Review article

Sustainable management practices for plant-parasitic nematodes in pomegranate orchards in Egypt

Ahmed A. A. Sallam¹ and Atef M. El-Sagheer^2*

1. Plant Protection Department, Faculty of Agriculture, Sohag University, Sohag, Egypt.

2. Agricultural Zoology and Nematology Department, Faculty of Agriculture, Al-Azhar University, Assiut (71524), Egypt.

Abstract: Traditional plant-parasitic nematode (PPN) management in agriculture often relies on individual approaches, such as chemical nematicides or resistant cultivars. While these methods can offer persistent control, they often face limitations, including environmental concerns, nematode resistance development, and potential harm to non-target organisms. Therefore, this article aims to clarify the complexities and mechanisms of integrated pest management (IPM) as part of a paradigm shift toward integrated sustainable management (ISM). ISM acknowledges the complexities of nematode communities and their interactions with the soil ecosystem. It emphasizes the use of complementary strategies —such as biocontrol agents, cultural practices (including crop rotation and cover crops), and host plant resistance —in a synergistic manner. This holistic approach aims to naturally suppress PPN populations, minimize reliance on chemical interventions, and promote long-term soil health.  Additionally, the article explores specific program proposals that exemplify this ISM approach, offering pomegranate growers practical solutions to achieve sustainable, profitable production while maintaining environmental well-being. By advocating for a shift towards ISM, this article aims to contribute to a more resilient and sustainable future for pomegranate cultivation and broader agricultural practices.

Keywords: PPNs control, Phytonematodes, Integrated pest management, Sustainable agriculture

Introduction[1][2]

Pomegranate Punica granatum L. (Lythraceae) boasts a diverse array of cultivars, with estimates reaching approximately 500 globally (Stover and Mercure, 2007). In Egypt, seven cultivars dominate the landscape: Araby, Assuity, Hegazy, Manfalouty, Nab El Gamal, Wardi, and Wonderful (Ismail et al., 2014; Amar and El-Zayat, 2017). The economic importance of pomegranates is significant due to their increasing demand and consumption across regions such as India, Spain, Egypt, and the United States (Seth, 2003; Chandra et al., 2010; Sepúlveda et al., 2010). Pomegranate is important not only in agricultural production as a fruit tree but also as an ornamental plant, thanks to its showy flowers, which further enhance its economic value (Seth, 2003). Pomegranate cultivation has had a significant economic impact in these regions, with the fruit serving as a cultural icon in Egypt and India, driving high demand and economic importance (Taha, 2018; Kahramanoglu, 2019). Additionally, pomegranate is a prominent crude ingredient for various industries, including pharmaceuticals, cosmetics, beverages, and food, further enhancing its economic value (Bilgili and Genç, 2023; Valero-Mendoza et al., 2023).

In Egypt, pomegranate cultivation has become a primary source of income for farmers, particularly in Upper Egypt, contributing to the economic sustainability of the agricultural sector. The cultivation of pomegranates has also expanded to newly reclaimed lands in Egypt, facilitated by the tree's drought tolerance, making it suitable for cultivation in dry weather and arid regions (CAPMAS, 2021). The economic importance of pomegranate is multifaceted, encompassing agriculture, industry, and trade. Egypt ranks seventh among the world's top pomegranate producers, with a cultivated area of 31,987 hectares and a production of 382,587 tonnes. In 2020, it further distinguished itself as the fifth largest exporter, shipping 82,866 tonnes (Ministry of Agriculture, 2020).

Plant-parasitic nematodes (PPNs) pose a significant threat to pomegranate production worldwide (Singh et al., 2014; Sharma et al., 2020; Mandal et al., 2021), resulting in substantial economic losses due to reduced yield and fruit quality (Sharma et al., 2020; Khan et al., 2022). These microscopic pests damage the root system, hindering nutrient and water uptake, leading to stunted growth, smaller fruit size, and malformations (Khan et al., 2022). Studies report yield reductions ranging from 20% to 70% due to PPNs, highlighting their critical impact on pomegranate profitability (Khan et al., 2022). Therefore, effective control of PPNs is essential for ensuring sustainable and profitable pomegranate production (Singh et al., 2014).

Therefore, the objectives of this review are to provide a comprehensive analysis of PPN management in pomegranate orchards by updating information on current strategies for managing PPNs, exploring strategies for sustaining the efficacy of these control methods, and proposing integrated pest management (IPM) programs that optimize control efficiency while adhering to environmental sustainability standards.

1. Common species of PPNS infecting pomegranate

Pomegranate cultivation faces significant threats from diverse PPN species, which affect yield and fruit quality worldwide (Karssen and Moens, 2002; Sikora et al., 2018; Yadav and Patil, 2021). Root-knot nematodes (RKNs), particularly Meloidogyne incognita and M. javanica, are widely reported to cause root galls, reduced growth, and yield losses (Singh et al., 2019a; Hammad and El-Sagheer, 2022).

