From Infection to Adaptation: Sclerotium rolfsii-Induced Stress and Defense in Tomato

Abstract

Tomato (Solanum lycopersicum) is a globally important horticultural crop, with Asia contributing 60.45% of total production, followed by the Americas at 13.36%. Tomato productivity is increasingly constrained by southern blight, a destructive disease responsible for yield losses ranging from 30 to 90% and annual economic damage of $10–20 million. The causal pathogen, Sclerotium rolfsii, infects the stem base and induces reddish-brown cankers through secretion of oxalic acid (OA) and cell wall-degrading enzymes, which girdle tissues, impair water transport, and result in rapid plant wilting and death. Its persistence in soil via sclerotia, broad host range, and adaptability make the disease difficult to manage. Recent advances in genomics, transcriptomics, proteomics and other multi-omics approaches have substantially improved understanding of pathogen virulence factors, host defense responses and disease epidemiology. These studies have revealed key roles of OA, carbohydrate-active enzymes, effector proteins, and sclerotial melanization in pathogenesis, while highlighting the activation of salicylic acid (SA)-, jasmonic acid (JA)-, and ethylene (ET)-mediated defense pathways in tomato. Although cultural, biological, and chemical measures are available, these measures often provide inconsistent protection when used alone. Promising strategies include the use of biocontrol agents, hypovirulence-inducing mycoviruses, and chemical fungicides such as carboxamides and quinone outside inhibitors (QoIs), though fungicide resistance remains a risk factor. Integrated Disease Management (IDM) approaches, such as combining biocontrol agents with fungicides, demonstrate enhanced efficacy. This review also evaluates progress in resistance breeding, grafting, RNA interference (HIGS and SIGS), CRISPR-based genome editing, and exploitation of wild genotypes for durable resistance. Furthermore, emerging precision agriculture tools, including hyperspectral imaging, machine learning-assisted disease detection and climate-resilient management strategies, were discussed as new components of sustainable disease management.

1. Introduction

Tomato (Solanum lycopersicum L.) is one of the most important horticultural crops worldwide, with global production reaching approximately 188.50 million tons in 2024 [1]. Tomatoes are highly versatile and can be consumed in various ways. They can be eaten fresh in salads, cooked in a wide range of dishes, or blended into juices. Due to their distinct flavor, tomatoes frequently serve as the foundation for sauces and contribute both sweetness and acidity to numerous recipes around the world [2]. The value of tomatoes goes beyond their widespread culinary use and rich nutritional content; they also have significant industrial applications and potential benefits for agricultural sustainability (Figure 1). Industrially, tomatoes are processed into concentrated products such as paste and purée, canned products such as peeled tomatoes, and tomato-derived ingredients, including lycopene-rich extracts used as natural antioxidants in foods and as bioactive ingredients in cosmetic formulations [3,4,5].

Tomatoes may offer several health benefits, mainly due to lycopene and other nutrients like fibre, vitamin C, and phenolics. They may help reduce cancer risk, support heart health, protect the brain and skin, improve gut health, reduce inflammation, aid exercise recovery, support immunity, and lower infertility risk [6]. This comprehensive nutrient profile highlights the significant role of tomatoes in supporting human health and balanced diets (

Table 1. Nutrient composition of a small tomato (91 g), highlighting its contribution to human health and dietary balance (Source: The table was constructed using the data of Cervoni [10].

Nutrient	Amount	Remarks
Calories	16 kcal	73% from carbs, 18% from protein, 9% from fat
Carbohydrates	3.5 g	Includes sugars and fiber
Sugars	2.4 g	Naturally occurring
Fiber	1.1 g	Supports digestive health
Protein	0.8 g	Low protein content
Fat	0.2 g	Very low fat
Sodium	5 mg	Low sodium level
Potassium	215.7 mg	Supports heart and muscle function
Vitamin C	12.5 mg	Powerful antioxidant, boosts immunity
Vitamin K	7.2 µg	Essential for blood clotting and bone health
Vitamin A	38.2 µg	Important for vision and immune function
Folate (Vitamin B9)	13.7 µg	Supports DNA synthesis and pregnancy health
Beta-carotene	408.6 µg	Precursor of vitamin A, antioxidant
Lycopene	2341.4 µg	Antioxidant linked to heart and cancer protection
Vitamin E	0.5 mg	Protects cells from oxidative damage

). In addition to its dietary value, tomato residues and byproducts can be valorized as compost, soil amendments, or bioactive extracts to improve soil fertility, enhance soil enzyme activity and beneficial microbial communities, and provide tomatine-rich compounds with potential biocidal properties, thereby supporting sustainable agricultural practices [7,8,9].

Despite its global importance, tomato production is threatened by diverse biotic stresses, particularly infectious diseases caused by fungi, bacteria, viruses, oomycetes, and nematodes, which can severely reduce yield and fruit quality [11]. Among these diseases, Southern blight, caused by Sclerotium rolfsii syn. Athelia rolfsii, is a soil-borne disease destructive under warm and humid conditions, causing severe plant mortality and yield losses and is widely distributed in tropical and subtropical regions, [12,13]. This pathogen causes serious losses in tomato and other solanaceous crops, with yield reductions ranging from 30% to 90% and annual economic damage estimated at $10–20 million under favorable conditions [14,15]. Its broad host range, rapid disease development, abundant sclerotia production, and long-term survival in soil make management difficult and allow the pathogen to persist between cropping cycles [16,17].

Although recent molecular and multi-omics studies have improved our understanding of the genetic diversity, pathogenicity, virulence factors, and stress tolerance mechanisms of S. rolfsii [18,19], key research gaps remain. The molecular basis of host resistance is poorly defined, limiting breeding for resistant tomato cultivars. Current management practices, including fungicides, soil solarization, and crop rotation, are often costly, inconsistent, and environmentally unsustainable [20,21]. Although omics and mycovirus research have advanced, their application to field-ready management remains limited [22]. Climate change may further intensify disease pressure, yet climate-resilient strategies are scarce. Moreover, existing reviews rarely integrate multi-omics, precision agriculture, and socio-economic perspectives, limiting translation into practical solutions.

While previous reviews on S. rolfsii have mainly emphasized pathogen morphology, disease biology, and conventional management strategies, limited attention has been given to the integration of recent molecular, digital, and climate-resilient approaches for southern blight management in tomato. This review addresses this gap by synthesizing current knowledge across four interconnected areas. First, it integrates recent molecular and multi-omics evidence to explain how tomato defense networks respond to fungal virulence factors, including carbohydrate-active enzymes and oxalic acid. Second, it evaluates emerging genetic and molecular tools, including HIGS, SIGS, and CRISPR-Cas, as potential strategies for improving host resistance. Third, it links precision agriculture tools, such as spectral diagnostics and machine learning-based disease detection, with pre-symptomatic surveillance and field-level decision-making. Finally, it considers practical adoption challenges, including economic scalability, digital literacy, and low-cost technologies suitable for smallholder production systems. By connecting molecular mechanisms, advanced breeding and engineering tools, digital diagnostics, and farmer-oriented management practices, this review provides an updated framework for sustainable integrated disease management of southern blight in tomato.

2. Global Trends in Tomato Production and the Threat of Sclerotium rolfsii

Although tomato is produced worldwide, Asia is the dominant producing region, accounting for 60.45% of global tomato production (Figure 2A). This leading share is mainly associated with major producers such as China and India, where suitable climatic conditions, large cultivation areas, and strong domestic demand support extensive tomato farming. The Americas contribute 13.36%, with major producers such as the United States of America (USA), Mexico, and Brazil playing crucial roles in both domestic consumption and international trade. Africa contributes 13.99%, followed by Europe at 11.93%, indicating the broad global distribution of tomato production [1]. At the country level (Figure 2B), China is the largest tomato producer by a wide margin, producing 61.70 million tons, followed by India with 21.32 million tons, Türkiye with 14.62 million tons, and the United States of America (USA) with 10.68 million tons. Other important producers include Egypt (7.52 million tons), Italy (6.02 million tons), Spain (4.57 million tons), Mexico (4.42 million tons), Brazil (4.41 million tons), and Nigeria (3.71 million tons), highlighting the global importance of tomato cultivation across different continents.

