Skip to main content
NCBI home page
Plants logoLink to Plants
. 2026 Jun 21;15(12):1917. doi: 10.3390/plants15121917

Recent Advances in Physiological and Biochemical Responses of Grapevines to Downy Mildew Infection

Sheng Wang 1,†, Tao He 2,†, Qi Liu 3,†, Mingxin Fu 4, Naiming Zhang 4,*, Li Bao 4,*
PMCID: PMC13307539  PMID: 42357236

Abstract

Grapevine downy mildew, caused by the oomycete pathogen Plasmopara viticola (P. viticola), is one of the most devastating diseases threatening the global grape industry. The pathogen invades host plants through stomata, triggering a series of highly coordinated physiological disorders and biochemical defense events. This review systematically summarizes the dynamic changes in morphological structures (stomatal characteristics), physiological functions (photosynthesis, membrane system integrity, and carbon metabolism), and multi-level biochemical defense systems (reactive oxygen species (ROS) scavenging enzyme system, phenylpropanoid metabolic pathway, pathogenesis-related proteins, and phenolic compounds) in grapevines following infection. It focuses on analyzing the differences in the timing, intensity, and metabolic reprogramming of defense responses between resistant and susceptible cultivars, pointing out that the essence of disease resistance lies in early pathogen recognition and rapid defense induction. The conflicting conclusions regarding indicators such as soluble sugars, peroxidase (POD), and superoxide dismutase (SOD) are discussed from the perspectives of experimental systems, cultivar genetic backgrounds, and pathogen physiological race differences. Furthermore, the known physiological and biochemical alterations are linked to upstream signaling pathways, including salicylic acid and jasmonic acid (SA/JA), calcium signaling, and mitogen-activated protein kinase (MAPK) cascades. Recent advances in revealing resistance mechanisms in the omics era are also introduced. Finally, future research directions are proposed, including constructing multi-indicator dynamic evaluation models, verifying key gene functions using gene editing, exploring the potential of epigenetic regulation, and developing integrated control strategies combined with microbiome research. This review aims to provide theoretical support for grapevine downy mildew resistance breeding and sustainable disease management.

Keywords: grapevine, downy mildew, Plasmopara viticola, defense signaling network, disease resistance

1. Introduction

Grapevine downy mildew, caused by the obligate biotrophic oomycete P. viticola (Berk. & M.A. Curtis), is one of the most widely distributed and destructive diseases in viticulture worldwide [1,2,3]. This disease primarily infects young tissues, including leaves, shoots, and immature fruits. The typical symptom is the formation of white downy mildew growth (consisting of sporangiophores and sporangia of the pathogen) on abaxial leaf surfaces, which leads to premature leaf senescence and abscission, shoot necrosis, and fruit shriveling and drop. In severe epidemic years, yield losses can reach up to 80% [2]. The pathogen overwinters as oospores or mycelia in infected plant debris. In the following year, when favorable temperature and humidity conditions occur, sporangia are produced and release zoospores, which invade host plants through stomata to complete the primary and secondary infection cycles [4,5].

For a long time, commercial grape production has mainly relied on chemical fungicides for downy mildew control. However, the intensive and repeated use of fungicides has resulted in the rapid development of fungicide resistance in pathogen populations and reduced control efficacy while also causing serious problems such as pesticide residues and environmental pollution [6]. Therefore, exploiting and utilizing the inherent disease resistance of grapevines has become the core strategy for sustainable disease management. In recent years, extensive research has been conducted on the screening of resistant germplasms and resistance mechanisms at morphological, physiological, biochemical, and molecular levels [7,8]. This review systematically summarizes the physiological and biochemical responses of grapevines to P. viticola infection, focusing on membrane integrity, photosynthesis, carbon metabolism, antioxidant enzymes, the phenylpropanoid pathway, PR proteins, and phenolic compounds. It analyzes the differential response patterns between resistant and susceptible cultivars and attempts to link these downstream response events with upstream signaling pathways. This review aims to reveal the physiological and biochemical nature of grapevine resistance to downy mildew and provide a theoretical basis for disease resistance breeding and green disease control.

2. Early Infection Stage: The Dual Role of Stomata as a Physical Barrier

Stomata are the primary natural entry route for P. viticola zoospores to invade host plants. The relationship between stomatal characteristics and disease resistance remains controversial in existing studies. Some studies have shown that stomatal length, width, and guard cell area are moderately positively correlated with disease resistance, but larger stomatal structures objectively facilitate zoospore attachment, cyst formation, and germ tube penetration [9]. The P. viticola can complete infection and produce sporangiophores through stomata [10]. Higher stomatal density and aperture increase the probability of zoospore encounter, thereby enhancing infection success rates.

Stomatal characteristics exhibit genetic variations among different grapevine cultivars, but stomatal parameters do not show a simple linear relationship with resistance. Han et al. [11] found that susceptible cultivars had higher leaf stomatal density. However, stomata primarily serve as pathogen entry channels, and disease resistance depends largely on post-invasive recognition and defense activation, including ABA-mediated stomatal immunity. In addition, the chemical composition of guard cells, such as waxes and phenolics, can influence zoospore attachment, while differences in pathogen physiological races contribute to variation in virulence. These factors together may explain the observed discrepancies in the relationship between stomatal density and disease severity [12]. Recent studies have shown that stomata are not only passive channels, but their opening and closing movements are also regulated by immune signals induced by pathogen-associated molecular patterns (PAMPs) such as flg22 and chitin (Figure 1) [13,14]. Plants can actively close stomata as an early “stomatal immunity” strategy to prevent bacterial invasion [15], but whether oomycetes trigger similar responses remains unclear. In the grapevine–P. viticola interaction, evidence suggests that pathogen-derived effectors may interfere with stomatal immunity and promote stomatal reopening, thereby facilitating invasion [9,11,16,17]. Therefore, the relationship between stomata and resistance needs to be re-examined in the context of a more complex attack–defense game, and morphological parameters alone are insufficient as resistance indicators.

Figure 1.

Figure 1

Open in a new tab

Schematic diagram of structures involved in leaf infection and the infection process of P. viticola.

3. Physiological Changes in Grapevines Following Downy Mildew Infection

3.1. Plasma Membrane System Damage and Lipid Peroxidation

The plasma membrane is a selective barrier that maintains the stability of the intracellular and extracellular environments. Following P. viticola infection, the pathogen causes host cell death by secreting cell wall-degrading enzymes and toxic proteins (effectors) while simultaneously inducing a ROS burst. This triggers a chain reaction of membrane lipid peroxidation, converting the plasma membrane from semipermeable to fully permeable, resulting in massive exudation of intracellular electrolytes and organic molecules [18,19].

Malondialdehyde (MDA) is the main end product of membrane lipid peroxidation, and its content directly reflects the degree of membrane damage. Studies have shown that after grapevine infection with P. viticola, cell membranes at sites of hyphal aggregation are dissolved, and both MDA content and relative conductivity increase significantly [20]. Comparisons between cultivars with different resistance levels revealed that MDA accumulation and electrolyte leakage rates were significantly lower in resistant cultivars than in susceptible ones [21]. The cellular mechanisms underlying this difference may include ① resistant cultivars having a lower proportion of unsaturated fatty acids in their membrane lipid composition, making them more tolerant to peroxidation; ② higher contents of membrane-bound antioxidants (α-tocopherol and ubiquinone); and ③ stronger activities of membrane repair-related proteins (phospholipid scramblases and vesicle trafficking-related proteins) [22,23]. In addition, maintenance of plasma membrane integrity depends on intracellular calcium homeostasis. Calcium ion influx is an early signaling event following pathogen infection, but sustained high calcium levels activate calcium-dependent phospholipases, exacerbating membrane degradation [24]. Resistant cultivars may more effectively confine calcium signals within specific spatial and temporal ranges.

3.2. Chlorophyll Degradation and Photosynthetic System Damage

A decrease in chlorophyll content is the most intuitive physiological change caused by downy mildew. As disease severity increases, chlorophyll synthesis is inhibited, leading to reduced content and diminished ability of leaves to absorb and utilize light energy [25]. Seven days after inoculation with P. viticola, the chlorophyll content of the susceptible cultivar decreased, showing a large and rapid decline. In contrast, resistant genotypes exhibited smaller or insignificant decreases in chlorophyll content [26].

Chlorophyll fluorescence parameters reveal more serious damage to the photosynthetic apparatus. Downy mildew infection significantly inhibits the potential photochemical efficiency of photosystem II (PSII) (Fv/Fm). The magnitude of Fv/Fm reduction in infected areas is positively correlated with disease severity, and this change often precedes visible symptoms [27,28]. This suggests that the pathogen has already inhibited the PSII repair cycle through mechanisms such as toxin secretion, alteration of chloroplast ROS homeostasis, and interference with D1 protein turnover before host cell death [29]. Furthermore, decreased CO2 assimilation capacity leads to excess reducing power (NADPH) and adenosine triphosphate (ATP), further exacerbating photoinhibition and ROS production. Resistant cultivars may alleviate photodamage through enhanced non-photochemical quenching (NPQ) and upregulated cyclic electron transport [30,31].