Other economically important PPNs include Rotylenchulus reniformis, which causes stunting, necrosis, and significant yield reduction (Darekar et al., 1990), and Pratylenchus spp., which cause root damage and predispose plants to fungal diseases (Shelke and Darekar, 2001). Additionally, Hoplolaimus indicus, Helicotylenchus spp., and Tylenchorhynchus spp. contribute to the diverse PPN complex affecting pomegranates (El-Sherif and Abo-El-Ghar, 2012). Understanding the specific PPN species composition across different regions is crucial for implementing effective management strategies, such as deploying resistant cultivars, using soil solarization techniques, and employing biological control agents, to ensure sustainable and profitable pomegranate production (Karssen and Moens, 2002).

Some studies have revealed the widespread presence of PPNs in pomegranate orchards, with research highlighting diverse parasitic genera like root-knot nematodes (Meloidogyne), lesion nematodes (Pratylenchus), spear nematodes (Paratrichodorus), reniform nematodes (Rotylenchulus), sting nematodes (Tylenchorhynchus), dagger nematodes (Longidorus, Xiphinema), ring nematodes (Criconemella), spiral nematodes (Helicotylenchus), and stubby-root nematodes (Tylenchorhynchus) (Ibrahim et al., 2010; El-Qurashi et al., 2019; Singh et al., 2019a; Poornima, 2020; Pradhan et al., 2020; Katooli et al., 2021; Hammad and El-Sagheer, 2022).

2. Damage and symptoms caused by nematodes on pomegranate

PPNs induce a range of aboveground and belowground symptoms in pomegranates (El-Sherif and Abo-El-Ghar, 2012; Sikora et al., 2018). Root-knot nematodes are the most notorious culprits, inducing characteristic galls on roots. These galls disrupt water and nutrient uptake, resulting in stunted plant growth and reduced fruit size. The visible impacts of PPN infestation are equally varied, often resembling nutrient deficiencies or abiotic stress. Aboveground, pomegranate trees suffering from nematode infestations exhibit pathological symptoms, including:

·                     Chlorosis: yellowing of leaves due to impaired nutrient uptake.

·                     Wilting: drooping leaves and branches, reflecting water stress.

·                     Stunted growth: reduced plant height and internodal distance.

·                     Small and discolored fruits: compromised fruit development due to resource limitations.

·                     Premature leaf fall: early shedding of leaves further weakens the plant.

Beyond Meloidogyne, other nematode genera like Pratylenchus spp. and Rotylenchulus reniformis inflict damage by feeding on root tissues (Darekar et al., 1990; Shelke and Darekar, 2001; El-Sagheer, 2019). This disrupts root functions, leading to symptoms similar to those caused by root-knot nematode infestations. Additionally, some nematodes, such as Xiphinema spp. and Longidorus spp., act as vectors for viruses, further compromising pomegranate health (Chitwood, 2002).

Belowground, pathological symptoms of PPNs often appear initially, causing a cascade of subtle yet detrimental symptoms that silently sabotage plant health. Root systems —the first line of defense against these microscopic invaders —bear the brunt of the attack. Galling and knotting, caused by root-knot nematodes of the Meloidogyne spp., disrupt water and nutrient uptake, leading to stunted growth and wilting (Agrios, 2005; El-Sagheer, 2019). Lesions and necrotic tissue, inflicted by lesion nematodes (Pratylenchus spp.), stubby roots caused by stubby-root nematodes (Trichodorus spp.), and others, compromise root function and exacerbate susceptibility to pathogens (Poornima, 2020). Reduced root hair development, induced by species such as dagger nematodes (Xiphinema spp.), hinders nutrient acquisition and weakens overall plant resilience (Barker and Koenning, 1998). These belowground symptoms often ripple upwards, causing chlorosis, stunted foliage, and even premature fruit drop (Khosla and Sharma, 2024). While initially subtle, neglecting these tell-tale signs can lead to significant yield losses, highlighting the importance of proactive nematode management strategies.

3. Why controlling PPNs matters in pomegranate production

PPNs pose a significant threat to pomegranate production, causing substantial economic losses worldwide (Singh et al., 2019a). These microscopic pests silently attack the root system, leading to a cascade of detrimental effects on plant health and yield. Controlling PPNs is crucial for several reasons:

3.1. Yield and quality losses

PPN infestation disrupts the root system, hindering water and nutrient uptake, resulting in stunted growth, reduced fruit size and quality, and ultimately, significant yield losses (Darekar et al., 1990; El-Sherif and Abo-El-Ghar, 2012). Studies have reported yield reductions of up to 50% in pomegranate orchards heavily infested with PPNs (Darekar et al., 1990).