As the global population grows, demand for tomatoes continues to rise, with worldwide production reaching an estimated 188.50 million tons in 2024 [1]. Meeting the increasing demand for tomatoes is becoming increasingly challenging due to various agricultural constraints, especially biotic stresses, with plant pathogens posing a significant threat to crop yield and quality. Diseases caused by bacteria, fungi, and viruses are established as the leading cause of economic and production losses in tomato cultivation [11,23]. Without adequate crop protection, it is estimated that such diseases, excluding those caused by viruses, can reduce potential tomato yields by up to 40% worldwide [24], while losses due to viral diseases are estimated to be around 2–5% annually [25]. According to the FAO, plant diseases are responsible for 20–40% of global crop losses, resulting in approximately $220 billion in economic damage annually [26].

Among the various tomato diseases, Southern blight caused by S. rolfsii is particularly worrisome. The name “Southern blight” originated from the disease’s first formal description in the southern USA in 1928, where it was most prevalent under warm and humid climatic conditions [27]. Although first reported from the southern USA, the disease is now distributed worldwide across tropical and subtropical regions, particularly in Asia, Africa, and South America [14,15]. The disease exhibits exceptional aggressiveness on solanaceous crops such as tomato, pepper, and eggplant, where yield losses range from 30 to 90% under favorable conditions [14,28]. In tomato alone, field surveys in India, Bangladesh, and Nigeria have documented average incidence levels of 25–65%, leading to productivity losses exceeding $10–20 million annually [15]. These losses are markedly higher than those caused by other soilborne fungi such as Pythium spp. or Phytophthora spp., which typically account for 10–30% yield reduction under similar environmental conditions [29,30]. Although S. rolfsii produced seedling collapse within 5–7 days in the present inoculation assay, consistent with reported southern blight symptom development in tomato [12,31], Phytophthora infestans should be regarded as the more aggressive epidemic pathogen because late blight can complete repeated disease cycles rapidly under favorable conditions and cause severe crop destruction within a short period [32,33].

Furthermore, the broad host range (over 500 plant species from >100 families) of S. rolfsii facilitates continuous survival between cropping cycles, allowing it to outcompete more host-specific pathogens like Phytophthora or Pythium [17]. The broad host range and rapid disease cycle of this pathogen, along with its ability to produce a high number of sclerotia (up to 400–600 per Petri plate within 15 days) and its persistence in soil for up to 7 years [16], give S. rolfsii a clear epidemiological advantage over other necrotrophic soilborne pathogens.

Recent molecular studies have significantly advanced understanding of the genetic variability and pathogenicity of S. rolfsii. Molecular characterization has revealed the existence of substantial intraspecific diversity across isolates from different crops and agro-ecological regions [17,18]. Multi-omics analyses have further identified roles for various virulence factors in enhancing pathogenesis, stress tolerance, survival, and hyphal development [34,35]. Concurrently, epidemiological factors, particularly rising soil temperatures and erratic rainfall, show a significant impact on expanding the pathogen’s distribution and prolonging sclerotia survival, thereby intensifying its effects on agriculture [36,37].

3. The Biology and Survival of Sclerotium rolfsii

Southern blight is a destructive soilborne disease caused by the necrotrophic basidiomycetous fungus S. rolfsii Sacc. [teleomorph: Athelia rolfsii], affecting potato, tomato, and many other crops. Its persistence and pathogenicity are mainly linked to rapid mycelial growth and abundant sclerotia production, especially under warm and moist conditions [12,19]. In culture, S. rolfsii grows rapidly on potato dextrose agar (PDA), producing white, radiating, cottony, or compact colonies within a few days of inoculation. Fast-growing isolates may reach 90 mm colony diameter within 3 days, whereas moderately growing isolates may reach 70–81 mm by 6 days; sclerotia may form between 7 and 20 days depending on isolate and incubation conditions [38] (Figure 3). Other studies also reported white-to-brown mycelia, compact or cottony colony texture, and numerous brown sclerotia on PDA [39,40].

Beyond its impact on tomato production, S. rolfsii Sacc. [syn. Agroathelia rolfsii] is a highly adaptable soilborne pathogen with an exceptionally broad host range [12,41]. The pathogen was reported to infect more than 500 plant species across about 100 botanical families, including economically important vegetables, legumes, cereals, ornamentals, and cash crops [42,43]. This broad host range is important for tomato production because alternative host plants and infected crop residues can help maintain pathogen inoculum in soil between tomato cropping seasons; S. rolfsii also survives for long periods as sclerotia in soil or diseased debris [12,44]. Sclerotia are the key survival structures of S. rolfsii. The fungus mainly survives and spreads through these structures, which serve as persistent survival bodies and primary inoculum in soil. Although Athelia rolfsii is recognized as the teleomorphic sexual stage, it is rarely observed in nature [19,40]. During maturation, melanin accumulates in the sclerotial rind, reducing cell permeability and protecting the pathogen from UV radiation, oxidative stress, and enzymatic degradation by the pathogen itself or antagonistic microorganisms [45]. Melanin biosynthesis occurs mainly through the 1,8-dihydroxynaphthalene pathway and is regulated by phosphorylation-dependent signaling pathways [46]. Evidence also suggested an alternative L-dihydroxyphenylalanine pathway derived from tyrosine oxidation [47]. Tyrosinases, which are involved in fungal browning and pigmentation, became active during sclerotial initiation and were associated with the onset of pigmentation [48]. Thus, sclerotial development involves coordinated morphological and biochemical changes controlled by environmental cues [47].

As sclerotia mature, their melanin content increases. Melanin may constitute about 13.9% of the sclerotial wall, and its accumulation is associated with lipid peroxidation and stress adaptation [49]. Oxidative stress can further stimulate melanin biosynthesis and sclerotial maturation, with reactive oxygen species acting as signals for pigment formation and environmental resilience [50]. Light and aeration also stimulate sclerotial formation in vitro, showing that environmental conditions influence sclerotial formation, pigmentation, maturation, and long-term survival [51]. When conditions become favorable, mature sclerotia germinate and initiate infection. Germination and growth are promoted by warm, moist, and well-aerated soil. Volatile compounds, including δ-cadinene and cis-calamenene, have been associated with S. rolfsii sclerotia, although their exact role in germination should be interpreted cautiously [52].

Environmental conditions strongly influence both growth and survival. Optimal hyphal growth generally occurs at 30–35 °C, with maximum growth near 30 °C, while little or no growth occurs at 5 °C and 40 °C [53,54]. Sclerotial production is often highest around 25 °C and declines outside the optimum range [53]. Although mycelium rarely survives freezing, sclerotia can remain viable for long periods in colder climates [14]. Soil pH also affects growth and sclerotial formation: S. rolfsii grows across pH 3–9, with optimal mycelial growth around pH 6–7 and sclerotial production commonly favored at pH 4–7 [55]. However, optimum pH varies among isolates, and the pathogen can still germinate and cause disease in acidic or alkaline soils [56]. In the field, dissemination occurs through infested soil during tillage, contaminated tools and machinery, infected seedlings, flood irrigation, and infected crop residues [57]. A small fraction of sclerotia may also survive passage through sheep and cattle, allowing possible spread through manure and organic fertilizers [58].

4. Signs, Symptoms and Disease Development of Southern Blight

Southern blight can cause serious yield losses when susceptible host tissues coincide with favorable environmental conditions [59]. In tomato, infection usually begins at the collar or crown region near the soil surface, especially from the seedling to early vegetative stages, because these tissues are in direct contact with infested soil [60] (Figure 4A). Initial symptoms appear as small, water-soaked lesions that rapidly expand and girdle the stem [14]. The lower stem or crown may become partially rotted, although decay does not always extend through the entire crown [57]. Depending on disease severity, plants may collapse quickly or survive with partial wilting. In mature tomato plants, the stem cortex above and below the soil line decays, while the central vascular cylinder may remain intact during early infection (Figure 4B,C). As decay advances, foliage turns brown and often remains attached [61] (Figure 4B) and severe infections may eventually invade the vascular system, causing systemic collapse and irreversible wilting [62].

As stem decay progresses, dense white mycelial mats develop on infected tissues and in the surrounding soil (Figure 4B). Within a few days, small white sclerotia form and later mature into smooth tan to light-brown structures [63]. Crown infection is often followed by root infection [64], resulting in progressive wilting, dieback, defoliation, and visible mycelia and sclerotia around decayed crown and root tissues. Fruits touching or near the soil surface are also vulnerable. Infected green or ripe fruits develop soft, sunken, water-soaked, slightly yellow lesions that expand rapidly and lead to fruit collapse [14] (Figure 4D,E). These lesions are soon covered with coarse white mycelium and abundant sclerotia, directly reducing marketable yield.