3.3. Changes in Gas Exchange Parameters

Following P. viticola infection, photosynthetic parameters of grapevines are significantly inhibited, manifested as marked decreases in net photosynthetic rate (Pn) and transpiration rate (Tr), while intercellular CO2 concentration (Ci) shows an increasing trend [26]. Further studies by Júnior et al. [32] in grapevine cultivars with different resistance levels demonstrated that as disease severity increased, Pn and Tr in resistant cultivars decreased but to a lesser extent, while susceptible cultivars exhibited more pronounced photosynthetic inhibition, including decreased maximum carboxylation rate of Rubisco, reduced photochemical efficiency, and significantly elevated Ci. Similar results have been reported in the cucumber downy mildew system, indicating that downy mildew infection generally leads to reduced photosynthetic efficiency and structural damage to the photosynthetic system in hosts [33].

The characteristic pattern of decreased Pn accompanied by increased Ci indicates that photosynthetic limitation primarily arises from non-stomatal factors, i.e., damage to the photosynthetic apparatus within mesophyll cells, rather than stomatal closure. The underlying mechanisms may involve oxidative inactivation of key enzymes such as Rubisco caused by ROS accumulation, inhibition of Calvin cycle key enzymes (glyceraldehyde-3-phosphate dehydrogenase), and dysfunction of the photosynthetic electron transport chain due to damage to chloroplast membrane systems [34]. In addition, the reduction in Tr not only reflects decreased stomatal conductance but may also be related to impaired mesophyll conductance, a process closely associated with downregulated expression or activity of plasma membrane intrinsic proteins (PIPs) [35].

3.4. Soluble Sugar Content: Temporal Dynamics Behind the Contradictions

Soluble sugars are not only important carbon sources and energy reserves in plants but also crucial metabolic nodes for osmotic regulation, stress signal transduction, and defense response regulation [36]. Existing studies have shown that changes in soluble sugar content following pathogen infection do not follow a single trend but are jointly influenced by multiple factors, including host genotype, pathogen type, infection stage, and environmental stress background. Mahatma et al. [37] found significant differences in leaf metabolite composition between resistant and susceptible pearl millet genotypes to downy mildew, suggesting that carbohydrate metabolism may be involved in host defense responses. Xin et al. [38] pointed out in rice blast research that soluble sugar and soluble protein contents have certain correlations with seedling disease resistance, indicating that soluble sugars can serve as potential physiological and biochemical indicators for evaluating plant disease resistance. Similarly, studies on cucumber downy mildew have demonstrated that alterations in photosynthesis and carbohydrate metabolism accompany disease development, further supporting the use of carbohydrate-related metabolites as indicators of plant responses to downy mildew stress [39].

However, the relationship between soluble sugar content and resistance is not entirely consistent across different studies: some studies suggest that resistant materials can maintain higher or more stable soluble sugar levels in the early infection stage, while others find that susceptible materials show more pronounced sugar accumulation during disease development [40,41]. Therefore, the relationship between soluble sugars and downy mildew resistance is not simply positive or negative but rather reflects a dynamic metabolic response process that changes with infection progression. These differences can be explained by the temporal dynamics of carbon metabolism and the remodeling of "source–sink" relationships during pathogen infection. In the very early stage of infection, resistant materials may rapidly recognize the pathogen and regulate sugar transport and signaling pathways, promoting the transient accumulation of soluble sugars to serve as energy substrates, osmotic regulators, and signaling molecules for defense gene activation. In the middle stage of infection, soluble sugars may be further redirected to defense-related processes such as respiratory metabolism, phenolic compound synthesis, and lignin deposition, thus showing a decline in content or maintenance of relative stability [42].

In contrast, susceptible materials exhibit delayed defense activation, which promotes pathogen spread and cellular damage, reduces membrane stability, impairs photosynthate export and source–sink balance, and ultimately leads to the continuous accumulation or irregular fluctuation of soluble sugars [43,44]. Studies on grapevine downy mildew have also shown that pathogen infection can significantly affect leaf photosynthesis and defense-related transcriptional processes, providing physiological and molecular evidence for the dynamic changes in soluble sugar content with infection progression [26,45].

Therefore, the absolute content of soluble sugars alone is insufficient to determine material resistance. Its early accumulation rate, mid-stage consumption or conversion rate, and late fluctuation pattern may better reflect the true state of the host’s defense response. Future research should focus on the dynamic regulation of soluble sugar metabolism during pathogen infection by continuously monitoring soluble sugar accumulation at key infection stages (0–72 h post-inoculation). Combined analyses of sugar metabolism-related enzymes, hexokinase-dependent sugar signaling, and downstream defense-responsive genes would help clarify how carbohydrate metabolism and sugar signaling coordinate host defense responses, thereby contributing to the development of resistance against downy mildew [46,47].

4. Activation of Biochemical Defense Systems in Grapevines Following Downy Mildew Infection

Upon infection by P. viticola, grapevines activate a multi-level biochemical defense network, including ROS scavenging enzyme systems, the phenylpropanoid metabolic pathway, PR proteins, and phenolic compound accumulation (Figure 2) [48].

Figure 2.

Figure 2

Open in a new tab

Multi-level defense mechanisms of grapevines in response to downy mildew pathogen infection.

4.1. Reactive Oxygen Species Scavenging Enzyme System

4.1.1. Superoxide Dismutase (SOD)

The SOD is a key enzyme in the plant ROS scavenging system, which catalyzes the dismutation of superoxide anions (O2−) into H2O2 and O2, thereby limiting excessive O2− accumulation and maintaining cellular redox homeostasis [49]. Changes in SOD activity following downy mildew infection are generally closely related to host resistance. Studies have shown that exogenous melatonin can enhance antioxidant enzyme activities and improve downy mildew resistance in cucumbers [50]; kaolin particle film treatment can also enhance grapevine resistance to downy mildew by inducing defense responses, with regulation of ROS metabolism being an important link [48]. These results indicate that a timely and effective SOD response helps scavenge excess O2−, reduce oxidative damage, and maintain defense signal transduction. However, together with evidence that resistant and susceptible grapevine cultivars activate distinct defense strategies, these findings suggest that the relationship between SOD activity and disease resistance is complex and cannot be interpreted as simply positive [51]. This discrepancy may arise from the dual role of ROS in plant–pathogen interactions. Moderate ROS accumulation can act as signaling molecules to participate in defense response activation, while excessive ROS leads to membrane lipid peroxidation, protein inactivation, and cellular structural damage [52]. Therefore, the role of SOD in disease resistance depends not only on its activity level but also on its induction timing, response intensity, and coordination with downstream H2O2 scavenging systems. Resistant materials usually rapidly induce SOD activity in the early infection stage, converting O2− to H2O2, which has dual signaling functions, thereby promoting defense response initiation while controlling oxidative damage. In contrast, higher SOD activity in susceptible materials may be more indicative of passive stress responses induced by ROS accumulation after pathogen spread; if their response is delayed or fails to coordinate with peroxidase (POD), catalase (CAT), and the ascorbate–glutathione cycle, it may still lead to H2O2 accumulation and exacerbate oxidative damage [53,54]. Therefore, the induction timing and peak intensity of SOD are more important than its final activity level.

4.1.2. Peroxidase (POD)

The POD participates in plant cell wall reinforcement, ROS homeostasis maintenance, and phenolic compound oxidation, making it an important defense-related enzyme following pathogen infection. On the one hand, POD promotes lignin polymerization to strengthen the physical barrier of cell walls; on the other hand, its mediated phenolic oxidation products may directly inhibit pathogen spread [48]. Existing studies have reported inconsistent relationships between POD activity and resistance: some studies showed that susceptible cultivars exhibited greater increases in POD activity after downy mildew infection [55], while others found that resistant materials had higher POD activity levels or stronger induction amplitudes [56,57]. This discrepancy may be related to the POD isozyme composition and functional differentiation. Different POD isozymes differ in subcellular localization, substrate preference, and physiological functions. Cell wall-bound acidic POD is more likely to be involved in lignification and structural defense, while some cytosolic or alkaline PODs mainly participate in H2O2 scavenging and redox regulation [58]. These findings suggest that the contribution of POD to disease resistance depends not only on its overall activity but also on the specific functions of individual POD isoforms and their coordination within the antioxidant defense network [59,60]. Thus, simply comparing total POD activity is difficult to accurately explain its role in defense responses. Distinguishing POD isozyme types through native PAGE, isozyme profile analysis, and substrate specificity determination is more meaningful than total POD activity.

4.1.3. Catalase (CAT)

The CAT is an important antioxidant enzyme in plants that decomposes H2O2 into H2O and O2, primarily located in peroxisomes. Studies have shown that CAT activity is usually significantly increased in resistant materials after downy mildew infection, while it remains low or decreases in the late infection stage in susceptible materials [45,61]. However, some studies have also reported a downward trend in CAT activity during induced defense processes [48]. Its role may depend on H2O2 accumulation levels, infection periods, and the synergistic status of other antioxidant enzyme systems.

