Virus Diseases of Peonies

Abstract

Peonies (Paeonia spp.) are renowned for their beautiful ornamental flowers and significant cultural, medicinal, and economic values. Based on growth habit, peonies are categorized into herbaceous and tree peonies. Viral infections in peonies, historically referred to as “peony ringspot” or “peony mosaic” diseases, have been reported worldwide over decades. Infections symptoms typically include leaf discoloration and diminished flowering, substantially reducing both ornamental and commercial quality. In severe cases, viral diseases can cause stunted plant growth and impaired flowering, directly affecting peony cultivation and the floriculture profitability. This review systematically summarizes the current research on key viral diseases in peonies, addressing disease classification, symptomatology, causative viruses, pathogenesis, molecular virus–host interactions, and contemporary approaches for prevention and management. The insights provided in this review offer a theoretical foundation and practical guidelines to facilitate effective control of peony viral diseases, potentially promoting sustainable development within the peony industry.

1. Introduction

Peonies (Paeonia spp.) are notable for their large, fragrant, and colorful flowers [1], marking them popular in garden landscaping and cut-flower cultivation [2]. Propagation primarily through branching allows peonies to retain desirable horticultural traits across generations, ensuring stable market quality. Currently, more than 25 countries produce cut peonies, with prominent markets located in Europe, Asia, and the USA [3]. The economic value of peonies is especially pronounced in regions with thriving ornamental and floricultural industries.

Peonies are robust, easy to cultivate, and capable of maintaining ornamental quality over a long period. Widely planted in parks and gardens, they hold significant cultural symbolism, especially in China, where they are considered an unofficial national flower, symbolizing wealth and peace [4]. Events such as the Peony Festival and the introduction of novel cultivars attract tourists, thereby boosting local economies [5].

In traditional Chinese medicine, peonies have been utilized therapeutically for over two thousand years. Their flowers contain astragalus, traditionally used for menstrual regulation, while the root bark of tree peonies (P. suffruticosa Andr.), known as Moutan Cortex (CM), is commonly prescribed to improve blood circulation [6]. The total flavonoids derived from leaves of peonies exhibit antioxidant, whitening, and antibacterial properties [7,8]. Seeds from tree and herbaceous peonies contain stilbenes with demonstrated antitumor, anti-inflammatory, and neuraminidase-inhibitory activities [9]. Additionally, peony seed oil is abundant in unsaturated fatty acids of medical significance [10]. These attributes underscore the promising prospects for the comprehensive utilization of peony plant resources.

Unfavorable growth conditions can increase peonies’ susceptibility to diverse viral infections, adversely affecting peonies’ health and ornamental quality. Such infections may lead to leaf lesions, branch deformities, impaired growth, and malformed root systems. Understanding viral pathogens infecting peonies, including their identification, distribution, symptomatology, and physiological effects, is crucial for effective disease management. This review addresses current knowledge on viral pathogens infecting peonies, their associated symptoms, physiological impacts, and molecular mechanisms underlying infections, while also proposing targeted strategies for preventing and managing viral diseases in peony cultivation.

2. Types and Distribution of Viruses Infecting Peonies

Multiple viruses from various taxonomic groups have been identified in peonies. Most known peony-infecting viruses possess positive-sense, single-stranded RNA genomes, with the notable exception of Tomato spotted wilt virus (TSWV, species Orthotospovirus tomatomaculae, genus Orthotospovirus, family Tospoviridae), which has a negative-sense RNA genome. These viruses are classified into multiple taxonomic families and genera, including Virgaviridae (genus Tobravirus, rod-shaped, bipartite), Secoviridae (genus Nepovirus, isometric, bipartite), Bromoviridae (genera Alfamovirus and Cucumovirus, spherical, multipartite; genus Anulavirus, tripartite), Betaflexiviridae (filamentous viruses, such as genera Capillovirus and Citrivirus), and Orthotospovirus (genus Bunyavirus, spherical, tripartite). To date, no DNA viruses have been definitively reported infecting peony. The classification and geographic distribution of significant peony-infecting viruses are summarized below (Table 1).

Tobacco rattle virus (TRV), historically termed peony ringspot virus (PRV), is among the most extensively studied viruses in peonies [11]. Its original designation was based on ringspot symptoms observed in infected plants. According to current virological taxonomy, this pathogen is accurately classified as TRV (genus Tobravirus, family Virgaviridae), a rod-shaped virus possessing a positive-sense RNA genome [12,13]. Electron microscopy reveals two characteristic particle sizes (190 nm and 45–115 nm) [14]. TRV infects a broad range of peonies and has been reported in various regions including the United States, Lithuania, Japan, New Zealand, and China [11,15,16,17].