Symptom expression and disease severity vary by crop type, plant age, cultivar susceptibility, soil condition, and environment. In sunflower, the pathogen causes basal rot, with light brown lesions near the soil line that girdle the stem and are often accompanied by white mycelial masses [65]. In beans, it causes wilting, stem shredding, rotting, and drying [66]. In cucurbits, symptoms include stem and fruit rot, water-soaked lesions, plant collapse, white mycelial mats, and sclerotia formation [67]. In tomato, infection may extend from the stem base to roots, fruits, petioles, leaves, and flowers; sclerotia initially appear round and white, later becoming dark brown to black mustard seed-like structures that aid diagnosis [68]. Disease severity is influenced by plant age, cultivar, and environment. Tomato seedlings are most susceptible; 30-day-old plants showed the highest incidence and severity, while 60-day-old plants were least affected [61]. Similar early-stage susceptibility occurs in sunflower [69]. Cultivar response also differs: susceptible varieties such as Nagina and Rio Grande show faster lesion expansion, 65–75% disease incidence, 40–60% growth suppression, and abundant sclerotia, whereas Nadir and AUT-309 restrict hyphal invasion and delay symptoms [13].

Environmental and crop management factors further influence disease development. Crops established during hot and humid months, especially from summer to early autumn, experience higher infection rates than those planted during cool or dry seasons, consistent with the thermophilic nature of the pathogen [70]. High relative humidity contributes to disease spread and severity. Soil moisture levels between 30% and 50% favor fungal population growth and spread, while elevated moisture promotes rapid mycelial growth and sclerotial production [71,72]. Dense plant populations and frequent irrigation further promote infection and mycelial spread within and between plants. The disease is most severe in irrigated fields with frequent surface wetting and poor drainage, where continuous moisture near the soil surface promotes mycelial spread and sclerotia germination [73,74]. In contrast, disease progress is generally slower in rain-fed fields with well-drained soils, although sporadic outbreaks may occur after heavy rainfall [73]. Therefore, the severity of S. rolfsii often fluctuates with seasonal rainfall distribution, irrigation frequency, soil moisture regime, and field drainage conditions.

5. Disease Cycle

S. rolfsii primarily overwinters as sclerotia in the soil and, to a lesser extent, as mycelium in infected tissues or plant debris. Sclerotia, which require high oxygen levels, usually survive near the soil surface, particularly in sandy, well-drained soils, for a period ranging from 2 months to 7 years, depending on the soil conditions [16,75]. Primary infection cycles start at the beginning of the growing season when environmental conditions are favorable, such as moist soil (Figure 5). Under these conditions, sclerotia germinate and produce mycelial strands [76]. Germination of sclerotia occurs through two modes: hyphal germination and eruptive germination [75]. In hyphal germination, hyphae emerge from the sclerotia rind and need a nutrient source for continued growth [77]. Eruptive germination is a form of sclerotial germination where mycelial plugs burst through the sclerotial rind, leaving the outer shell empty after internal food reserves are utilized. This germination pathway is often stimulated by volatile chemicals like alcohol or allyl sulfide. Sclerotia undergoing eruptive germination exude more amino compounds and carbohydrates compared to sclerotia in a dormant, “nonconditioned” state, a process potentially influenced by drying, volatile compounds from remoistened plants, or other treatments that prepare the sclerotia for this unique mode of germination [75]. As the infection progresses, the fungus produces numerous sclerotia on the white mycelium. These structures are initially white but mature into dark brown, round bodies. The newly produced sclerotia then fall to the soil or remain on infected plant debris, surviving until the following favorable conditions for infection.

Secondary cycles occur when hyphae from existing infections spread to nearby healthy plants, especially in warm, humid conditions during the growing season (Figure 5). Basidiospore production may also play a role; after landing on host surfaces, basidiospores germinate, produce germ tubes, and form appressoria that penetrate plant tissues. These secondary cycles increase disease spread within the crop canopy and soil.

Understanding the conditions that favor the germination and spread of sclerotia can inform better management practices. For instance, improving soil drainage and minimizing practices that spread infested soil or debris can reduce disease incidence. Furthermore, research into the environmental triggers for basidiospore production and germination could provide new avenues for disease control, such as the development of targeted treatments or cultural practices that disrupt the pathogen’s life cycle.

6. Pathogenesis and Virulence Mechanisms of Sclerotium rolfsii

S. rolfsii employs a sophisticated and multifactorial infection strategy involving a diverse arsenal of virulence determinants that act sequentially during host invasion and colonization (Figure 6). The pathogen initiates infection through chemotropic recognition of host-derived signals, followed by rapid secretion of oxalic acid (OA) to suppress host oxidative defenses and facilitate penetration. Subsequent deployment of cell wall-degrading enzymes (CWDEs) promotes tissue maceration and necrosis, while effector proteins manipulate host cellular signaling and trigger programmed cell death (PCD) to enhance nutrient acquisition. In the final phase, sclerotial melanization ensures environmental resilience and long-term survival in soil. Collectively, these coordinated virulence mechanisms enable S. rolfsii to infect plant hosts and establish persistent infections under diverse agroecological conditions.

6.1. Oxalic Acid (OA)

OA is one of the most critical virulence determinants of S. rolfsii, facilitating host invasion by disrupting structural, biochemical, and redox homeostasis within plant tissues (Figure 7). During the early stages of infection, OA disrupts the host’s redox balance and inhibits initial immune responses by blocking callose deposition and the oxidative burst, two essential defense mechanisms that typically limit pathogen entry [78,79]. As infection progresses, OA accumulates to high levels. Quantitative studies reported that the production of OA may increase by up to ~415 mg g⁻¹ fungal biomass [78], which acidifies host tissues, activates CWDEs, and destabilizes calcium-mediated pectin cross-linking in the cell wall. During the early stages of colonization, OA exerts a dual role by initially suppressing ROS to evade host recognition, then later inducing excessive ROS accumulation that drives programmed cell death (PCD) [79,80]. This necrotic tissue serves as a nutrient base for the pathogen’s proliferation and colonization. Furthermore, OA functions as a potent, disrupting Ca²⁺-mediated pectin cross-linking within the cell wall [81]. This disruption not only destabilizes the structural integrity of the plant but also hinders calcium-dependent signaling pathways, crucial for plant defense.

6.2. Cell Wall-Degrading Enzymes (CWDEs)

In conjunction with OA, S. rolfsii secretes a broad spectrum of CWDEs, including polygalacturonases, cellulases, xylanases, and pectin lyases, which collectively dismantle host cell walls [35]. The secretion of CWDEs, coupled with rapid mycelial growth, has been identified as a key determinant of establishing successful infection [82]. OA potentiates the activity of these enzymes by lowering tissue pH and chelating calcium, thereby weakening pectin cross-links and enabling enzymatic penetration. Genomics and transcriptomic analyses indicate that S. rolfsii employs a diverse array of gene repertoires, including pathogenicity-related genes (PHI genes) and those for carbohydrate-active enzymes (CAZymes) during infection [83]. CAZymes facilitate tissue colonization and aid the pathogen in evading the host immune system. Comparative proteomic analyses have demonstrated that highly virulent isolates secrete larger quantities of CAZymes than less virulent strains, with polygalacturonase activity being strongly associated with lesion expansion and rapid disease progression [18]. This highlights a correlation between the abundance of CWDEs and the virulence of S. rolfsii.

6.3. Effector Proteins and Secondary Metabolites

Beyond chemical and enzymatic virulence, S. rolfsii secretes an array of effector proteins and secondary metabolites that fine-tune host–pathogen interactions [84,85,86,87]. Genomic and transcriptomic studies have identified numerous small secreted proteins (SSPs), including necrosis- and ethylene-inducing proteins (NEPs), that manipulate host defense signaling and accelerate necrosis. A recent whole-proteome analysis identified 30 effector candidates in the weakly aggressive isolate GP3 and 27 in the highly aggressive isolate ZY, with the two isolates exhibiting entirely distinct effector repertoires and secondary metabolite biosynthetic gene clusters [18,88]. These findings reveal isolate-specific effector and secondary metabolite repertoires. Moreover, highly virulent isolates exhibit broader effector repertoires and more active secondary metabolite biosynthetic clusters, including genes for laccases, cutinases, and proteases that degrade host barriers and detoxify phenolic compounds [89]. These effectors not only promote cell death but also help the pathogen evade recognition by the host immune system, fine-tuning infection success.