Compared with ascorbate peroxidase (APX) and some peroxidases, CAT has a lower affinity for H2O2 and usually plays a major scavenging role when H2O2 concentrations are high [62]. In the early stage of pathogen infection, resistant cultivars may preferentially use higher-affinity APX and peroxidases (PRX) to finely regulate H2O2 signals, while in the late infection stage, when H2O2 is produced in large quantities, CAT is activated to prevent oxidative damage. Susceptible cultivars may experience CAT release or inactivation due to impaired peroxisome integrity. Therefore, the change pattern of the CAT/APX ratio can serve as a resistance indicator: resistant cultivars show APX dominance in the early stage and CAT elevation in the late stage, while susceptible cultivars maintain persistently low CAT levels, and APX is also prone to inactivation.

4.1.4. Ascorbate–Glutathione Cycle and APX

The APX catalyzes H2O2 reduction using ascorbate (AsA) as an electron donor and is an important enzyme for finely regulating intracellular H2O2 levels in plant cells [63]. Ascorbate peroxidase (APX), together with monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and glutathione reductase (GR), constitutes the ascorbate–glutathione (AsA–GSH) cycle. By continuously regenerating ascorbate (AsA) and glutathione (GSH), this cycle maintains cellular redox balance and represents one of the most important H2O2-scavenging pathways in ROS-producing organelles, especially chloroplasts [63,64,65]. Transgenic studies have further demonstrated the critical role of APX in oxidative stress defense. Previous studies have shown that chloroplast-targeted APX overexpression enhances antioxidant capacity and protects the photosynthetic machinery by maintaining higher photosynthetic rates and PSII photochemical efficiency under oxidative stress [66]. Nazish et al. [61] demonstrated that overexpression of thylakoid APX in Arabidopsis thaliana mitigates paraquat-induced photooxidative stress and enhances cellular ROS scavenging [67]. These results indicate that chloroplast APX and its associated antioxidant network play important roles in maintaining photosynthetic system stability and limiting ROS damage. In the grapevine–P. viticola interaction, studies have found that the reduced state ratios of AsA and GSH pools (AsA/DHA, GSH/GSSG) in leaves of resistant cultivars are significantly higher than those of susceptible cultivars, even when total antioxidant capacities are similar. This suggests that the key to resistance in resistant cultivars lies in higher activities of regeneration systems (MDHAR, DHAR, and GR), which allow rapid reduction and regeneration of oxidants [68].

4.2. Key Enzymes of the Phenylpropanoid Metabolic Pathway

4.2.1. Phenylalanine Ammonia-Lyase (PAL)

The PAL is the key rate-limiting enzyme of the phenylpropanoid metabolic pathway, which catalyzes the deamination of phenylalanine to produce cinnamic acid, thereby initiating the synthesis of various defense-related metabolites, including lignin, phenolic acids, flavonoids, and stilbenes [69]. This pathway plays a central role in grapevine defense responses against downy mildew. Its products can not only strengthen cell wall structural barriers through lignin deposition but also directly inhibit pathogen spread via antimicrobial substances such as chlorogenic acid, flavonoids, and resveratrol [70]. Recent physiological and transcriptomic studies have shown that the accumulation of phenylpropanoid metabolites in grapevine leaves is closely correlated with downy mildew resistance [21]; exogenous thiamine-induced grapevine resistance to downy mildew is also accompanied by significant activation of the phenylpropanoid metabolic pathway [71]. In terms of response patterns, resistant cultivars exhibit a large induction amplitude of PAL activity, with an early and long-lasting activity peak [72]. The five PAL family members (VvPAL1-5) show distinct expression patterns in grapevines. Studies have indicated that several PAL family members, including VvPAL1, VvPAL2, and VvPAL5, have been reported to be induced following P. viticola infection, although their expression patterns may vary among cultivars and infection stages [73].

Phenylpropanoid metabolites also exhibit clear spatial division of labor at the tissue and subcellular levels: lignin is mainly deposited in cell walls and vascular tissues around infection sites, promoting papilla formation and cell wall reinforcement; phenolic substances such as chlorogenic acid are mostly accumulated in vacuoles and can be released to participate in local antimicrobial reactions when pathogens invade or cells are damaged. This spatial compartmentalization and coordination are important features of disease resistance mechanisms [74,75].

4.2.2. Polyphenol Oxidase (PPO)

The PPO is a key enzyme in plant phenolic oxidative metabolism, which mainly catalyzes the oxidation of phenolic substrates to produce quinone compounds [76]. Quinones have strong antimicrobial activity, can covalently modify pathogen proteins and enzymes, and simultaneously promote cell wall lignification [77]. In line with these findings, PPO activity was rapidly and strongly induced in the resistant genotype Garovilli following Macrophomina phaseolina infection, whereas it remained low and declined in the susceptible genotype H 174 [78]. For a long time, PPO has been considered to be stored in chloroplasts or plastids in the form of inactive precursors (latent pro-PPO), strictly spatially separated from phenolic substrates stored in vacuoles. Membrane system disturbances, Ca2+ influx, or cellular structural damage caused by pathogen infection can promote the contact of PPO with substrates such as chlorogenic acid and catechol, triggering phenolic oxidation reactions and generating quinone products with antimicrobial and antinutritional properties, thereby limiting pathogen spread [79,80]. Resistant cultivars can more effectively maintain PPO mRNA stability and induce the synthesis of precursor proteins, while susceptible cultivars may experience PPO degradation due to excessive protease activity.

4.3. Pathogenesis-Related Proteins (CHT and GLU)

Chitinase (CHT; PR-3, PR-4, PR-8, and PR-11) and β-1,3-glucanase (GLU; PR-2) are important members of plant pathogenesis-related proteins. They are often induced after pathogen infection and participate in processes such as cell wall degradation, antimicrobial substance release, and defense signal amplification [81]. These two enzymes can synergistically hydrolyze structural polysaccharides in pathogen cell walls, thereby inhibiting pathogen spread. Although P. viticola is an oomycete whose cell walls are mainly composed of β-1,3-glucan and cellulose with low or no chitin content, GLU can still directly act on its cell wall components; CHT may indirectly enhance host defense responses by recognizing or hydrolyzing structurally similar glycosidic bonds or promoting the release of oligosaccharide elicitors [82].

Studies have confirmed that CHT and GLU activities and gene expression are significantly increased in resistant cultivars after inoculation with P. viticola [51,83,84], and their antifungal activity is greatly enhanced when acting synergistically [85]. Numerous studies have found that there are two types of GLU in grapevine leaves: alkaline GLU is localized in vacuoles, while acidic GLU is secreted into the intercellular spaces. Since the early stage of P. viticola infection mainly occurs in intercellular spaces and mesophyll tissues, secreted GLU can contact pathogen structures earlier and participate in local defense responses. Endo-β-1,3-glucanase with anti-P. viticola activity has been identified in grapevines, indicating that GLU can directly participate in the inhibition of downy mildew [86].

Meanwhile, PR proteins not only have direct antimicrobial activity but also interact with the plant immune signaling network, playing extensive regulatory functions in responses to both biotic and abiotic stresses [87]. Furthermore, the hydrolysis products of CHT and GLU (chitooligosaccharides and glucans) can act as damage-associated molecular patterns (DAMPs) to further amplify defense signals, forming a positive feedback loop [88].

4.4. Phenolic Compounds: From End Products to Signaling Hubs

Phenolic compounds are the end products of phenylpropanoid metabolism, including phenolic acids (chlorogenic acid, ferulic acid), flavonoids (catechin, proanthocyanidins), and stilbenes (resveratrol). They can inhibit pathogen cell wall-degrading enzymes, directly inactivate pathogens, enhance cell wall mechanical strength, and act as signaling molecules to activate downstream defense responses [89]. Studies have shown that the contents of chlorogenic acid, ferulic acid, proanthocyanidins, catechin, and total phenolics in fruits or leaves of resistant cultivars exhibited significantly greater increases after inoculation than those of susceptible cultivars [90,91]. Resveratrol, a phytoalexin unique to grapevines, is rapidly synthesized and accumulated after P. viticola infection, and its content is highly correlated with disease resistance. Stilbene synthase (STS), the key enzyme catalyzing the condensation of one molecule of coumaroyl-CoA with three molecules of malonyl-CoA to form resveratrol, belongs to the type III polyketide synthase (PKS) family [92]. Unlike other stilbene-producing plants, the grapevine genome (cv. PN40024) contains an exceptionally large STS multigene family, whose large-scale expansion itself constitutes the genetic basis for grapevine disease resistance potential [90,93,94]. Pathogen-induced STS expression varies among cultivars, with resistant cultivars generally exhibiting stronger and more rapid induction of STS genes following pathogen infection [95]. Furthermore, phenolic compounds can be oxidized by PPO to quinones, which can cross-link cell wall proteins to form an impermeable barrier. Covalent linkages between phenolics and cell wall polysaccharides (ferulic acid bridging of arabinoxylans) are also important mechanisms for enhancing cell wall resistance to degradation.