TSWV, a negative-sense RNA virus, also infects peonies [18]. Known for its exceptionally wide host range exceeding a thousand plant species, TSWV infections in peonies have been documented in Europe and the United States [19].

Alfalfa mosaic virus (AMV, genus Alfamovirus, family Bromoviridae) is a positive-sense RNA virus affecting peonies [20]. AMV has a diverse host range across various ornamentals and crops. In peonies, it was first identified as the cause of mosaic and line-pattern diseases in Italy. Although less prevalent than TRV, AMV infections have been reported in Europe and North America [21].

Cucumber mosaic virus (CMV, genus Cucumovirus, family Bromoviridae), an aphid-transmitted positive-sense RNA virus, has been confirmed to be infecting Paeonia lactiflora plants in France [22]. While cases in peonies remain relatively uncommon, CMV is of particular concern due to its extremely broad host range (over 1000 species) and efficient aphid-mediated transmission.

Other viruses identified in peonies include lychnis mottle virus (LycMoV, genus Stralarivirus, family Secoviridae) [23,24], citrus leaf blotch virus (CLBV, genus Citrivirus, family Betaflexiviridae) [25], and apple stem grooving virus (ASGV, genus Capillovirus, family Betaflexiviridae). Recently, Chinese investigation of diseased tree peonies identified complex co-infections involving cycas necrotic stunt virus (CNSV, genus Nepovirus, family Secoviridae), ASGV, LycMoV, grapevine line pattern virus (GLPV, genus Anulavirus, family Bromoviridae), as well as three novel viruses: peony yellowing-associated virus (genus Citrivirus, related to CLBV), peony betaflexivirus 1 (not yet classified), and peony leafroll-associated virus (genus Ampelovirus, related to grapevine leafroll virus) [23].

Table 1. Peony viral diseases: symptoms, genetic composition, and geographical distribution.

Disease/Symptom	Virus	Genome	Family	Country	References
Latent infections or subtle leaf chlorosis	apple stem grooving virus (ASGV)	+ssRNA	Betaflexiviridae	China	[23]
Stunting, gnarled irregularities	citrus leaf blotch virus (CLBV)	+ssRNA	Betaflexiviridae	USA	[25]
Leaf chlorosis	peony yellowing-associated citri virus (PYaCV)	+ssRNA	Betaflexiviridae	China	[23]
Root galling, stunted growth	amazon lily mild mottle virus (ALiMMV)	+ssRNA	Bromoviridae	USA	[26]
Yellow mosaic and line patterns	alfalfa mosaic virus (AMV)	+ssRNA	Bromoviridae	Italy, USA	[27,28]
Systemic mosaic symptoms	cucumber mosaic virus (CMV)	+ssRNA	Bromoviridae	France	[22]
Leaf rolling and deformation, dwarfism, mosaics	grapevine line pattern virus (GLPV)	+ssRNA	Bromoviridae	China	[23]
Dwarfism, leaf rolling and deformation	grapevine leaf roll-associated virus-3 (GLRaV-3)	+ssRNA	Closteroviridae	Ukraine	[29,30]
Stunted growth, reduced flowering, root galls	gentian kobu-sho associated virus (GKaV)	+ssRNA	Flaviviridae	The Netherlands, USA	[31,32]
Chlorosis, stunting, rosette leaf curl, leaf mottle, tip epinasty and necrosis	cycas necrotic stunt virus (CNSV)	+ssRNA	Secoviridae	USA, Korea, Japan, China New Zealand	[21,23,24,33,34,35,36]
Leaf mottle, chlorosis, stunting	lychnis mottle virus (LycMoV)	+ssRNA	Secoviridae	USA, China	[23,24,37]
Chlorotic rings and mottling	raspberry ringspot virus (RRSV)	+ssRNA	Secoviridae	Finland	[38]
Dwarfed yellow mottling leaves	strawberry latent ringspot virus (SLRSV)	+ssRNA	Secoviridae	Finland	[38]
Necrotic ringspots, chlorosis, stunted growth, smaller and distorted leaves and flowers	tomato spotted wilt virus (TSWV)	-ssRNA	Tospoviridae	USA	[18,19,39]
Yellow ringspots or mosaic patterns on leaves	tobacco rattle virus (TRV)	+ssRNA	Virgaviridae	USA, Japan Lithuania, New Zealand, China, Ohio	[13,14,16,17,20,40,41,42]

The viruses in the table are organized alphabetically first by family classification and then by virus name within each family.