6.4. Sclerotial Melanization

Sclerotial melanization represents a crucial survival strategy for S. rolfsii, linking virulence to long-term persistence in soil. Melanin deposition in sclerotia enhances structural integrity, reduces cell permeability, and provides protection against ultraviolet radiation, reactive oxygen species, and microbial degradation [45,90]. Melanin biosynthesis occurs primarily through the DHN pathway, though alternative routes involving L-DOPA oxidation have also been reported [46,47]. Sclerotial pigmentation not only improves resistance to oxidative stress but also contributes to virulence by facilitating survival between cropping cycles and enhancing tolerance to antifungal compounds. The upregulation of melanin- and polyketide-synthesis gene clusters during infection suggests an adaptive mechanism linking stress response and pathogenicity [90].

Environmental conditions may also modulate the production of virulence determinants [91]. Isolates obtained from open-field soils may secrete different amounts of OA and exhibit various levels of polygalacturonase activity compared to isolates from protected environments, likely due to stronger abiotic and biotic stresses. Conversely, protected systems with high humidity and limited soil microbial competition may be selective for isolates with relatively reduced OA and pigmentation, though still capable of localized outbreaks. Systematic comparative studies of virulence factor expression under open versus protected cultivation remain scarce, and addressing this gap will be crucial for tailoring management strategies to specific production environments.

7. Tomato Defense Responses Against Sclerotium rolfsii

Tomato plants mount a complex and multilayered defense response upon infection by S. rolfsii (Figure 8). Transcriptomic analyses of infected roots revealed the early activation of major defense-related signaling pathways, particularly those involving salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) [92,93]. Although SA is primarily associated with resistance against biotrophic pathogens, its interaction with JA and ET enhances defense against necrotrophic fungi such as S. rolfsii. Activation of these pathways triggers the expression of pathogenesis-related (PR) genes, including PR-1, PR-3 (encoding chitinases), and PR-5 (encoding thaumatin-like proteins), which inhibit fungal hyphal growth and restrict colonization [94,95].

Defense signaling is further coordinated by transcription factors (TFs) from the WRKY, MYB, NAC, and ERF families, with WRKY33 playing a central role in JA-mediated resistance responses [41,96] (Figure 7). Genes associated with reactive oxygen species (ROS) production and detoxification are also induced. Superoxide dismutase, catalase, peroxidases, and glutathione S-transferase regulate the oxidative burst, balancing its dual role in pathogen restriction and prevention of host tissue damage [97,98].

In addition, secondary metabolite biosynthetic pathways are activated, particularly those involved in flavonoid and phytoalexin production, which exert direct antifungal activity [99]. The phenylpropanoid pathway is strongly up-regulated, leading to the accumulation of lignin and antimicrobial phenolics that reinforce cell walls and create physical and chemical barriers against fungal invasion [100,101]. Proteomic evidence corroborated these transcriptomic patterns, with enhanced abundance of PR proteins, ROS-scavenging enzymes, and phenylpropanoid pathway enzymes observed in infected tissues.

Signal transduction cascades also play a critical role in orchestrating these defense mechanisms. Mitogen-activated protein kinases (MAPKs) and calcium-dependent protein kinases (CDPKs) are rapidly activated, transmitting early pathogen recognition signals and ensuring timely induction of defense gene expression [102] (Figure 8). These transcriptomic and proteomic responses highlight the ability of tomatoes to deploy both basal and inducible defenses against S. rolfsii, although the intensity and timing of activation likely determine the outcome of infection and disease severity.

8. Genetics and Breeding for Southern Blight Resistance

Developing tomato cultivars with durable resistance to southern blight remains challenging because S. rolfsii is a broad-host-range necrotrophic pathogen. Its virulence was reported to be associated with oxalic acid production and cell wall-degrading enzymes that damage host tissues [18,103]. Available studies indicated that tomato responses to S. rolfsii were partial, genotype-dependent, and complex rather than controlled by a clearly resolved single dominant resistance gene. Southern blight-resistant breeding lines, including 5635M and 5707M, were developed through conventional selection, and recent genotype evaluations showed variation in disease incidence, disease severity, growth suppression, pigment retention, phenolic accumulation, and antioxidant enzyme activity after S. rolfsii challenge [13,104].

At present, clearly validated tomato QTLs for S. rolfsii resistance remain poorly documented, representing an important gap for molecular breeding. Future studies should therefore use resistant breeding lines and wild Solanum relatives to develop biparental mapping populations, association panels, and QTL-seq populations for identifying genomic regions associated with reduced lesion expansion, restricted mycelial colonization, delayed wilting, improved survival, and lower disease severity. Once validated across genetic backgrounds and environments, linked SNP, SSR, or InDel markers could be applied in marker-assisted selection and marker-assisted backcrossing to introgress partial resistance into elite tomato cultivars [105,106,107]. Because no validated S. rolfsii-specific molecular markers are currently established for tomato, MAS and MABC should be presented as future breeding tools rather than established approaches for this disease. If future studies show that southern blight resistance is controlled by many small-effect loci, genomic selection may provide a complementary strategy. Tomato-specific studies showed that genome-wide marker data could estimate breeding values for complex traits and disease resistance in other pathosystems, but for southern blight, GS will still require disease-specific training populations, reliable phenotyping, and multi-environment validation [108,109,110].

A clear linkage between molecular mechanisms and breeding targets should also be emphasized. Candidate traits for QTL mapping include phenylpropanoid activation, POX/PPO-associated defense, lignification, suberization, PR-protein induction, antioxidant activity, and phenolic accumulation, all of which were associated with reduced S. rolfsii infection or colonization in tomato [13,111,112]. PGIP-related cell-wall protection and oxalic-acid detoxification may also be considered prospective targets, although their direct roles in tomato resistance to S. rolfsii still require validation [113,114]. Tomato was reported to contain numerous NLR-type R-gene candidates [115]; however, no tomato R gene has yet been functionally validated in the published literature as conferring specific resistance to S. rolfsii. Therefore, future work should integrate NLR-gene mining, QTL, transcriptomics, and functional validation to determine whether any tomato R genes contribute to southern blight resistance.

9. Sustainable Approaches in Managing Southern Blight in Tomato

Management of southern blight disease in tomato necessitates a multifaceted management approach. Effective control of this pathogen requires the integration of various strategies, including cultural, biological, and chemical methods. Cultural practices such as crop rotation, soil solarization, and proper field sanitation help reduce pathogen loads and prevent disease spread. Biological control methods utilize beneficial microorganisms to suppress S. rolfsii and improve soil health. Chemical control, although necessary, should be used judiciously to prevent the development of resistance and minimize environmental impact. However, by incorporating various disease management strategies into a comprehensive program, growers can effectively control Southern blight disease and enhance sustainable tomato production.

9.1. Cultural Control

Excluding S. rolfsii from planting areas is crucial for preventing new infections and managing existing outbreaks. One effective method is to source pathogen-free planting materials, including seeds, cuttings, and transplants, from reputable suppliers. In greenhouse settings, using clean, pathogen-free pots and tools is essential to prevent contamination. Additionally, selecting planting sites with no previous history of S. rolfsii is advisable. Southern Blight is less common in areas with harsh winters, but it can still pose a problem if infected transplants from warmer regions are introduced. This approach involves rigorous sanitation practices and site selection to reduce the risk of introducing or spreading the pathogen, which is particularly important in areas prone to disease outbreaks [116].

Soil solarization is a heat-based method used to manage S. rolfsii and other soil-borne pathogens. The process involves covering moist soil with clear polyethylene sheets, which trap solar energy to raise the soil temperature. Effective solarization requires maintaining soil temperatures of at least 50 °C (122 °F) for four to six hours or 55 °C (13 °F) for three hours to kill sclerotia [117]. Solarization is most effective in smaller plots, but for large farms, it is usually too costly and labor-intensive to be practical. The success of this method depends on proper soil preparation, adequate moisture, and exposure to direct sunlight. In regions like Alabama, where high temperatures are prevalent in summer, a shorter exposure period of 4 weeks can be sufficient [118]. Solarization not only reduces S. rolfsii populations but also controls other soil-borne diseases, plant-parasitic nematodes, and weeds. Nevertheless, it is a high-investment practice that requires annual repetition to maintain effectiveness.