4.5. Upstream Signaling Pathways: From Physiological and Biochemical Responses to Molecular Regulation

The physiological and biochemical events described above do not occur in isolation but are controlled by a highly regulated signaling network. Pathogen-associated molecular patterns (conserved microbial molecules derived from P. viticola, including β-glucans and other pathogen-associated molecular patterns (PAMPs)) are perceived by plant pattern-recognition receptors (PRRs) on the plant plasma membrane, triggering PAMP-triggered immunity (PTI) [96]. This process involves ① activation of plasma membrane NADPH oxidase (RBOH) leading to ROS burst; ② calcium ion influx activating calcium-dependent protein kinases (CDPKs) and calmodulins; and ③ phosphorylation of transcription factors by MAPK cascades (MEK2-MPK3/MPK6) [97,98]. These signals ultimately lead to the expression of downstream defense genes (PAL, STS, CHT, and GLU). SA and JA/ethylene (ET) are the major endogenous hormonal signals. It is generally accepted that the SA pathway plays a dominant role against biotrophic pathogens (downy mildew), while the JA/ET pathway is effective against necrotrophic pathogens. In the grapevine–P. viticola interaction, resistant cultivars exhibit earlier and higher SA accumulation, which triggers systemic acquired resistance (SAR), whereas susceptible cultivars may experience abnormal activation of the JA pathway or dysregulation of the SA/JA balance. Although existing studies have verified the roles of these signals through exogenous SA or methyl jasmonate treatments, the fine-tuned crosstalk between SA and JA in grapevine downy mildew still requires in-depth exploration [99].

5. Conclusions and Perspectives

5.1. Conclusions

This review systematically summarizes the research progress on the physiological and biochemical responses of grapevines to downy mildew infection. At the physiological level, pathogen infection leads to intensified membrane lipid peroxidation (MDA↑, electrical conductivity↑), impaired photosynthesis (Chl↓, Fv/Fm↓, Pn↓, Ci↑), and carbon metabolism reprogramming (dynamic fluctuations of soluble sugars). Resistant cultivars exhibit milder damage and faster recovery capacity in these indicators. At the biochemical level, grapevines activate a multi-level defense system, including ROS scavenging enzyme systems (SOD, POD, CAT, and APX), phenylpropanoid metabolic enzymes (PAL, PPO), pathogenesis-related proteins (CHT, GLU), and phenolic compound accumulation. The core characteristics distinguishing resistant cultivars from susceptible ones lie in the timeliness, intensity, and sustainability of defense responses, rather than the absolute magnitude of any single indicator. Furthermore, the roles of physical structures such as stomata cannot be considered in isolation but need to be comprehensively evaluated in combination with chemical barriers and induced defenses (Figure 3, Table 1 and Table 2).

Figure 3.

Figure 3

Open in a new tab

Multi-level defense response model of grapevines under P. viticola infection.

Table 1.

Physiological responses of grapevines to P. viticola infection.

Indicator Change After Infection Resistance Implication References
Stomatal traits Variable Affect pathogen entry; interplay between stomatal immunity and pathogen-induced opening [9,10,11,12,13,14,15]
Chlorophyll content Decrease Lower reduction in resistant cultivars [25,26]
Fv/Fm Decrease Early disease indicator; reflects PSII damage [27,28,30,31,32]
Net photosynthetic rate (Pn) Decrease Photosynthetic inhibition [26,32,34]
Transpiration rate (Tr) Decrease Gas exchange limitation [26,32]
Intercellular CO2 concentration (Ci) Increase Non-stomatal limitation (mesophyll cell damage) [26,32,34]
Soluble sugars Dynamic (depends on infection stage) Early accumulation as signals/energy; later fluctuations related to source-sink balance [26,36,37,38,39,40,41,42,43,44,45,46,47]
Malondialdehyde (MDA) Increase Membrane lipid peroxidation; indicates membrane damage [18,19,20,21,22,23,24]
Open in a new tab

Table 2.

Biochemical defense responses associated with grapevine resistance.

Component Function Response in Resistant Cultivars Response in Susceptible Cultivars References
SOD Scavenges superoxide anions (O2−) Rapid early induction; converts O2− to H2O2 signal Delayed response or passive stress-induced increase [33,48,49,50,51,52,53,54]
POD Lignification, cell wall reinforcement, phenolic oxidation Strong activation; changes in isozyme profile Total activity may increase but functional differentiation insufficient [19,48,55,56,57,58,59,60]
CAT Decomposes high-concentration H2O2 Maintained or increased at late stage; prevents oxidative damage Activity often decreased or was inactivated due to release [45,48,61,62]
APX Fine regulation of H2O2 (high affinity) High activity; efficient AsA-GSH cycle regeneration Lower activity; weak regeneration system [63,64,65,66,67]
PAL Rate-limiting enzyme of phenylpropanoid pathway Rapid, sustained, and strong induction Weak or delayed induction [21,69,70,71,72,73,74,75]
PPO Oxidizes phenolics to quinones (antimicrobial, cross-linking) Increased activity; effective activation of proenzyme Lower activity or protein degradation [76,77,78,79,80]
CHT (Chitinase) Pathogenesis-related protein; degrades pathogen cell walls Strong induction; synergistic with GLU Weak induction [81,82,83,84,85,86,87,88]
GLU (β-1,3-glucanase) Pathogenesis-related protein; degrades oomycete cell walls Strong induction; secreted isoforms crucial Weak induction [81,82,83,84,85,86,87,88]
Resveratrol (Stilbene) Phytoalexin; inhibits pathogen Rapid accumulation; efficient STS gene expression Lower accumulation [89,90,91,92,93,94,95]
Open in a new tab

5.2. Research Perspectives

Although existing studies have outlined the physiological and biochemical landscape of grapevine–P. viticola interactions, there remains considerable room for improvement in mechanistic depth, integration level, and translational application:

(1) Constructing multi-indicator dynamic evaluation models: Current resistance identification mostly relies on field disease indices or enzyme activity measurements at single time points, which lack sufficient information dimensions. It is recommended that future studies utilize high-temporal-resolution phenotyping platforms combined with technologies such as chlorophyll fluorescence imaging, thermal imaging, and multispectral reflectance to simultaneously acquire high-frequency data on photosynthesis, transpiration, and antioxidant status. Machine learning algorithms (random forests, support vector machines) can then be employed to establish resistance prediction models based on early physiological and biochemical characteristics. This will provide non-destructive and high-throughput tools for large-scale germplasm screening.

(2) Moving from correlation analysis to causal relationship verification: Numerous studies have confirmed correlations between certain enzyme activities and resistance, but functional validation is lacking. Technologies such as virus-induced gene silencing (VIGS), CRISPR/Cas9, or overexpression should be used to functionally validate candidate genes such as VvPAL1, VvSTS, and VvGLU in the grapevine endogenous system, clarifying their necessity and sufficiency in disease resistance pathways. Meanwhile, heterologous expression systems (transient expression in tobacco) combined with effector co-infiltration can enable high-throughput screening of plant targets for pathogen effector proteins.

(3) Integrating omics to reveal regulatory networks: Single-indicator studies can no longer meet the demands of the systems biology era. It is suggested to conduct a joint analysis of time-series transcriptomics (RNA-seq) and metabolomics (LC-MS/MS) to construct gene–metabolite co-expression networks and identify core regulatory nodes (transcription factors such as WRKY, MYB, and NAC). Metabolic flux analysis (13C labeling) can reveal the dynamic allocation of carbon and nitrogen between primary and secondary metabolism. Furthermore, single-cell transcriptomics technology holds promise for resolving the heterogeneous responses of different cell types (guard cells, mesophyll cells, vascular cells) around pathogen infection sites.

(4) Focusing on epigenetic regulation and environmental adaptability: The occurrence of downy mildew is highly dependent on temperature and humidity. Investigating the roles of DNA methylation and histone modifications (H3K4me3, H3K9ac) in resistance induction and memory may reveal epigenetic variation-mediated resistance priming phenomena. Meanwhile, integrating multi-omics analysis of adaptive differences to downy mildew among different grapevine ecotypes will provide a basis for breeding broadly adaptable cultivars.

(5) Exploring the potential of the microbiome and rhizosphere immunity: Grapevine leaves and rhizospheres harbor complex microbial communities, and certain beneficial bacteria can enhance grapevine resistance to downy mildew through induced systemic resistance (ISR). Future research can use physiological and biochemical indicators as tools for evaluating the efficacy of microbial agents and should explore microbiome transplantation to restore resistance.

(6) Promoting the efficient utilization of resistance resources: Chinese wild grapevine resources (Vitis pseudoreticulata, Vitis amurensis) retain abundant resistance genes. It is recommended to systematically evaluate the physiological and biochemical characteristics of these resources (such as PAL induction rate, MDA accumulation threshold, and resveratrol production), combine genome-wide association studies (GWAS) to map superior alleles, and pyramid them into main cultivars through molecular marker-assisted breeding or gene editing.