Table 1. Peony viral diseases: symptoms, genetic composition, and geographical distribution.

Disease/Symptom	Virus	Genome	Family	Country	References
Latent infections or subtle leaf chlorosis	apple stem grooving virus (ASGV)	+ssRNA	Betaflexiviridae	China	[23]
Stunting, gnarled irregularities	citrus leaf blotch virus (CLBV)	+ssRNA	Betaflexiviridae	USA	[25]
Leaf chlorosis	peony yellowing-associated citri virus (PYaCV)	+ssRNA	Betaflexiviridae	China	[23]
Root galling, stunted growth	amazon lily mild mottle virus (ALiMMV)	+ssRNA	Bromoviridae	USA	[26]
Yellow mosaic and line patterns	alfalfa mosaic virus (AMV)	+ssRNA	Bromoviridae	Italy, USA	[27,28]
Systemic mosaic symptoms	cucumber mosaic virus (CMV)	+ssRNA	Bromoviridae	France	[22]
Leaf rolling and deformation, dwarfism, mosaics	grapevine line pattern virus (GLPV)	+ssRNA	Bromoviridae	China	[23]
Dwarfism, leaf rolling and deformation	grapevine leaf roll-associated virus-3 (GLRaV-3)	+ssRNA	Closteroviridae	Ukraine	[29,30]
Stunted growth, reduced flowering, root galls	gentian kobu-sho associated virus (GKaV)	+ssRNA	Flaviviridae	The Netherlands, USA	[31,32]
Chlorosis, stunting, rosette leaf curl, leaf mottle, tip epinasty and necrosis	cycas necrotic stunt virus (CNSV)	+ssRNA	Secoviridae	USA, Korea, Japan, China New Zealand	[21,23,24,33,34,35,36]
Leaf mottle, chlorosis, stunting	lychnis mottle virus (LycMoV)	+ssRNA	Secoviridae	USA, China	[23,24,37]
Chlorotic rings and mottling	raspberry ringspot virus (RRSV)	+ssRNA	Secoviridae	Finland	[38]
Dwarfed yellow mottling leaves	strawberry latent ringspot virus (SLRSV)	+ssRNA	Secoviridae	Finland	[38]
Necrotic ringspots, chlorosis, stunted growth, smaller and distorted leaves and flowers	tomato spotted wilt virus (TSWV)	-ssRNA	Tospoviridae	USA	[18,19,39]
Yellow ringspots or mosaic patterns on leaves	tobacco rattle virus (TRV)	+ssRNA	Virgaviridae	USA, Japan Lithuania, New Zealand, China, Ohio	[13,14,16,17,20,40,41,42]

The viruses in the table are organized alphabetically first by family classification and then by virus name within each family.

3. Damage of Peonies Caused by Viruses

3.1. Main Patterns of Infection and Transmission

Virus transmission significantly threatens the sustainable development and commercialization of peony plants. Transmission frequently occurs via biological vectors, primarily nematodes and insects. For example, TRV is transmitted by soil-inhabiting nematodes of the family Trichodoridae. These nematodes acquire viruses from infected roots and inoculate healthy plants through feeding, facilitating viral entry into the root system [43]. Thrips (Frankliniella spp.) serve as persistent vectors for TSWV, carrying the virus throughout their lifecycle and transmitting it efficiently during feeding on healthy plants, thereby accelerating intra- and inter-population virus spread [19]. Aphid-borne viruses, such as CMV, utilize coat protein motifs that briefly adhere to the aphid’s stylet, enabling immediate transmission to plants during exploratory feeding [44]. Viruses can also spread mechanically; for instance, AMV can infect plants through direct contact with infected sap [27].