Deep plowing is another effective cultural control measure for managing Southern Blight. By plowing the soil to depths greater than 2.5 cm, sclerotia are buried below the germination zone, reducing their ability to produce new infections. Studies show that depths of 8 cm or more effectively inhibit sclerotia germination due to mechanical stress [75]. However, deep plowing can alter pathogen distribution in the soil and may shift the location of future outbreaks [119]. This practice is most beneficial when combined with other management strategies to ensure comprehensive control and reduce the risk of exacerbating the problem in certain areas. Although deep plowing and soil solarization are useful cultural practices, their field value depends on soil conditions, crop schedule, and production cost. Burial-depth studies showed that S. rolfsii sclerotia lost viability as soil depth and burial duration increased, supporting deep plowing as a method to reduce surface inoculum [16]. Soil solarization suppresses soilborne pathogens by covering moist soil with transparent polyethylene film to raise soil temperature, but recent studies described it as requiring several weeks of field coverage, which may conflict with intensive cropping schedules [120]. Conventional polyethylene films also create disposal and environmental burdens, while tomato mulch studies have emphasized the need to reduce reliance on such plastics because of waste concerns [121,122]. Therefore, solarization should be recommended cautiously, mainly for warm regions and high-value tomato or vegetable systems where disease suppression and yield benefits can justify temporary field closure and plastic-film costs.

Soil amendments play a crucial role in managing Southern Blight. Incorporating organic materials such as compost, cotton gin trash, and corn straw enhances microbial activity and promotes antagonistic organisms like Trichoderma spp., which suppress S. rolfsii [123]. Similarly, oil cakes from coconut, groundnut, neem, mustard, and sesame have shown complete inhibition of S. rolfsii while supporting T. asperellum growth [124]. Oil cakes also improve soil structure, water retention, and cation exchange capacity, further aiding disease suppression [125]. Additionally, deep plowing combined with inorganic fertilizers such as calcium nitrate, ammonium bicarbonate, or urea has effectively reduced disease incidence in crops like processing carrots [75]. Increased nitrogen levels can inhibit sclerotia germination, while calcium may alter host susceptibility. However, these methods may be less effective in sandy soils prone to leaching, necessitating further research for optimization across various soil types.

9.2. Biological Control

Biological control represents a sustainable and effective strategy for managing S. rolfsii, the pathogen responsible for southern blight. Various microorganisms have shown promise in controlling this disease (

Table 2. The list of common biological control agents and their modes of action against Sclerotium rolfsii.

Biological Control Agent	Mode of Action	Remarks	Citation
Stenotrophomonas maltophilia PPB3 and Bacillus subtilis PPB9	Production of antibiotics and hydrolytic enzymes	Also show potential to solubilize phosphate and fix nitrogen, improving seed germination, seedling vigor, etc.	[12]
Trichoderma harzianum	Antagonism, mycoparasitism	Widely used, enhances plant growth	[130]
Bacillus species	Production of antibiotics and hydrolytic enzymes	Plant growth-promoting attributes	[131]
Bacillus velezensis NC318	Antibiotic production, competition	Produces antifungal compounds like iturins and fengycins	[132]
Gliocladium virens	Antibiosis, competition, and mycoparasitism	Effective against S. rolfsii, especially in high-humidity conditions	[133]
Pseudomonas fluorescens	Antibiotic production, enzyme production, competition	Plant growth-promoting traits	[134]
Streptomyces sp. RP1A-12	Production of antibiotics and hydrolytic enzymes	Plant-growth-promoting traits	[135]
Streptomyces spp.	Antibiotic production and extracellular enzymes	Produce a variety of secondary metabolites that inhibit the growth of many bacteria, fungi, and protozoa	[136]
Myrothecium verrucaria	Mycoparasitism, hydrolytic enzyme production	Increases germination rates and suppresses pathogens	[137]
Penicillium decaturense and Penicillium rubens	Competition, antibiotic production	Exhibit strong inhibitory effects on mycelial growth and sclerotial formation	[138]
Paenibacillus sp. Strain UY79	Antibiotic production	Produces a wide range of antibiotics and stimulates plant defenses	[139]
Aspergillus niger	Enzyme production, competition	Little inhibition of mycelial growth of the pathogen	[140]

). Key biological agents include Gliocladium virens, which has been effective in reducing sclerotia populations in soil up to 30 cm deep and thereby lowering the incidence of southern blight on tomatoes [126]. T. koningii has also proven effective in reducing both the number of sclerotia and the spread of the disease in field conditions [127]. Laboratory studies indicate that T. viride, T. harzianum, and T. pseudokoningii can significantly inhibit S. rolfsii mycelial growth, with reductions of 68%, 57%, and 53%, respectively [128,129].

Combining these agents with other treatments can enhance their effectiveness. For example, a combination of T. harzianum and Glomus clarum (an arbuscular mycorrhizal fungus) has shown greater control over Jerusalem artichoke than either fungus alone, likely due to synergistic effects [141]. Additionally, mixing T. harzianum with fungicides like carboxin and thiram, along with mustard oil cake, achieved better control than using these components separately [142]. Field trials using Trichoderma formulations mixed with ryegrass seed demonstrated significant control of S. rolfsii in tomato crops, with incidence rates dropping to less than 10% compared to untreated controls with 78% incidence [143]. In greenhouse studies, T. harzianum grown on wheat bran proved more effective than liquid conidial suspensions [144], although liquid formulations are advantageous for large-scale production due to their ease of use [145]. The timing and frequency of application are crucial; multiple doses of T. harzianum resulted in healthier plants compared to a single application, underscoring the importance of strategic application [143].

The transition from laboratory assays to field application remains challenging for southern blight biocontrol because antagonist performance must be validated under tomato–S. rolfsii conditions. In tomato, Bacillus sp. 2P2 reduced collar rot infection, restricted S. rolfsii colonization, and induced defense-related enzymes and PR proteins [111]. Similarly, Trichoderma asperellum A10 enhanced tomato defense against southern blight by suppressing collar rot and activating PR genes, antioxidant enzymes, WRKY31, MYC2, lipoxygenase, ethylene-response genes, and SA/JA/ET-related pathways [112]. Earlier greenhouse works also showed that selected Trichoderma isolates reduced tomato collar rot incidence and improved seedling performance under S. rolfsii challenge [146]. More recently, Trichoderma isolate combinations were shown to suppress southern blight in tomato, reduce S. rolfsii growth and oxalic acid production, improve plant growth and yield traits, and enhance PO, PPO, and PAL activities [60]. Therefore, Bacillus and Trichoderma strains should be used for southern blight management only after tomato-specific validation under local soil and production conditions.

Overall, biological control offers a viable alternative for managing S. rolfsii, with various agents and combination treatments providing effective disease control. The selection and application of these biological agents should be tailored to specific conditions and crop needs for optimal results.

9.3. Mycovirus-Induced Hypovirulence

Mycoviruses or viruses that infect fungi have gained increasing attention for their potential role in biocontrol strategies against plant pathogens, including S. rolfsii. These viruses, particularly those associated with hypovirulence, provide an eco-friendly alternative to chemical fungicides by naturally weakening pathogenic fungi. Their successful application has been well documented in Cryphonectria parasitica and S. sclerotiorum [147,148], whereas reports involving S. rolfsii are still emerging. Nonetheless, recent studies revealed that mycoviruses can suppress this aggressive soil-borne pathogen through profound molecular and physiological disruptions.

In S. rolfsii, dsRNA mycovirus infections caused hypovirulence characterized by reduced mycelial growth, impaired sclerotial development, and diminished pathogenicity. For example, the hypovirulent strain BHL-1 exhibited slower growth and reduced aggressiveness due to dsRNA elements, whereas virus-free isolates remained virulent [149]. Mycovirus-infected strains also showed impaired secretion of oxalic acid and key cell wall-degrading enzymes such as laccases, cellulases, and polygalacturonases, which are factors essential for host penetration and colonization [80,150]. The disruption of sclerotia formation further reduced the fungus’ ability to survive adverse conditions and initiate new infections [151,152].