In conclusion, the field of physiological and biochemical research on grapevine downy mildew resistance has entered a new stage from phenomenological description to mechanistic dissection and integrated application. Multidisciplinary integration (plant physiology, molecular biology, bioinformatics, and microbiomics) will provide a solid foundation for ultimately achieving green and sustainable management of downy mildew.

Abbreviations

The following abbreviations are used in this manuscript:

P. viticola Plasmopara viticola
POD Peroxidase
SOD Superoxide dismutase
SA Salicylic acid
JA Jasmonic acid
MAPK Mitogen-activated protein kinase
PR Pathogenesis-related
PAMPs Pathogen-associated molecular patterns
ROS Reactive oxygen species
MDA Malondialdehyde
PSII Photosystem II
Fv/Fm Photochemical efficiency
NADPH Nicotinamide adenine dinucleotide phosphate (reduced form)
ATP Adenosine triphosphate
NPQ Non-photochemical quenching
Pn Net photosynthetic rate
Tr Transpiration rate
Ci Intercellular CO2 concentration
CAT Catalase
APX Ascorbate peroxidase
PRX Peroxidases
AsA Ascorbate
MDHAR Monodehydroascorbate reductase
DHAR Dehydroascorbate reductase
GR Glutathione reductase
PAL Phenylalanine ammonia-lyase
PPO Polyphenol oxidase
CHT Chitinase
GLU β-1,3-glucanase
DAMPs Damage-associated molecular patterns
STS Stilbene synthase
PKS Polyketide synthase
PTI PAMP-triggered immunity
RBOH Respiratory burst oxidase homolog
CDPKs Calcium-dependent protein kinases
ET Ethylene
SAR Systemic acquired resistance
Open in a new tab

Author Contributions

Conceptualization, S.W. and T.H.; methodology, S.W., T.H. and M.F.; validation, Q.L.; formal analysis, S.W., T.H. and Q.L.; investigation, S.W., T.H., M.F. and Q.L.; resources, N.Z. and L.B.; writing—original draft preparation, S.W., T.H. and Q.L.; writing—review and editing, N.Z. and L.B.; visualization, S.W., T.H. and Q.L.; supervision, N.Z. and L.B.; project administration, N.Z. and L.B.; funding acquisition, N.Z. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

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

Conflicts of Interest

The authors declare no conflicts of interest.

Funding Statement

This research was funded by the Innovation Guidance and Technology-based Enterprise Cultivation Program of the Yunnan Provincial Science and Technology Department, grant number 202404BI090011.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