3.2. Infected Parts and Symptoms

Virus-infected peonies display various symptoms, depending on the infecting virus (Table 1 and Figure 1). One of the most common indicators of viral infection is the foliar patterning, which may manifest as mosaic patterns, mottling, ring spots, or line patterns. Necrotic lesions characterized by brown, dead tissue are also frequently observed. TRV infection results in concentric ring or line patterns of dark green and light green on peony leaves, accompanied by small necrotic spots [13,16,40]. TSWV infection causes chlorotic and necrotic ringspots, often appearing as dark brown or black circular lesions surrounded by yellow halos [15]. It is noteworthy that different viruses can lead to similar leaf patterns. For example, peonies infected with CMV display yellow-green mosaic patches or rings patterns, making accurate diagnosis by symptoms monitoring difficult without laboratory confirmation [22].

Apart from foliar symptoms, virus-infected peonies frequently exhibit growth distortions. Infected leaves become cupped or curled, as commonly termed “peony leaf curl” [25]. Systemic infections could result in the stunting of the entire plant. Peonies with severe virus infections (or certain combinations of viruses) have short, spindly stems and fail to reach their typical height [30]. For example, severe TRV infection could induce severe systemic symptoms, such as leaf deformation, wilting, and stunted growth due to impaired water and nutrient uptake via roots and foliage [14,16]. Similarly, TSWV infection could lead to leaf deformities, stem necrosis, withering, and increased susceptibility to secondary infections [19].

Gentian Kobu-sho-associated virus (GKaV) infection is associated with Lemoine’s disease of peonies (LDP), characterized by root galls and stunted plant growth [31]. Examination of root cross-sections from infected peonies reveals yellow or brown inclusions within the abnormally swollen areas, indicative of virus-induced tissue degeneration and the accumulation of viral products and phenolic compounds. These systemic infections extend beyond foliage, affecting subterranean tissues and severely disrupting normal root growth and nutrient storage [31], directly reducing ornamental quality.

Peony viral diseases usually do not induce symptoms on flowers, but could affect flowering quality by impacting leaves, and the growth of plants. In extreme scenarios, severely infected peony plants may produce fewer or no flower buds, as observed in LDP. This condition, characterized by dwarfing, extremely thin shoots, and failure to flower, has been associated with complex infections involving multiple viruses [26].

Some infected peonies are symptomless carriers, showing no obvious outward symptoms despite harboring viruses (as documented for certain peonies infected by TRV, cycas necrotic stunt virus, or SLRSV). Environmental stressors and co-infections can exacerbate symptom severity compared to single-virus infections, leading to intensified symptoms such as severe chlorosis, pronounced growth suppression, and impaired flowering [20].

4. Molecular Mechanisms of Viral Action

4.1. Molecular Structure of the Viruses

Understanding how viruses interact with host cellular machinery to replicate and spread is crucial for developing accurate detection and control strategies specific to peony viral diseases. Techniques such as electron microscopy and nucleotide sequencing have advanced the characterization of these viral pathogens.

TRV possesses a bipartite positive-sense single-stranded RNA genome composed of RNA-1 and RNA-2 segments [40]. Replication involves synthesizing complementary negative-sense RNA intermediates by RNA-dependent RNA polymerase (RdRp), encoded by RNA-1. These negative strands then serve as templates for generating new genomic positive-sense RNA molecules [13]. TRV exhibits complex gene expression, with RNA-1 encoding replication-associated proteins and RNA-2 coding for movement and coat proteins necessary for viral assembly and dissemination [45,46]. The positive-sense RNA segments directly function as mRNA in the host cell, ensuring coordinated gene expression critical for successful replication and systemic spread [47].

TSWV has enveloped spherical virions approximately 80 to 120 nm in diameter with a tripartite negative-sense RNA genome composed of small (S), medium (M), and large (L) segments. Viral replication involves using negative-sense RNA templates to synthesize positive-sense complementary RNAs, facilitated by viral RdRp encoded by the L segment. These positive-sense RNAs serve as templates for viral genome replication and as mRNAs for protein synthesis [48]. The virus envelope, derived from the host plasma membrane, includes glycoproteins G1 and G2, responsible for binding the virus to target cells [49]. TSWV RNA segments form ribonucleoprotein complexes within the envelope, essential for viral transcription and replication. Additionally, the ambisense coding strategy of TSWV allows expression from both strands of RNA, further contributing to its biological complexity [19].

Current research on viruses infecting peonies has primarily focused on their identification, while studies on their molecular mechanisms and pathogenesis remain relatively limited. Therefore, this article selects two well-characterized viruses as examples to illustrate their molecular structures.