Molecular studies provided insight into these phenotypes. Transcriptomic analyses of hypovirulent strains revealed broad reprogramming of metabolic and pathogenicity networks, including downregulation of virulence-associated genes encoding pectinases, cellulases, necrosis-inducing proteins, and oxidative stress-related enzymes [153,154]. Concomitantly, antiviral RNAi machinery, Dicer, Argonaute, and RdRP, was upregulated, suggesting crosstalk between antiviral defense and fungal developmental pathways [155]. Proteomic analyses supported these findings, showing reduced accumulation of virulence-related proteins (e.g., NLPs, proteases, laccases) and altered abundance of proteins involved in signal transduction pathways such as MAPK cascades, calcium-dependent kinases, and oxidative stress regulators [102,156,157]. These shifts highlighted that hypovirulence was not restricted to the loss of individual virulence factors but reflected a systemic remodeling of signaling, stress adaptation, and host-interaction pathways.

A major advance was reported by [158], who identified multiple novel dsRNA mycoviruses in a hypovirulent S. rolfsii strain, including members of Benyviridae, Endornaviridae, Fusariviridae, Hypoviridae, and Fusagraviridae. Importantly, the study provided the first evidence of Dicer-mediated small RNA production in S. rolfsii, underscoring the role of RNAi-based antiviral responses that also impinged on fungal growth, differentiation, and virulence. Similarly, ref. [159] detected dsRNA mycoviruses in ~20% of S. rolfsii isolates from diverse crops in Bangladesh, indicating the natural occurrence of hypovirulent strains. These findings paralleled field-level successes in other systems, such as CHV1 in Cryphonectria and SsHADV1 in Sclerotinia, which had been deployed for biocontrol [160,161].

Collectively, these studies demonstrated that mycoviruses not only weakened S. rolfsii physiologically but also reshaped its transcriptomic and proteomic landscape, particularly by modulating cell wall degradation, oxidative stress responses, secondary metabolism, and signaling cascades critical for pathogenicity. Harnessing naturally occurring hypovirulent strains or introducing mycoviruses into virulent populations could therefore provide a sustainable, environmentally sound strategy for managing southern blight in tomato and other susceptible crops.

9.4. Development of Resistant Cultivars

The development of resistant tomato cultivars remains one of the most effective and sustainable strategies for managing southern blight caused by S. rolfsii. However, progress has been limited due to the pathogen’s wide host range, high genetic variability, and the scarcity of strong resistance sources in cultivated germplasm. Efforts to strengthen host resistance have therefore relied on both conventional breeding approaches and modern biotechnological tools.

9.4.1. Conventional Breeding Approaches

Traditional breeding programs focused on screening tomato cultivars and their wild relatives for resistance to S. rolfsii. In these screenings, resistance to S. rolfsii varied widely among tomato germplasm, and several valuable sources of resistance across cultivated, wild, and breeding lines were identified. A 2010 study screened 50 tomato lines, including two local checks, under greenhouse conditions during both dry and wet seasons. Plants were artificially inoculated with S. rolfsii. Four lines (AVTO 1314, AVTO 1715, AVTO 1716, and AVTO 1616) consistently demonstrated high levels of resistance across both seasons. Significant genotype × environment interactions were also observed for yield traits [162], highlighting the importance of multi-environment testing for identifying stable sources of resistance.

In Nigeria, four tomato varieties (Akeakpev, Ihoozwa, Ishase, and UTC) were tested for resistance to fungal pathogens, including S. rolfsii. Various symptoms, such as stem rot and wilt, were induced through artificial inoculations. UTC was the most susceptible, with high rates of necrosis (21.23%) and whole-plant wilt (83.33%), while Akeakpev showed the greatest tolerance at 33.42% disease incidence, followed by Ishase at 35.73%. The results highlighted Akeakpev as a comparatively resistant variety, suitable for cultivation even in pathogen-infested soils, offering potential for improved yield stability under disease pressure [163].

A recent screening of twenty tomato genotypes against S. rolfsii revealed considerable variation in resistance responses [13]. Under greenhouse conditions, five genotypes (e.g., Nadir, AUT-309) exhibited high resistance, maintaining normal growth, photosynthetic pigment content, and enhanced biochemical defenses. In contrast, Nagina and Rio Grande were highly susceptible, with disease incidence ranging from 65 to 75% and up to 60% growth reduction. Resistant lines exhibited pronounced increases in phenolic accumulation and antioxidant enzyme activities, whereas susceptible genotypes displayed weaker defense responses and chlorophyll degradation. Detached leaf and fruit assays confirmed these trends, with greater necrosis and fungal colonization in susceptible types. These findings also indicated that resistance to S. rolfsii in tomato was genotype-dependent rather than determined by whether a line was hybrid or open-pollinated. For example, Nadir (resistant) and Nagina (susceptible) were both reported hybrids [164,165], while Rio Grande (open-pollinated) [166] also exhibited high susceptibility. These results highlighted that hybrid status alone did not predict resistance. Instead, biochemical defense responses such as phenolics, Polyphenol oxidase, peroxidase, and catalase activity served as reliable indicators of resistance potential.

While resistance sources within cultivated tomato varieties are infrequent, wild tomato germplasm (Lycopersicon pimpinellifolium Mill.) represents a valuable reservoir of resistance to S. rolfsii. Early efforts identified resistance in two wild Peruvian accessions, PI 126932 and PI 126432 [167]. Subsequent evaluations confirmed that L. pimpinellifolium and some of its derived breeding lines exhibited greater resistance than cultivated tomato genotypes [168]. A major breakthrough arose from long-term breeding programs in the United States, initiated in the 1950s, which culminated in the release of six resistant breeding lines (5635M, 5707M, 5719M, 5737M, 5876M, and 5913M) with resistance traced to L. pimpinellifolium [104]. Resistance in these lines was associated with the precocious development of a protective peridermal phellem barrier at the stem base, effectively restricting pathogen ingress. Their survival rates were comparable to those of resistant L. pimpinellifolium accessions (e.g., PI 126432) and markedly superior to susceptible controls. Importantly, these lines also carried resistance to Fusarium oxysporum f. sp. lycopersici race 1 and gray leaf spot (Stemphylium solani), demonstrating the potential for pyramiding multiple disease resistance traits into elite tomato germplasm.

In Mexico, the center of tomato domestication, a systematic screening of 42 wild tomato accessions (Solanum lycopersicum var. cerasiforme) revealed valuable sources of resistance to S. rolfsii [169]. Artificial inoculation assays demonstrated that the majority of accessions were highly susceptible, resulting in plant mortality. However, five accessions (Nos. 8–12), collected from diverse regions, expressed clear resistance and survived pathogen challenge. These findings confirmed that significant resistance to S. rolfsii existed within wild tomato germplasm and underscored its importance as a genetic reservoir for resistance breeding. The identification and strategic deployment of such accessions represented critical steps toward developing cultivars with durable resistance to southern blight. Marker-assisted selection (MAS) could further accelerate the introgression of resistance loci, although progress had been constrained by the limited characterization of specific resistance (R) genes against S. rolfsii [170]. In addition, grafting susceptible tomato scions onto interspecific resistant or tolerant rootstocks had emerged as a promising complementary strategy to provide adequate resistance to S. rolfsii while sustaining fruit yield and quality [56].

It is also worth mentioning that most of these resistance screenings had been performed under controlled greenhouse conditions. While this type of screening was useful for rapid and uniform evaluation, such controlled settings do not fully capture the complexity of open-field environments, where fluctuating temperature, soil moisture, microbial competition, and inoculum pressure could significantly influence disease expression. Consequently, resistance observed in greenhouses may not translate directly to the field. Therefore, rigorous open-field trials were essential to validate greenhouse findings, determine the durability of resistance, and identify cultivars capable of performing reliably under real-world production conditions.

9.4.2. Biotechnological Approaches

Biotechnological approaches offer innovative solutions for developing tomato resistance to S. rolfsii, overcoming the limitations of conventional breeding, which is constrained by the limited resistance sources available in cultivated germplasm. Modern tools, such as RNA interference (RNAi) and CRISPR-Cas genome editing, enable the precise targeting of pathogen virulence genes or host susceptibility factors, offering environmentally friendly and durable strategies for managing southern blight. RNAi is a conserved cellular mechanism in eukaryotes whereby double-stranded RNA (dsRNA) is processed into small interfering RNAs (siRNAs) that guide sequence-specific degradation of target mRNAs through the RNA-induced silencing complex (RISC) [171,172]. This process leads to post-transcriptional gene silencing (PTGS) and has been widely exploited as a tool for functional genomics and crop protection. Recent advances in dsRNA delivery technologies enabled the application of RNAi as an eco-friendly alternative to chemical fungicides [173].