References

  • 1.Zhang Z., Niu Z., Chen Z., Zhao Y., Yang L. Review of the Pathogenic Mechanism of Grape Downy Mildew (Plasmopara viticola) and Strategies for Its Control. Microorganisms. 2025;13:1279. doi: 10.3390/microorganisms13061279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Sun Z., Song H., Liu Y., Ren Q., Wang Q., Li X., Pan H., Huang X. The Potential of Microorganisms for the Control of Grape Downy Mildew—A Review. J. Fungi. 2024;10:702. doi: 10.3390/jof10100702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Gouveia C., Santos R.B., Paiva-Silva C., Buchholz G., Malhó R., Figueiredo A. The Pathogenicity of Plasmopara Viticola: A Review of Evolutionary Dynamics, Infection Strategies and Effector Molecules. BMC Plant Biol. 2024;24:327. doi: 10.1186/s12870-024-05037-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Wong F.P., Burr H.N., Wilcox W.F. Heterothallism in Plasmopara viticola. Plant Pathol. 2001;50:427–432. doi: 10.1046/j.1365-3059.2001.00573.x. [DOI] [Google Scholar]
  • 5.Perazzolli M., Nesler A., Giovannini O., Antonielli L., Puopolo G., Pertot I. Ecological Impact of a Rare Sugar on Grapevine Phyllosphere Microbial Communities. Microbiol. Res. 2020;232:126387. doi: 10.1016/j.micres.2019.126387. [DOI] [PubMed] [Google Scholar]
  • 6.Gulzar M.W., Maqsood R., Abbas H., Manzoor M., Suleman M., Bajwa H.A., Hamza A., Yar S., Zain M., Wadood A., et al. Use of Insecticides and Their Impact on Viral Diseases in Humans, Animals and Environment. Hosts Viruses. 2024;11:64–77. doi: 10.17582/journal.hv/2024/11.64.77. [DOI] [Google Scholar]
  • 7.Salotti I., Caffi T., Fedele G., Rossi V. Resistant Grapevine Varieties to Downy Mildew. Plant Health Cases. 2024 doi: 10.1079/planthealthcases.2024.0008. [DOI] [Google Scholar]
  • 8.Merdinoglu D., Schneider C., Prado E., Wiedemann-Merdinoglu S., Mestre P. Breeding for Durable Resistance to Downy and Powdery Mildew in Grapevine. OENO One. 2018;52:203–209. doi: 10.20870/oeno-one.2018.52.3.2116. [DOI] [Google Scholar]
  • 9.Samarth R.R., Shetty D., Saha S., Sawant I. Leaf Micro-Morphological Diversity in Vitis Species and Its Association with Resistance to Plasmopara viticola. Res. Crops. 2021;22:334–341. doi: 10.31830/2348-7542.2021.076. [DOI] [Google Scholar]
  • 10.Viret O., Gindro K. Science of Fungi in Grapevine. Springer International Publishing; Cham, Switzerland: 2025. Fungal Diseases of Green Organs; pp. 197–312. [Google Scholar]
  • 11.Han X., Li Y., Wang Z., Li Z., Li N., Li H., Duan X. Identification and Genetic Analysis of Downy Mildew Resistance in Intraspecific Hybrids of Vitis vinifera L. Plants. 2025;14:2415. doi: 10.3390/plants14152415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Du Y., Zhang H., Jia K., Chu Z., Xu S., Tran L.P., Guo J., Li W., Li K. Role of Abscisic Acid-mediated Stomatal Closure in Responses to Pathogens in Plants. Physiol. Plant. 2024;176:e14135. doi: 10.1111/ppl.14135. [DOI] [Google Scholar]
  • 13.Patyka M.V., Khablak S.H., Bondareva L.M., Patyka T.I., Dolia M.M., Spychak V.M., Lykholat Y.V. Bacterial Strategies for Suppression and Evasion of Plant Immunity: Molecular and Cellular Aspects. Regul. Mech. Biosyst. 2025;16:e25139. doi: 10.15421/0225139. [DOI] [Google Scholar]
  • 14.Melotto M., Mecey C., Niu Y., Chung H.S., Katsir L., Yao J., Zeng W., Thines B., Staswick P., Browse J., et al. A Critical Role of Two Positively Charged Amino Acids in the Jas Motif of Arabidopsis JAZ Proteins in Mediating Coronatine- and Jasmonoyl Isoleucine-dependent Interactions with the COI1 F-box Protein. Plant J. 2008;55:979–988. doi: 10.1111/j.1365-313x.2008.03566.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Gahir S., Bharath P., Raghavendra A.S. Stomatal Closure Sets in Motion Long-Term Strategies of Plant Defense Against Microbial Pathogens. Front. Plant Sci. 2021;12:761952. doi: 10.3389/fpls.2021.761952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Alonso-Villaverde V., Boso S., Santiago J.L., Gago P., Martínez M.C. Variability of the Stomata among “Albariño” (Vitis vinifera L.) Clones and Its Relationship with Susceptibility to Downy Mildew. VITIS-J. Grapevine Res. 2015;50:45. doi: 10.5073/VITIS.2011.50.45-46. [DOI] [Google Scholar]
  • 17.Allègre M., Daire X., Héloir M., Trouvelot S., Mercier L., Adrian M., Pugin A. Stomatal Deregulation in Plasmopara viticola—Infected Grapevine Leaves. New Phytol. 2007;173:832–840. doi: 10.1111/j.1469-8137.2006.01959.x. [DOI] [PubMed] [Google Scholar]
  • 18.Zandi P., Schnug E. Reactive Oxygen Species, Antioxidant Responses and Implications from a Microbial Modulation Perspective. Biology. 2022;11:155. doi: 10.3390/biology11020155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Haghpanah M., Namdari A., Kaleji M.K., Nikbakht-dehkordi A., Arzani A., Araniti F. Interplay Between ROS and Hormones in Plant Defense Against Pathogens. Plants. 2025;14:1297. doi: 10.3390/plants14091297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Ji W., Zheng W., Yin H., Mei J., Liu X., Abe-Kanoh N., Rhaman M.S., Qin G., Ye W. Layered Stomatal Immunity Contributes to Resistance of Vitis Riparia against Downy Mildew Plasmopara viticola. J. Exp. Bot. 2026;77:1324–1337. doi: 10.1093/jxb/eraf491. [DOI] [PubMed] [Google Scholar]
  • 21.Xun Z., Qin H., Li F., Yao Z., Xu Y., Wang M., Huang L., Zhu Y., Geng X., Zhao Q. Phenylpropanoid Metabolites from Grape Leaves Contribute to Strong Defense Roles against Downy Mildew Based on Physiological and Transcriptomic Analyses. Front. Microbiol. 2026;17:1805591. doi: 10.3389/fmicb.2026.1805591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Hawk T.E., Li P., Abbas H.M.K., Sultana M.S., Piya S., Coffey N., Öztürk C., Zadegan S.B., Laird S.T., Alazem M., et al. A Highly Conserved SNARE-Associated Protein Enhances Plant Immunity by Regulating Vesicle Trafficking. Plant Biotechnol. J. 2026;24:3426–3440. doi: 10.1111/pbi.70573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Possamai T., Baltenweck R., Wiedemann-Merdinoglu S., Lacombe M.-C., Dorne M.-A., Bareyre M., Griem E., Fuchs R., Bogs J., Duchêne É., et al. Metabolic Biomarker-Based Phenotyping Unveils Quantitative Effects of Plant Resistance and Pathogen Aggressiveness in the Grapevine (Vitis Spp.)—Downy Mildew (Plasmopara viticola) Pathosystem. Plant Stress. 2026;21:101339. doi: 10.1016/j.stress.2026.101339. [DOI] [Google Scholar]
  • 24.Sun L., Wang Y., Zhang J. Calcium Signaling in Plant Defense. New Plant Prot. 2026;3:e70028. doi: 10.1002/npp2.70028. [DOI] [Google Scholar]
  • 25.Das S., Mustafi S., Dan S., Mandal S.N., Sinha P. Chlorophyll Based Downy Mildew Analysis in Cucumber Using Deep Learning. Glob. J. Agric. Innov. Res. Dev. 2025;12:27–38. doi: 10.15377/2409-9813.2025.12.3. [DOI] [Google Scholar]
  • 26.Yang H., Gao T., Li Q., Tan W., Sun X., Wang D., Cao H. Effects of Grape Downy Mildew on Photosynthesis of ‘Red Globe’ Grape Leaves under High Temperature Stress. Int. J. Fruit Sci. 2022;22:581–594. doi: 10.1080/15538362.2022.2084805. [DOI] [Google Scholar]
  • 27.Šebela D., Olejníčková J., Župčanová A., Sotolář R. Response of Grapevine Leaves to Plasmopara Viticola Infection by Means of Measurement of Reflectance and Fluorescence Signals. Acta Univ. Agric. Silvic. Mendel. Brun. 2013;60:229–238. doi: 10.11118/actaun201260080229. [DOI] [Google Scholar]
  • 28.Bellow S., Latouche G., Brown S.C., Poutaraud A., Cerovic Z.G. Optical Detection of Downy Mildew in Grapevine Leaves: Daily Kinetics of Autofluorescence upon Infection. J. Exp. Bot. 2013;64:333–341. doi: 10.1093/jxb/ers338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Kuźniak E., Kopczewski T. The Chloroplast Reactive Oxygen Species-Redox System in Plant Immunity and Disease. Front. Plant Sci. 2020;11:572686. doi: 10.3389/fpls.2020.572686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Sun Y., Gao Y., Wang H., Yang X., Zhai H., Du Y. Stimulation of Cyclic Electron Flow around PSI as a Response to the Combined Stress of High Light and High Temperature in Grape Leaves. Funct. Plant Biol. 2018;45:1038–1045. doi: 10.1071/fp17269. [DOI] [PubMed] [Google Scholar]
  • 31.Zuo G. Non-photochemical Quenching (NPQ) in Photoprotection: Insights into NPQ Levels Required to Avoid Photoinactivation and Photoinhibition. New Phytol. 2025;246:1967–1974. doi: 10.1111/nph.70121. [DOI] [PubMed] [Google Scholar]
  • 32.Nogueira Júnior A.F., Tränkner M., Ribeiro R.V., Von Tiedemann A., Amorim L. Photosynthetic Cost Associated With Induced Defense to Plasmopara viticola in Grapevine. Front. Plant Sci. 2020;11:235. doi: 10.3389/fpls.2020.00235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Wang Y., Shi Q., Du X., Chen T., Taha M.F. Impact of Nitrogen on Downy Mildew Infection and Its Effects on Growth and Physiological Traits in Early Growth Stages of Cucumber. Horticulturae. 2025;11:1182. doi: 10.3390/horticulturae11101182. [DOI] [Google Scholar]
  • 34.Feng B., Li G., Islam M., Fu W., Zhou Y., Chen T., Tao L., Fu G. Strengthened Antioxidant Capacity Improves Photosynthesis by Regulating Stomatal Aperture and Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Activity. Plant Sci. 2020;290:110245. doi: 10.1016/j.plantsci.2019.110245. [DOI] [PubMed] [Google Scholar]