4.2. Molecular Mechanism of Interaction Between Virus and Host Plants

Plant viruses are obligate intracellular parasites dependent on the host cellular machinery for replication [50]. Upon entry into host cells (through vector feeding, mechanical injury, or during meristematic cell division), viruses release their genomic material and exploit host translational mechanisms. The virus forms replication complexes on cellular membranes (often deriving from the endo-plasmic reticulum or chloroplast membranes), creating viral factories within the host cell. Viral infections result in exponential accumulation of viral genomes and proteins, subsequently assembled into new infectious virions, which spread systemically throughout the plant. Viruses produce specialized proteins facilitating intercellular movement by altering plasmodesmata, which are the microscopic channels connecting plant cells. For instance, movement proteins from nepoviruses or tobraviruses may form a tubular structure through plasmodesmata, creating conduits for viral RNA passage into adjacent cells [51].

Unlike animals, plants lack an adaptive immune system and do not produce antibodies against viruses. Instead, plant defense is based on innate molecular mechanisms in each cell. The primary antiviral defense is RNA silencing [52]. When detecting viral double-stranded RNA or aberrant RNA structures, host Dicer-like enzymes cleave these molecules into small interfering RNAs (siRNAs). These siRNAs, incorporated into RNA-induced silencing complexes (RISC), target complementary viral RNAs for degradation, thereby suppressing viral replication [53]. The accumulation of virus-derived siRNAs within infected tissues is indicative of this defense response [23,54]. Viruses, however, counteract host defenses using silencing-suppressor proteins. For example, the 2b protein of CMV binds siRNAs, facilitating systemic infection and symptom development [55], while TSWV produces an NSs protein functioning as a silencing suppressor [56]. The interplay between viral suppressors and host RNA silencing determines the outcome of infection—ranging from asymptomatic persistence to severe symptom expression.

In addition to RNA silencing, plants may possess specific resistance (R) genes recognizing viral components, triggering localized defense responses such as hypersensitive responses (HR), characterized by programmed cell death that limits virus spread. While no specific antiviral R genes have yet been formally identified in peonies, resistance is inferred from observations of certain cultivars exhibiting minimal symptoms and maintained vigor despite virus presence [35]. Conversely, highly susceptible cultivars display pronounced viral symptoms and reduced growth [31]. Investigating the molecular basis of such resistance represents an important area for future research and breeding programs aimed at developing virus-tolerant peony cultivars.

Despite extensive studies on virus–host interactions in model plants like Arabidopsis and tobacco, no molecular mechanisms have been characterized in peonies. However, conserved pathways such as RNA silencing or resistance (R) gene-mediated responses may operate in peonies. Investigating these mechanisms could unlock innovative strategies for enhancing viral resistance in this economically vital ornamental species.

5. Virus Quarantine and Control

5.1. Detection Methods of Virus Infection

Early and accurate diagnosis of viral infections in peonies is critical for effective disease management, enabling timely quarantine measures to prevent further spread. Common diagnostic methods include visual inspection, serological assays, and molecular techniques, each with distinct advantages and limitations.

Visual inspection is a practical initial diagnostic method, with characteristic symptoms such as ringspots, chlorosis, necrosis, and stunted growth serving as critical indicators. Despite its simplicity, visual diagnosis is limited by the occasional asymptomatic phase of infections and the frequent overlap of viral symptoms with those caused by nutrient deficiencies or environmental stress, potentially leading to misdiagnosis [20,57].

Serological methods, particularly enzyme-linked immunosorbent assay (ELISA), are widely adopted due to their specificity, sensitivity, and ease of use. ELISAs detect viruses through antibody-mediated recognition of viral coat proteins, indicated by colorimetric reactions upon binding. Commercial ELISA kits for common peony pathogens such as TRV and TSWV are widely available, offering practical diagnostic tools for growers [58,59]. Another serological method is immunosorbent electron microscopy (ISEM), which combines serological techniques with electron microscopy. In ISEM, virions are captured from suspensions on a grid by virion-specific antibodies and then examined using an electron microscope. This approach allows researchers to see the morphology of the virus and thereby confirm that infection has occurred [60].