Two major strategies have been developed for RNAi-based plant disease control: host-induced gene silencing (HIGS) and spray-induced gene silencing (SIGS) [174]. In HIGS, transgenic plants are engineered to express hairpin dsRNAs targeting essential fungal genes during infection. This approach was effective in related necrotrophic fungi: for instance, silencing of oxaloacetate acetylhydrolase reduced oxalic acid accumulation and suppressed S. sclerotiorum pathogenicity in Brassica napus [175]. SIGS, in contrast, involves exogenous application of dsRNA or siRNA molecules directly onto plant surfaces, where they are taken up by pathogens to silence target genes. This non-transgenic method showed promise against multiple fungi, including Fusarium graminearum [176,177].

In the case of S. rolfsii, RNAi-based strategies could be targeted against genes encoding oxalic acid biosynthetic enzymes, CWDEs such as polygalacturonases and cellulases, or virulence-associated signaling proteins. Virome studies confirmed the presence of Dicer-mediated small RNAs in S. rolfsii, suggesting that the fungus is capable of processing exogenous dsRNAs and was therefore a suitable target for RNAi-mediated silencing [158]. While no commercialized RNAi-based products are yet available against S. rolfsii, the proven efficacy in related pathogens provided strong evidence for feasibility. The ability to deploy RNAi either through durable transgenic HIGS or flexible, field-based SIGS offers a highly adaptable platform for southern blight management in tomato.

The CRISPR-Cas (clustered regularly interspaced short palindromic repeats) system revolutionized genome editing due to its simplicity, cost-effectiveness, and high precision [178]. Using a guide RNA (gRNA) to direct the Cas9 nuclease to specific DNA sequences, this system introduced double-stranded breaks that are repaired by the cell, enabling precise insertions, deletions, or substitutions. In crop improvement, CRISPR was widely applied to engineer resistance against diverse pathogens, either by inactivating host susceptibility (S) genes or by enhancing the expression and regulation of defense-related genes [179].

Recent progress was also made in establishing CRISPR-based genetic transformation protocols in S. rolfsii. Ref. [180] successfully employed PEG-mediated transformation to deliver Cas9 ribonucleoprotein complexes (RNPs) into fungal protoplasts, achieving targeted gene editing of the AAT1 gene and demonstrating proof-of-concept for functional genomics in this pathogen. Such advances opened the possibility of simultaneously editing multiple pathogenicity factors in S. rolfsii to generate hypovirulent strains, which could serve as biocontrol agents.

For tomato, CRISPR-Cas could be deployed in two complementary ways to improve resistance against southern blight. Firstly, by editing host susceptibility genes (S-genes) involved in oxalate sensitivity, hormone signaling imbalance, or ROS misregulation, thereby reducing the host’s vulnerability. Secondly, enhancing host defense pathways by targeting transcriptional regulators (e.g., WRKY33, NAC, MAPKs) or biosynthetic pathways for lignin and phytoalexins, thus boosting basal and inducible immunity. With the development of multiplex CRISPR systems, it became feasible to engineer polygenic resistance by simultaneously editing multiple genes, which was crucial against broad-host-range necrotrophs like S. rolfsii. Moreover, precision tools such as base editing and prime editing could introduce beneficial alleles without the need for foreign DNA integration, which could accelerate regulatory approval and public acceptance.

9.5. Chemical Control

The management of southern blight in tomatoes often relied on fungicides, particularly under high disease pressure; however, their effectiveness varied depending on compound, dose, and application timing. Widely used fungicide classes included triazoles (FRAC Group 3; e.g., tebuconazole, prothioconazole) and QoIs (Group 11; e.g., pyraclostrobin, azoxystrobin, fluoxastrobin). Although these compounds effectively inhibited mycelial growth in vitro, field performance was often inconsistent under conducive conditions [181,182]. Benzimidazoles (e.g., carbendazim) and chloronitriles (e.g., chlorothalonil) were also evaluated. Still, these fungicides are typically more effective against foliar pathogens than soilborne fungi, limiting their usefulness for southern blight management [181].

Among newer chemistries, succinate dehydrogenase inhibitors (SDHIs, FRAC Group 7) such as penthiopyrad and fluxapyroxad showed promising activity against S. rolfsii. In vitro studies demonstrated that fluxapyroxad + pyraclostrobin and penthiopyrad significantly reduced sclerotial germination and colony growth when applied directly to sclerotia or to inoculated tomato stems. Field trials in South Carolina during 2015–2016 confirmed that fluxapyroxad + pyraclostrobin and quintozene (PCNB) significantly lowered southern blight incidence compared with untreated controls, although the latter caused severe phytotoxicity, stunting 43–75% of plants. In contrast, the efficacy of pyraclostrobin and penthiopyrad alone varied across years, and no significant differences in fruit yield were observed among treatments [181].

Several other recent evaluations also provided more precise data on fungicide performance against S. rolfsii and its teleomorph Athelia rolfsii. In vitro assays showed that inpyrfluxam, mefentrifluconazole, and a mixture of bixafen and flutriafol achieved 80–95% inhibition, with residual activity lasting up to three weeks. However, efficacy declined on new plant tissues [183]. Greenhouse trials revealed that mefentrifluconazole achieved 95.36% preventive efficacy and 60.94% curative efficacy within nine days [184]. Pyraclostrobin inhibited ~90% mycelial growth in vitro and provided ~80% disease reduction under field conditions [185]. Similarly, [186] reported strong suppression of A. rolfsii using benzovindiflupyr under controlled conditions.

Earlier studies support these findings: tebuconazole (0.15%) inhibited ~94% of mycelial growth [187], while carbendazim + mancozeb combinations showed synergistic inhibition, and trifloxystrobin + hexaconazole achieved 100% inhibition in vitro [37]. EC₅₀ values for triazoles and carboxamides such as flutolanil and tebuconazole ranged from 0.005 to 0.213 ppm, confirming their high potency [188]. A summary of quantitative efficacy data was presented in

Table 3. Reported efficacy of selected fungicides against Sclerotium rolfsii.

Fungicide/Combination	Efficacy/EC50	Reference
Tebuconazole (0.15%)	~94% inhibition (in vitro)	[187]
Carbendazim + Mancozeb (0.2%)
Captan + Hexaconazole/Trifloxystrobin	100% inhibition (in vitro)	[37]
Propiconazole (50–100 ppm)	70.9–82.96% inhibition; 100% at ≥500 ppm (in vitro)
Flutolanil, Tebuconazole, etc.	EC50 = 0.005–0.213 ppm	[188]
[188] Mefentrifluconazole	Mean EC50 = 0.21 ± 0.11 mg L−1 (range: 0.02–0.55 mg L−1)	[184]
Pyraclostrobin	~90% inhibition (in vitro); ~80% efficacy (field)	[185]
Mefentrifluconazole (200 mg L−1)	95.36% preventive; 60.94% curative efficacy (greenhouse trial)	[184]
Fluxapyroxad + Pyraclostrobin (SDHI + QoI)	Strong inhibition of sclerotial germination and colony growth (in vitro); significantly reduced field incidence (both years tested)	[181]
Penthiopyrad (SDHI)	Reduced sclerotial germination and mycelial growth (in vitro); field efficacy variable across years	[181]
Quintozene (PCNB)	Reduced disease incidence in field but caused 43–75% plant stunting (phytotoxicity)	[181]
Benzovindiflupyr	Significant inhibition of mycelial growth and sclerotia formation (in vitro)	[186]

.

Although these fungicides provide strong suppression of S. rolfsii, their indiscriminate or repeated use raises concerns about the development of resistance, environmental contamination, toxic residues, and safety hazards [189]. Thus, fungicides should be applied judiciously, in rotation with different modes of action, and integrated with biological and cultural practices. Looking ahead, improved timing and precision in fungicide use could enhance efficacy while reducing the need for inputs. Remote sensing and precision agriculture, discussed in the following section, offer tools to identify infection hotspots, optimize application schedules, and integrate fungicides more effectively into sustainable Integrated Disease Management (IDM) strategies.

