progression of dollar spot disease, presenting pronounced leaf dwarfism and apical stunting, with coalescing white necrotic lesions extending across the entire foliar surface; (d) Morphological characterization of S. homoeocarpa colonies cultured on potato dextrose agar (PDA) medium; (e) Visualization of S. homoeocarpa hyphal architecture under microscopic examination. (Source: Original figure created by the authors for this review).
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Figure 2. Pathological manifestations of brown patch disease and hyphal morphology of Rhizoctonia solani. (a–c) At the fulminant stage of brown patch disease, foliage exhibits extensive browning accompanied by progressive tissue maceration, culminating in either necrotic decay or desiccated yellowing of leaf blades; (d) Morphological characterization of R. solani colonies cultured on potato dextrose agar (PDA) medium; (e) Visualization of R. solani hyphal architecture under microscopic examination. (Source: Original figure created by the authors for this review).
Figure 2. Pathological manifestations of brown patch disease and hyphal morphology of Rhizoctonia solani. (a–c) At the fulminant stage of brown patch disease, foliage exhibits extensive browning accompanied by progressive tissue maceration, culminating in either necrotic decay or desiccated yellowing of leaf blades; (d) Morphological characterization of R. solani colonies cultured on potato dextrose agar (PDA) medium; (e) Visualization of R. solani hyphal architecture under microscopic examination. (Source: Original figure created by the authors for this review).
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Figure 3. Key genes and regulatory networks of creeping bentgrass tolerance to abiotic stresses. (Source: Original figure created by the authors for this review).
Figure 3. Key genes and regulatory networks of creeping bentgrass tolerance to abiotic stresses. (Source: Original figure created by the authors for this review).
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Table 1. Characteristics of major diseases on creeping bentgrass.
Table 1. Characteristics of major diseases on creeping bentgrass.
DiseasePathogenSymptomsPrevention MeasuresReferences
Dollar SpotClarireedia spp.Small round, sunken, bleached, or straw-colored patchesResistance materials: Declaration, Kingpin,
Benchmark DSR, 007, 13M, HTM, HTL Physical control: removal of dew, sand cover, rolling.
Chemical control: ferric sulfate/ferrous sulfate, azoxystrobin + propiconazole, triadimefon/paclobutrazol + fungicide, antifungal protein Efe-AfpA, mustard powder.
Agricultural control: calcium fertilizer, nitrogen fertilizer
Biological control: Pseudomonas putida 88cfp and 166fp, Bacillus cereus 44bac, Bacillus licheniformis		[14,15,16,17,18,19,20,21,22,23,24,25,26]
Brown PatchRhizoctonia solaniBrown or tan plaquePhysical control: Fan
Chemical control: 2,3-butanediol, PepEST protein
Agricultural control: Potassium Fertilization
Biological control: T-phylloplanins, S-phylloplanins, Trichoderma atroviride		[27,28,29,30,31,32,33,34]
Bacterial EtiolationAcidovorax avenae subsp.
/Xanthomonas translucens
/Pantoea ananatis		Leaf tip necrosis, wilting, yellowing and stem yellowing, electrolyte leakage in leaves and roots increased, chlorophyll content decreased and root activity decreased.Chemical control: Salicylic acid, jasmonic acid, oxytetracycline, acibenzolar-S-methyl + chlorothalonil, trinexapac-ethyl[35,36,37,38,39,40,41,42,43,44,45,46]
Microdochium patchMicrodochium nivaleRound, watery patches; leaves light gray, brown, white or grayish black, pink margin; pink mildewChemical control: Medallion, Headway, ferric sulfate, Civitas + Harmonizer, Phosphite
Biological control: Turf WPG, Turf S+		[47,48,49,50,51]
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Ren, Z.; Sun, X.; Chen, Y.; Zhang, Y.; Yuan, M.; Li, M.; Ren, X.; Wang, X. Resistance of Creeping Bentgrass to Biotic and Abiotic Stresses: A Model System for Grass Stress Biology. Agronomy 2025, 15, 2761. https://doi.org/10.3390/agronomy15122761

AMA Style

Ren Z, Sun X, Chen Y, Zhang Y, Yuan M, Li M, Ren X, Wang X. Resistance of Creeping Bentgrass to Biotic and Abiotic Stresses: A Model System for Grass Stress Biology. Agronomy. 2025; 15(12):2761. https://doi.org/10.3390/agronomy15122761

Chicago/Turabian Style

Ren, Zhuang, Xinbo Sun, Yalin Chen, Yaxi Zhang, Meng Yuan, Mengyu Li, Xiaopeng Ren, and Xiaodong Wang. 2025. "Resistance of Creeping Bentgrass to Biotic and Abiotic Stresses: A Model System for Grass Stress Biology" Agronomy 15, no. 12: 2761. https://doi.org/10.3390/agronomy15122761

APA Style

Ren, Z., Sun, X., Chen, Y., Zhang, Y., Yuan, M., Li, M., Ren, X., & Wang, X. (2025). Resistance of Creeping Bentgrass to Biotic and Abiotic Stresses: A Model System for Grass Stress Biology. Agronomy, 15(12), 2761. https://doi.org/10.3390/agronomy15122761

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