Compared to traditional methods, molecular diagnostics offer greater sensitivity and specificity in detecting viral infections in peonies. Polymerase chain reaction (PCR) techniques, including reverse transcription PCR (RT-PCR) and quantitative real-time PCR (qPCR), are highly effective for detecting minute quantities of viral nucleic acids. RT-PCR, specifically beneficial for RNA viruses, synthesizes complementary DNA (cDNA) from viral RNA templates, which are then amplified. Real-time PCR further provides quantitative data, enabling precise assessment of viral load within plant tissues [61]. Next-Generation Sequencing (NGS) techniques offer comprehensive genomic characterization, facilitating identification and monitoring of both known and novel viral strains, thus informing surveillance programs and targeted disease management strategies [62]. Transcriptome and small RNA sequencing technologies also facilitate discovery of novel viral pathogens co-infecting symptomatic peonies [23]. Continuous updates and standardization of these assays are critical to match evolving viral strains.

Combining multiple diagnostic methods, including visual inspection, serological assays, and molecular techniques, into integrated systems enhances diagnostic accuracy and reliability. For instance, initial visual screenings and serological tests can be confirmed and further characterized by PCR-based assays. Automated, high-throughput screening systems permit rapid analysis of large sample volumes, benefiting commercial production and phytosanitary programs by rapidly identifying infection hotspots and enabling targeted interventions [57].

5.2. Specific Methods for Preventing and Controlling Virus Infection in Peonies

Effective management of viral diseases in peonies requires integrated strategies combining cultural practices, biological and chemical controls, resistant cultivars, and biochemical approaches (Figure 2). These strategies collectively maintain plant health, ornamental value, and economic viability of peony production.

One possible method is utilizing cultural practices: cultural practices are critical for limiting virus introduction and spread. Optimal irrigation, balanced fertilization, and appropriate planting density promote robust plant growth, reducing susceptibility and enhancing recovery following viral infection. Crop rotation and intercropping with diverse plant species disrupt the life cycles of viral vectors and pathogens, mitigating infection risks. Additionally, it is crucial to avoid reusing contaminated soil or plant debris, promptly remove symptomatic plants, utilize certified virus-free planting materials, and consistently manage weed populations to minimize vector habitats [57].

Routine disinfection during horticultural activities significantly limits mechanical transmission of viruses. For example, peonies should be pruned and carefully treated with disinfection methods throughout the planting period. Tools should be sterilized with effective disinfectants such as 10% bleach or 70% ethanol in order to prevent the mechanical spread of viruses during subsequent horticultural activities. Regular plant monitoring facilitates early identification and prompt removal of infected tissues, with removing infected plants being a crucial step in preventing disease spread [57]. The timing of diseased tissue removal is also important, as many viruses persist in residual plant debris and soil, posing risks of reinfection. Conducting comprehensive cleanup in autumn, including the removal of fallen leaves, plant residues, and weeds harboring viruses or vectors, significantly reduces disease incidence in subsequent growing seasons [19].

Biological control is a further possible method: utilizing beneficial insects offers an effective biological strategy for managing vectors of peony viruses. Natural predators, such as lady beetles and lacewings, can reduce populations of insect vectors, particularly thrips (Frankliniella spp.), which transmit TSWV [19,39]. Additionally, aphid vectors (Aphidoidea spp.) can be suppressed through biological control agents such as predatory ladybird beetles (Coccinellidae) and green lacewing larvae (Chrysoperla spp.), which actively prey on aphid colonies across all developmental stages [63]. The parasitic wasp Aphidius colemani further enhances suppression by targeting aphids for oviposition, leading to host mortality. Importantly, aphid-transmitted viruses like CMV require sustained aphid feeding for transmission, and reducing aphid populations through these natural enemies disrupts viral spread [64,65].

Moreover, chemical treatments can be utilized: viral vectors can also be controlled with chemical treatments to reduce the chance of infection. Systemic insecticides, including imidacloprid and acetamiprid, are particularly effective if the vectors are piercing–sucking mouthpart insects (e.g., aphids, thrips). Foliar insecticides such as Spinosad or pyrethroids also effectively target mobile life stages of vectors, reducing their populations and consequently lowering infection pressure [66].

Another method is the breeding of peonies with antiviral traits: selecting resistant peony cultivars through traditional breeding and biotechnological methods is a long-term and sustainable approach to manage viral infections in peonies [5]. Resistant cultivars can reduce virus replication, limit virus spread within the plant, or minimize susceptibility to vector-mediated transmission. Selecting and propagating peonies exhibiting fewer symptoms or reduced viral loads enhances overall population resistance, decreasing dependence on chemical interventions and improving crop resilience [67].