9.6. Remote Sensing and Precision Agriculture as Promising Transformative Tools

Remote sensing and precision agriculture represent cutting-edge approaches for enhancing crop health surveillance and targeted interventions. These technologies offer new opportunities to detect, monitor, and manage S. rolfsii infections with greater efficiency and precision. Recent studies have demonstrated the feasibility of applying hyperspectral and thermal imaging for early detection of S. rolfsii and its teleomorph Athelia rolfsii. For example, 183] combined hyperspectral and thermal sensors with machine learning to detect peanut plants infected by A. rolfsii one day before symptom expression, identifying key diagnostic wavelengths (~505, 690, and 884 nm). Similarly, [190] used UAV-based visible and thermal imagery to detect S. rolfsii-induced canopy stress at the field scale, with thermal indices providing earlier signals than RGB imagery. Ref. [191] further demonstrated that hyperspectral imaging, coupled with machine learning, could monitor the progression of soil-borne diseases, including S. rolfsii, in wild rocket, providing transferable methodologies for tomato. Remote sensing was also been applied to evaluate biological control, as demonstrated by [192], who correlated vegetation indices (OSAVI, SAVI, TSAVI, TVI) with the efficacy of Trichoderma-based suppression of S. rolfsii.

Very recent advances reinforce these findings. Refs. [193,194] demonstrated that UAV-based hyperspectral imaging combined with deep learning can detect early physiological stress signatures associated with soil-borne infections. In contrast, [195] showed that vegetation indices integrated with Gaussian Process classifiers could differentiate disease severity with high accuracy. Despite its promise, widespread adoption of remote sensing for S. rolfsii management faced challenges. High costs of UAVs, hyperspectral sensors, and data processing limited feasibility for smallholder farmers [196,197]. Scalability was further constrained by limited infrastructure, low digital literacy, and weak extension services in rural areas [198,199]. Farmer adoption was also hindered by uncertainty regarding cost–benefit returns [200]. To overcome these barriers, strategies such as affordable multispectral drones, mobile-based decision-support tools, cooperative service models, and targeted subsidies and training programs are recommended.

9.7. Integrated Disease Management (IDM)

Effective management of southern blight in tomato requires a multifaceted Integrated Disease Management (IDM) strategy that combines chemical, biological, cultural, and technological approaches in a coordinated manner (Figure 9). The aim is not only to suppress immediate infections but also to minimize recurrence, enhance soil health, and secure long-term productivity. For prospective IDM, chemical control remains a crucial component, particularly under high disease pressure. Fungicides such as Mancozeb and Ketoconazole achieved near-complete inhibition when applied in conjunction with antagonistic fungi, like Trichoderma spp. [201], while strobilurin fungicides, such as Azoxystrobin, and triazoles, like Propiconazole, suppress mycelial growth effectively [202]. However, sole reliance on chemicals is unsustainable due to environmental and health risks, highlighting the need for their integration with safer, complementary strategies such as biological control. Biological control provides an eco-friendly and resilient alternative. Trichoderma spp. remained the most widely studied antagonists, with commercial products such as Soilguard and Trichodex consistently reducing pathogen colonization, while T. viride had shown up to 69.62% inhibition of S. rolfsii [15]. Integration of Trichoderma with organic amendments such as neem cake further enhances suppression and simultaneously improves soil fertility [203]. Such synergistic bio-based interventions strengthen natural soil suppressiveness and promote rhizosphere resilience. Additionally, cultural practices form the foundation of IDM by lowering the initial inoculum load and creating unfavorable conditions for pathogen establishment. Crop rotation with non-host species disrupts the pathogen’s life cycle, while organic amendments and irrigation management help maintain soil health, reduce stress on tomato plants, and indirectly improve host defense [204]. When strategically combined with biological and chemical inputs, these practices create a multi-layered barrier against infection. Furthermore, host resistance, though limited in tomato germplasm against S. rolfsii, remains a critical component of IDM. Current sources offer only partial resistance, often derived from wild relatives or tolerant rootstocks, but advances in molecular breeding, RNAi, and CRISPR-based genome editing hold promise for developing resistant cultivars. Even partial resistance, when combined with cultural, biological, and chemical approaches, can reduce pathogen pressure and enhance the durability of IDM systems.

While these approaches have demonstrated effectiveness, the next generation of IDM must move toward predictive, adaptive, and sustainable frameworks. We propose three forward-looking hypotheses/models for enhancing IDM against S. rolfsii:

(1)

Microbiome-assisted IDM-harnessing beneficial microbial consortia (e.g., Trichoderma + PGPR + AMF) tailored to specific soil types, hypothesizing that microbial network engineering will provide longer-lasting suppression than single-agent biocontrol.

(2)

Climate-smart IDM—integrating weather- and soil-moisture-based predictive models to optimize timing of cultural, chemical, or biological interventions, thereby reducing input use and improving efficiency under climate variability.

(3)

Technology-enhanced IDM—leveraging RNAi sprays (SIGS), CRISPR-based resistant cultivars, and digital surveillance tools to combine host resistance with precision application of control agents, hypothesizing that integration of biotech with traditional IDM will significantly reduce reliance on fungicides.

By embedding IDM into a systems framework that couples classical methods with microbiome engineering, predictive modeling, and modern biotechnological tools, tomato production systems can transition from reactive disease control to proactive, sustainable, and resilient management of southern blight.

10. Socio-Economic Feasibility and Climate-Adaptive Strategies

Effective management of S. rolfsii requires not only biological efficacy but also socio-economic feasibility, particularly under the pressures of climate change [205]. Southern blight is most prevalent in tropical and subtropical regions, where smallholder farmers often face limited access to costly fungicides, precision monitoring systems, and resistant cultivars [206]. High input costs and labor demands, such as those for soil solarization or repeated fungicide sprays, restrict adoption in resource-constrained systems [207].

Economic feasibility and the challenges to adopting any management strategies should be determined. Affordable and locally adaptable solutions are critical for farmer-level adoption. Low-cost biological control using native microbial strains, compost or organic amendments, and rotation with non-host crops provides scalable options. Resistant tomato cultivars, though scarce, remain one of the most farmer-friendly interventions, and advances in marker-assisted selection and genome editing (e.g., CRISPR) are accelerating the development of more durable resistance [208]. However, regulatory hurdles and limited seed dissemination systems continue to hinder access. Cooperative production of biocontrol inoculants, mobile-based advisory platforms, and shared equipment service models could reduce costs and improve adoption among smallholder farmers.

Adopting climate-adaptive strategies is crucial in the face of ongoing climate change. Climate change intensifies the threat of S. rolfsii by creating more favorable conditions for its survival and spread. Rising soil temperatures, erratic rainfall, and prolonged humidity accelerate sclerotia germination and disease outbreaks, while waterlogging increases the susceptibility of hosts. Climate-adaptive approaches such as predictive disease modeling, improved field drainage, optimized irrigation, and climate-resilient cropping calendars can reduce disease risk [209,210]. Integrating resistant varieties with these agronomic adjustments will be crucial for sustainable management under variable climates.

Policy and extension perspectives play a critical role in implementing adaptive measures. Successful scaling of these measures requires supportive policies and effective knowledge transfer. Initiatives such as public–private partnerships, farmer field schools, and community-based forecasting systems can enhance access to technologies, improve digital literacy, and boost farmers’ confidence in adopting innovative solutions. By integrating biological control, resistant cultivars, and precision tools with climate-adaptive agronomy, IDM can become both economically viable and resilient to climate variability.

11. Conclusions

Southern blight, caused by S. rolfsii, is a major threat to global tomato production due to the pathogen’s adaptability, broad host range, and long-term survival as sclerotia. Advances in molecular research have clarified its virulence mechanisms, notably oxalic acid production, cell wall-degrading enzymes, and signaling pathways. The disease is most prevalent in warm, humid regions, with incidence influenced by cultural practices and environmental factors. Effective management requires an integrated approach combining cultural measures (crop rotation, deep plowing, solarization, and organic amendments), biological control (e.g., Trichoderma, Bacillus), and judicious chemical use. Emerging tools such as mycoviruses, RNA interference, genetic resistance breeding, and precision agriculture technologies, including remote sensing and hyperspectral imaging, offer new opportunities for early detection and targeted intervention. Climate-adaptive strategies, farmer training, and socio-economic feasibility are essential for practical adoption. Future progress depends on merging scientific innovations with sustainable farming in a climate-resilient IDM framework to protect tomato yields and strengthen global food security.