  • 35.Singh S., Kumar V., Parihar P., Dhanjal D.S., Singh R., Ramamurthy P.C., Prasad R., Singh J. Differential Regulation of Drought Stress by Biological Membrane Transporters and Channels. Plant Cell Rep. 2021;40:1565–1583. doi: 10.1007/s00299-021-02730-4. [DOI] [PubMed] [Google Scholar]
  • 36.Formela-Luboińska M., Chadzinikolau T., Drzewiecka K., Jeleń H., Bocianowski J., Kęsy J., Labudda M., Jeandet P., Morkunas I. The Role of Sugars in the Regulation of the Level of Endogenous Signaling Molecules during Defense Response of Yellow Lupine to Fusarium Oxysporum. Int. J. Mol. Sci. 2020;21:4133. doi: 10.3390/ijms21114133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Mahatma M.K., Bhatnagar R., Dhandhukia P., Thakkar V.R. Variation in Metabolites Constituent in Leaves of Downy Mildew Resistant and Susceptible Genotypes of Pearl Millet. Physiol. Mol. Biol. Plants. 2009;15:249–255. doi: 10.1007/s12298-009-0028-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Long X., Guan C., Wang L., Jia L., Fu X., Lin Q., Huang Z., Liu C. Rice Storage Proteins: Focus on Composition, Distribution, Genetic Improvement and Effects on Rice Quality. Rice Sci. 2023;30:207–221. doi: 10.1016/j.rsci.2023.03.005. [DOI] [Google Scholar]
  • 39.Ji Z., Liu Z., Han Y., Sun Y. Exogenous Dopamine Promotes Photosynthesis and Carbohydrate Metabolism of Downy Mildew-Infected Cucumber. Sci. Hortic. 2022;295:110842. doi: 10.1016/j.scienta.2021.110842. [DOI] [Google Scholar]
  • 40.Xiao N., Ma H., Wang W., Sun Z., Li P., Xia T. Overexpression of ZmSUS1 Increased Drought Resistance of Maize (Zea mays L.) by Regulating Sucrose Metabolism and Soluble Sugar Content. Planta. 2024;259:43. doi: 10.1007/s00425-024-04336-y. [DOI] [PubMed] [Google Scholar]
  • 41.Szügyi S., Sárdi É. Connection between the Disease Resistance of Sour Cherry Genotypes and the Carbohydrate Content of the Leaf and Phloem Tissues. Hortic. Sci. 2018;45:181–186. doi: 10.17221/26/2017-hortsci. [DOI] [Google Scholar]
  • 42.Karan R., Prasannakumar M.K., M. K.B., Harish J., Roopashree B., Venkateshbabu G., Patil S.S., Shreedevasena S., Mahesh H.B., Devanna P., et al. Genome and Transcriptome Analyses Reveal Molecular Mechanisms Underlying the Interaction between Plasmopara viticola and Grapevine. Front. Plant Sci. 2026;17:1765002. doi: 10.3389/fpls.2026.1765002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Han W., Zhang X., Hao Y., Sun C., Lin X. Coordinated Regulation of Tomato Sugar Accumulation by Relative Humidity and Field Capacity through Source–Sink–Transport Balance. Front. Plant Sci. 2026;17:1775354. doi: 10.3389/fpls.2026.1775354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Sugiura D., Betsuyaku E., Terashima I. Interspecific Differences in How Sink–Source Imbalance Causes Photosynthetic Downregulation among Three Legume Species. Ann. Bot. 2019;123:715–726. doi: 10.1093/aob/mcy204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Gong P., Kang J., Sadeghnezhad E., Bao R., Ge M., Zhuge Y., Shangguan L., Fang J. Transcriptional Profiling of Resistant and Susceptible Cultivars of Grapevine (Vitis L.) Reveals Hypersensitive Responses to Plasmopara viticola. Front. Microbiol. 2022;13:846504. doi: 10.3389/fmicb.2022.846504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Liu Y., Song Y., Ruan Y. Sugar Conundrum in Plant–Pathogen Interactions: Roles of Invertase and Sugar Transporters Depend on Pathosystems. J. Exp. Bot. 2022;73:1910–1925. doi: 10.1093/jxb/erab562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Wu J., Lu L., Meng Z., Qin Y., Guo L., Ran M., Peng P., Tang Y., Huang G., Li W., et al. Advancements on the Mechanism of Soluble Sugar Metabolism in Fruits. Horticulturae. 2025;11:1001. doi: 10.3390/horticulturae11091001. [DOI] [Google Scholar]
  • 48.Wang Y., Cao X., Han Y., Han X., Wang Z., Xue T., Ye Q., Zhang L., Duan X., Wang H., et al. Kaolin Particle Film Protects Grapevine Cv. Cabernet Sauvignon Against Downy Mildew by Forming Particle Film at the Leaf Surface, Directly Acting on Sporangia and Inducing the Defense of the Plant. Front. Plant Sci. 2022;12:796545. doi: 10.3389/fpls.2021.796545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Liu R., Wang S., Song J. New Progress in the Production, Oxidative Damage, and Scavenging Mechanisms of Reactive Oxygen Species in Plants under Abiotic Stress. Front. Plant Sci. 2026;17:1774033. doi: 10.3389/fpls.2026.1774033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Sun Y., Liu Z., Lan G., Jiao C., Sun Y. Effect Ofexogenous Melatonin on Resistance of Cucumber to Downy Mildew. Sci. Hortic. 2019;255:231–241. doi: 10.1016/j.scienta.2019.04.057. [DOI] [Google Scholar]
  • 51.Lv S., Wei L., Luan X., Khan N., Wang X., Xi Z. Sustainable Control of Grapevine Downy Mildew: 24-Epibrassonolide Triggers Distinct Defense Strategies in Grapevine Cultivars. Physiol. Plant. 2025;177:e70625. doi: 10.1111/ppl.70625. [DOI] [PubMed] [Google Scholar]
  • 52.Nadarajah K.K. Defensive Strategies of ROS in Plant–Pathogen Interactions. In: Verma P.K., Mishra S., Srivastava V., Mehrotra S., editors. Plant Pathogen Interaction. Springer Nature; Singapore: 2023. pp. 163–183. [Google Scholar]
  • 53.Fujita M., Hasanuzzaman M. Approaches to Enhancing Antioxidant Defense in Plants. Antioxidants. 2022;11:925. doi: 10.3390/antiox11050925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Tarfeen N., Nisa Q., Khair-Ul-Nisa, Kahlief K. Antioxidant Defense System in Plants Against Biotic Stress. In: Aftab T., Hakeem K.R., editors. Antioxidant Defense in Plants. Springer Nature; Singapore: 2022. pp. 383–395. [Google Scholar]
  • 55.Bommesh J.C., Pitchaimuthu M., Manjunathagowda D.C., Maragal S., Ramesh A.N. Unveiling the Downy Mildew Disease (Pseudoperonospora Cubensis Berk. & Curt.) Resistance Response in Cucumber (Cucumis sativus L.) Indian Phytopathol. 2025;78:97–104. doi: 10.1007/s42360-025-00825-6. [DOI] [Google Scholar]
  • 56.Hachez C., Besserer A., Chevalier A.S., Chaumont F. Insights into Plant Plasma Membrane Aquaporin Trafficking. Trends Plant Sci. 2013;18:344–352. doi: 10.1016/j.tplants.2012.12.003. [DOI] [PubMed] [Google Scholar]
  • 57.Li W., Qin D., Ma R., Li S., Wang L. Comparative Evaluation of Physiological and Molecular Responses of Blackcurrant Varieties to Powdery Mildew Infection. Front. Plant Sci. 2024;15:1445839. doi: 10.3389/fpls.2024.1445839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Liu J., Lv Y., Li M., Wu Y., Li B., Wang C., Tao Q. Peroxidase in Plant Defense: Novel Insights for Cadmium Accumulation in Rice (Oryza sativa L.) J. Hazard. Mater. 2024;474:134826. doi: 10.1016/j.jhazmat.2024.134826. [DOI] [PubMed] [Google Scholar]
  • 59.Shigeto J., Tsutsumi Y. Diverse Functions and Reactions of Class III Peroxidases. New Phytol. 2016;209:1395–1402. doi: 10.1111/nph.13738. [DOI] [PubMed] [Google Scholar]
  • 60.Veljović Jovanović S., Kukavica B., Vidović M., Morina F., Menckhoff L. Class III Peroxidases: Functions, Localization and Redox Regulation of Isoenzymes. In: Gupta D.K., Palma J.M., Corpas F.J., editors. Antioxidants and Antioxidant Enzymes in Higher Plants. Springer International Publishing; Cham, Switzerland: 2018. pp. 269–300. [Google Scholar]
  • 61.Yang X., Yan S., Li G., Li Y., Li J., Cui Z., Sun S., Huo J., Sun Y. Rice-Magnaporthe Oryzae Interactions in Resistant and Susceptible Rice Cultivars under Panicle Blast Infection Based on Defense-Related Enzyme Activities and Metabolomics. PLoS ONE. 2024;19:e0299999. doi: 10.1371/journal.pone.0299999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Pathak A., Kumar A., Wany A. Hydrogen Peroxide Is a Central ROS Regulator in Plant Immunity. Physiol. Mol. Biol. Plants. 2025;31:2061–2085. doi: 10.1007/s12298-025-01673-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Liang J., Xu M., Yang B., Liu J., Xu Z., Yao X., Lu J., Fu P. Evolutionary Analysis of Ascorbate-Glutathione Cycle Genes across Green Plants with Lineage-Specific Profiling in Grapevine (Vitis vinifera L.) Hortic. Res. 2026;13:uhaf247. doi: 10.1093/hr/uhaf247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Foyer C.H., Kunert K. The Ascorbate–Glutathione Cycle Coming of Age. J. Exp. Bot. 2024;75:2682–2699. doi: 10.1093/jxb/erae023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Yoshimura K., Ishikawa T. Physiological Function and Regulation of Ascorbate Peroxidase Isoforms. J. Exp. Bot. 2024;75:2700–2715. doi: 10.1093/jxb/erae061. [DOI] [PubMed] [Google Scholar]
  • 66.Li C., Li J., Du X., Zhang J., Zou Y., Liu Y., Li Y., Lin H., Li H., Liu D., et al. Chloroplast Thylakoidal Ascorbate Peroxidase, PtotAPX, Has Enhanced Resistance to Oxidative Stress in Populus Tomentosa. Int. J. Mol. Sci. 2022;23:3340. doi: 10.3390/ijms23063340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 67.Nazish T., Huang Y., Zhang J., Xia J., Alfatih A., Luo C., Cai X., Xi J., Xu P., Xiang C. Understanding Paraquat Resistance Mechanisms in Arabidopsis Thaliana to Facilitate the Development of Paraquat-Resistant Crops. Plant Commun. 2022;3:100321. doi: 10.1016/j.xplc.2022.100321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Noctor G., Foyer C.H. ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998;49:249–279. doi: 10.1146/annurev.arplant.49.1.249. [DOI] [PubMed] [Google Scholar]