Biotechnological interventions can also be undertaken: advancements in biotechnology offer powerful tools for enhancing peony resistance to viruses. Genetic engineering techniques can introduce antiviral genes encoding proteins that inhibit viral replication or movement. RNA interference (RNAi), which employs small interfering RNAs (siRNAs) to degrade specific viral RNAs, has successfully enhanced virus resistance in other plant species and has similar potential in peonies [68].

CRISPR-Cas9 genome editing offers another promising way for enhancing virus resistance by precisely editing peony genomes. CRISPR-Cas9 is used to disrupt host susceptibility genes targeted by virus effectors and over-express resistance genes for plant immunity [69]. It could largely increase plant immunity and provide a flexible, accurate method for developing virus-resistant peony cultivars.

Induced resistance methods are also an option: induced resistance in peonies involves pretreatment with specific chemical or biological agents that activate systemic acquired resistance (SAR) or induced systemic resistance (ISR) pathways. The application of plant activators, such as salicylic acid (SA), jasmonic acid (JA), or various plant-derived extracts, can prime peonies’ defense responses against viral pathogens [70]. These activators, applied as foliar sprays or soil treatments, enhance innate immunity and enable plants to more effectively detect and respond to subsequent viral challenges.

In addition, microbial inoculants can be used: beneficial microbes, including mycorrhizal fungi and rhizobacteria, could enhance the resistance of plants to viral pathogens [71]. Moreover, rhizobacteria microbiomes have co-evolved with their hosts to optimize nutrient acquisition and immune responses [72]. Beneficial microbes further promote plant growth and enhance plant resistance to pathogens [73]. For example, beneficial microorganisms such as those found in rhizosphere inoculants contribute to robust plant-microbe mutualism, providing additional defense mechanisms against viral infections when applied to soil or seeds [74]. These beneficial microorganisms have the potential to be utilized for the prevention and control of peony virus diseases.

To summarize, effective management of viral infections in peonies requires an integrated approach, incorporating cultural practices, biological control methods, targeted chemical treatments, and resistant cultivar utilization. The successful application of these combined strategies can significantly reduce viral damage, preserve peony health and ornamental value, and support sustainable economic returns within the floriculture industry.

6. Discussion

Future studies aimed at improving viral disease management in peonies should prioritize elucidating the molecular mechanisms underlying virus-induced symptomatology, identifying viral pathogenicity determinants, and developing novel strategies for disease control. Enhanced research on virus–host interactions in peonies is essential for identifying molecular targets for targeted intervention. Further exploration into the detailed processes by which viruses enter host cells, assemble replication complexes, and systemically spread through plant vasculature is needed. Emerging techniques such as cryo-electron microscopy (cryo-EM) and single-molecule imaging can reveal atomic-level details of these intricate viral-host interactions [75,76].

Increased attention should be given to studies of viral proteins and their interactions with host cellular components, facilitating the identification of host factors exploited or antagonized during viral infection. For example, understanding how TRV manipulates host ribosomes for viral protein synthesis could inform the development of inhibitors to disrupt such critical interactions [6]. Investigating host membrane structures involved in viral replication complex assembly may also yield promising targets for antiviral strategies.

Moreover, comprehensive identification of viral pathogenicity genes and host-defense suppressors remains crucial. Combining transcriptomics and proteomics will provide holistic insights into molecular disruptions caused by viral infections. Profiling gene expression in infected peonies can clarify how viral proteins manipulate host signaling pathways to evade immune defenses and facilitate viral replication [77]. Detailed characterization of viral effectors that suppress plant immunity could lead to novel approaches for engineering virus-resistant peonies or developing chemical inhibitors targeting essential virus–host interactions.

Additionally, the development of innovative virus control strategies beyond traditional breeding and chemical applications is an important research area. RNA interference (RNAi)-based antiviral treatments present a promising option, capable of targeting viral RNA at specific stages in its life cycle, thereby preventing virus replication. RNAi-mediated control strategies may involve topical application of virus-specific siRNAs or transgenic plants engineered to constitutively express these antiviral molecules, offering environmentally sustainable disease management alternatives [68,78].

Further refinement of integrated pest management strategies that combine cultural, biological, and chemical approaches is essential [79]. Grower education on integrated control tactics and practical implementation guidelines will be instrumental for successful disease management. Continued research into virus infection mechanisms, functional characterization of viral pathogenic genes, and innovative management strategies will enhance peony health, ornamental value, and productivity, reinforcing their economic and cultural significance.