  • 69.Nehela Y., Killiny N. Revisiting SA Biosynthesis: New Post-PAL Route in Plant Immunity. Trends Plant Sci. 2026 doi: 10.1016/j.tplants.2026.03.011. [DOI] [PubMed] [Google Scholar]
  • 70.Li G., Song C., Manzoor M.A., Li D., Cao Y., Cai Y. Functional and Kinetics of Two Efficient Phenylalanine Ammonia Lyase from Pyrus Bretschneideri. BMC Plant Biol. 2023;23:612. doi: 10.1186/s12870-023-04586-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Boubakri H., Poutaraud A., Wahab M.A., Clayeux C., Baltenweck-Guyot R., Steyer D., Marcic C., Mliki A., Soustre-Gacougnolle I. Thiamine Modulates Metabolism of the Phenylpropanoid Pathway Leading to Enhanced Resistance to Plasmopara viticola in Grapevine. BMC Plant Biol. 2013;13:31. doi: 10.1186/1471-2229-13-31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Fröbel S., Dudenhöffer J., Töpfer R., Zyprian E. Transcriptome Analysis of Early Downy Mildew (Plasmopara viticola) Defense in Grapevines Carrying the Asian Resistance Locus Rpv10. Euphytica. 2019;215:28. doi: 10.1007/s10681-019-2355-z. [DOI] [Google Scholar]
  • 73.Zhao T., Li R., Yao W., Wang Y., Zhang C., Li Y. Genome-Wide Identification and Characterisation of Phenylalanine Ammonia-Lyase Gene Family in Grapevine. J. Hortic. Sci. Biotechnol. 2021;96:456–468. doi: 10.1080/14620316.2021.1879685. [DOI] [Google Scholar]
  • 74.Jeon H.S., Jang E., Kim J., Kim S.H., Lee M.-H., Nam M.H., Tobimatsu Y., Park O.K. Pathogen-Induced Autophagy Regulates Monolignol Transport and Lignin Formation in Plant Immunity. Autophagy. 2023;19:597–615. doi: 10.1080/15548627.2022.2085496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Amin A. Specialized Metabolic Reprogramming in Plant Immunity: Biosynthetic Networks, Spatiotemporal Regulation, and Quantitative Defense. Plants. 2026;15:1424. doi: 10.3390/plants15101424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Wang Y., Liu Y., Huang Y., Hou S., Zhu X., Teng J. Characterization and Inhibition of Plant Polyphenol Oxidase for Quality Preservation in Post-Harvest Processing. Food Rev. Int. 2026:1–23. doi: 10.1080/87559129.2026.2634731. [DOI] [Google Scholar]
  • 77.De Rossi L., Rocchetti G., Lucini L., Rebecchi A. Antimicrobial Potential of Polyphenols: Mechanisms of Action and Microbial Responses—A Narrative Review. Antioxidants. 2025;14:200. doi: 10.3390/antiox14020200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Saini S., Kumar R., Mandhania S., Kumar A., Malik K., Bhambhu M.K., Saini A.K. Genotype-Specific Temporal Shifts in Biochemical Constituents and Antioxidant Enzyme Activity under Macrophomina Phaseolina (Tassi) Goid Stress in Asiatic Cotton (Gossypium Arboreum) J. Plant Pathol. 2026 doi: 10.1007/s42161-026-02131-0. [DOI] [Google Scholar]
  • 79.Zhang J., Sun X. Recent Advances in Polyphenol Oxidase-Mediated Plant Stress Responses. Phytochemistry. 2021;181:112588. doi: 10.1016/j.phytochem.2020.112588. [DOI] [PubMed] [Google Scholar]
  • 80.Sezgin F.G. Defense-Related Enzymes in Plant Disease Resistance: Molecular Regulation and Agricultural Applications. Black Sea J. Agric. 2026;9:323–331. doi: 10.47115/bsagriculture.1868834. [DOI] [Google Scholar]
  • 81.Han Z., Schneiter R. Dual Functionality of Pathogenesis-Related Proteins: Defensive Role in Plants versus Immunosuppressive Role in Pathogens. Front. Plant Sci. 2024;15:1368467. doi: 10.3389/fpls.2024.1368467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.AbuTahon M.A., Aboelmagd H.I., Housseiny M.M., Abdel-Mageed A.M., Daifalla N., Isichei A.C., Algadi S., Ali Y.H., Saeed I.K., Mostafa H.M., et al. Microbial Chitinases—Production, Characterization, Purification and Their Biotechnological and Therapeutic Applications: An Integrated Review. BioResources. 2026;21:2587–2632. doi: 10.15376/biores.21.1.Abu-Tahon. [DOI] [Google Scholar]
  • 83.Llamazares De Miguel D., Mena-Petite A., Corio-Costet M.-F., Nieto J., Fernández-Navarro J.R., Díez-Navajas A.M. Modulation of the Genetic Response in Vitis vinifera L. Against the Oomycete Plasmopara viticola, Causing Grapevine Downy Mildew, Through the Action of Different Basic Substances. Horticulturae. 2026;12:112. doi: 10.3390/horticulturae12010112. [DOI] [Google Scholar]
  • 84.Mahmoud E., Hussien Z.N., Shehata A.G.S.F., Marraiki N., Almanzalawi E., Alqahtani T., Abou-Zeid M., Kamhawy M. Induction and Expression of Systemic Resistance to Downy Mildew Disease in Grapevine by Chitosan. Not. Bot. Horti Agrobot. Cluj-Napoca. 2025;53:14265. doi: 10.15835/nbha53114265. [DOI] [Google Scholar]
  • 85.Mian G., Musetti R., Belfiore N., Boscaro D., Lovat L., Tomasi D. Chitosan Application Reduces Downy Mildew Severity on Grapevine Leaves by Positively Affecting Gene Expression Pattern. Physiol. Mol. Plant Pathol. 2023;125:102025. doi: 10.1016/j.pmpp.2023.102025. [DOI] [Google Scholar]
  • 86.Li Z., Wu R., Guo F., Wang Y., Nick P., Wang X. Advances in the Molecular Mechanism of Grapevine Resistance to Fungal Diseases. Mol. Hortic. 2025;5:1. doi: 10.1186/s43897-024-00119-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 87.Zhu Y., Gao F. Involvement of Pathogenesis-Related Proteins and Their Roles in Abiotic Stress Responses in Plants. Biomolecules. 2025;15:1103. doi: 10.3390/biom15081103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Mijailovic N., Richet N., Villaume S., Nesler A., Perazzolli M., Aït Barka E., Aziz A. D-Tagatose-Based Product Triggers Sweet Immunity and Resistance of Grapevine to Downy Mildew, but Not to Gray Mold Disease. Plants. 2022;11:296. doi: 10.3390/plants11030296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.War A.F., Nanda S.A., Bashir I., Rehmaan S., Sheergojri I.A., Rehman I.U., Reshi Z.A., Rashid I. Plant Phenolics Role in Bacterial Disease Stress Management in Plants. In: Lone R., Khan S., Mohammed Al-Sadi A., editors. Plant Phenolics in Biotic Stress Management. Springer Nature; Singapore: 2024. pp. 217–241. [Google Scholar]
  • 90.Gabaston J., Richard T., Cluzet S., Palos Pinto A., Dufour M.-C., Corio-Costet M.-F., Mérillon J.-M. Pinus pinaster Knot: A Source of Polyphenols against Plasmopara viticola. J. Agric. Food Chem. 2017;65:8884–8891. doi: 10.1021/acs.jafc.7b04129. [DOI] [PubMed] [Google Scholar]
  • 91.Štambuk P., Šikuten I., Karoglan Kontić J., Maletić E., Preiner D., Tomaz I. Leaf Polyphenolic Profile as a Determinant of Croatian Native Grapevine Varieties’ Susceptibility to Plasmopara viticola. Front. Plant Sci. 2022;13:836318. doi: 10.3389/fpls.2022.836318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Santiago A., Pizzio G.A., Romero P., Martínez-Márquez A., Martínez-Esteso M.J., Echeverria J., Selles-Marchart S., Alvarez-Urdiola R., Zhang C., Navarro-Payá D., et al. Integrated Multi-Omics Analyses Reveal That p-Coumaroyl-CoA 2′-Hydroxylases Act Upstream of Stilbene Synthases to Mediate Oxyresveratrol Biosynthesis in Mulberry (Morus alba) Plant Commun. 2026:101751. doi: 10.1016/j.xplc.2026.101751. [DOI] [PubMed] [Google Scholar]
  • 93.Parage C., Tavares R., Réty S., Baltenweck-Guyot R., Poutaraud A., Renault L., Heintz D., Lugan R., Marais G.A.B., Aubourg S., et al. Structural, Functional, and Evolutionary Analysis of the Unusually Large Stilbene Synthase Gene Family in Grapevine. Plant Physiol. 2012;160:1407–1419. doi: 10.1104/pp.112.202705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Vannozzi A., Wong D.C.J., Höll J., Hmmam I., Matus J.T., Bogs J., Ziegler T., Dry I., Barcaccia G., Lucchin M. Combinatorial Regulation of Stilbene Synthase Genes by WRKY and MYB Transcription Factors in Grapevine (Vitis vinifera L.) Plant Cell Physiol. 2018;59:1043–1059. doi: 10.1093/pcp/pcy045. [DOI] [PubMed] [Google Scholar]
  • 95.Xu W., Ma F., Li R., Zhou Q., Yao W., Jiao Y., Zhang C., Zhang J., Wang X., Xu Y., et al. VpSTS29/STS2 Enhances Fungal Tolerance in Grapevine through a Positive Feedback Loop. Plant Cell Environ. 2019;42:2979–2998. doi: 10.1111/pce.13600. [DOI] [PubMed] [Google Scholar]
  • 96.Nicaise V., Candresse T. Plum pox virus Capsid Protein Suppresses Plant Pathogen-associated Molecular Pattern (PAMP)-triggered Immunity. Mol. Plant Pathol. 2017;18:878–886. doi: 10.1111/mpp.12447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Niekerk L., Gokul A., Basson G., Badiwe M., Nkomo M., Klein A., Keyster M. Heavy Metal Stress and Mitogen Activated Kinase Transcription Factors in Plants: Exploring Heavy metal-ROS Influences on Plant Signalling Pathways. Plant Cell Environ. 2024;47:2793–2810. doi: 10.1111/pce.14926. [DOI] [PubMed] [Google Scholar]
  • 98.Lin J., Zhao J., Du L., Wang P., Sun B., Zhang C., Shi Y., Li H., Sun H. Activation of MAPK-Mediated Immunity by Phosphatidic Acid in Response to Positive-Strand RNA Viruses. Plant Commun. 2024;5:100659. doi: 10.1016/j.xplc.2023.100659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Ferrandino A., Pagliarani C., Pérez-Álvarez E.P. Secondary Metabolites in Grapevine: Crosstalk of Transcriptional, Metabolic and Hormonal Signals Controlling Stress Defence Responses in Berries and Vegetative Organs. Front. Plant Sci. 2023;14:1124298. doi: 10.3389/fpls.2023.1124298. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

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

Articles from Plants are provided here courtesy of Multidisciplinary Digital Publishing Institute (MDPI)

RESOURCES