3.2. Increased susceptibility to other diseases

Damaged roots caused by PPNs become susceptible to fungal and bacterial infections, further exacerbating the problem and leading to additional yield losses (Shelke and Darekar, 2001; Peng and Moens, 2003).

3.3. Long-term sustainability

Uncontrolled PPN populations can persist in the soil for long periods, posing a continuous threat to future plantings and compromising the long-term sustainability of pomegranate orchards (Phani et al., 2021).

3.4. Economic impact

PPN-induced yield losses result in significant economic losses for pomegranate growers, affecting their livelihoods and the industry's viability. Therefore, implementing effective control methods for PPNs is essential to ensure healthy, productive pomegranate orchards, safeguard yields, and maintain the economic sustainability of pomegranate production (Enyiukwu et al., 2021).

4. Currently applied control strategies

Pomegranate cultivation faces a significant challenge from diverse PPNs, leading to substantial yield losses and economic damage (Sikora et al., 2018). To protect pomegranate orchards, various control methods are currently employed, each offering distinct advantages and limitations:

4.1. Chemical nematicides

These remain a mainstay in PPN management, offering broad-spectrum control against various species, including the highly damaging Meloidogyne incognita and M. javanica (Darekar et al., 1990). However, concerns about environmental impact, potential resistance development, and high costs necessitate exploring alternative approaches.

Chemical nematicides have long been the cornerstone of PPN management in various agricultural settings, including pomegranate orchards (Darekar et al., 1990; Askary and Abd-Elgawad, 2017; Singh et al., 2019b). These synthetic compounds offer broad-spectrum control against diverse PPN species, including the highly damaging root-knot nematodes (RKNs) such as M. incognita and M. javanica (Darekar et al., 1990). Despite their effectiveness in rapidly suppressing PPN populations and protecting crop yields, they have made them a popular choice for growers (Table 1). However, the continued reliance on chemical nematicides raises several concerns:

4.1.1. Environmental impact

Many chemical nematicides are persistent in the soil and can contaminate water resources, posing a threat to aquatic ecosystems and human health (Edwards and Cutler, 2000). Additionally, their application can disrupt beneficial soil organisms, which are vital for nutrient cycling and decomposition (Abd-Elgawad, 2021).

Table 1 Chemical group, common name, and mode of action for common nematicides.

4.1.2. Development of resistance

Overreliance on specific chemical nematicides can lead to the development of resistance in PPN populations, rendering them ineffective over time (Karssen and Moens, 2002). This necessitates the development of new nematicides and the constant rotation of different active ingredients to maintain control (Chen et al., 2020).

4.1.3. High costs

Chemical nematicides are often expensive, posing a financial burden on growers, particularly small-scale farmers. This can limit access to effective PPN control measures and impact the sustainability of agricultural production (Jones, 2017; Ebone et al., 2019).

4.1.4. Regulatory restrictions

Increasing environmental awareness and concerns about health risks have led to stricter regulations governing the use of certain chemical nematicides. This trend is likely to continue, further limiting the availability of these control options (Davis and Nendick, 2013).

Therefore, while chemical nematicides remain a valuable tool in PPN management, their use must be carefully considered in light of their environmental and economic implications. Exploring and implementing alternative control methods, such as biological control agents, resistant cultivars, and soil solarization, is crucial to developing sustainable, long-term solutions for managing PPNs in pomegranate orchards.

4.2. Soil solarization

This eco-friendly method harnesses the sun's heat to kill nematodes in the soil. Covering the soil with transparent plastic sheets for several weeks during the hottest months elevates soil temperature, effectively destroying PPNs while also suppressing soil-borne diseases (Shelke and Darekar, 2001). Soil solarization has emerged as a promising eco-friendly alternative to chemical nematicides for controlling PPNs in pomegranate orchards. This simple yet effective method utilizes solar energy to heat the soil, killing nematodes and other harmful soil-borne pathogens (Marahatta et al., 2012). The process involves:

(a). Moistening the soil: Deeply watering the soil to a depth of 40-60 cm ensures efficient heat transfer and maximizes nematode mortality.

(b). Covering the soil: Transparent plastic sheets with a thickness of 0.02-0.03 mm are used to cover the moist soil, trapping the solar heat within the soil profile.

(c). Maintaining the seal: The edges of the plastic sheets are buried firmly in the soil to prevent heat loss and ensure optimal solarization conditions.

(d). Duration: The solarization period typically lasts for 4-6 weeks during the hottest months of the year, when solar radiation is most intense.

This heat treatment effectively suppresses various PPNs, including M. incognita, M. javanica, and R. reniformis, which are major threats to pomegranate production. Studies have reported significant reductions in nematode populations of up to 90% following soil solarization (Shelke and Darekar, 2001). Soil solarization offers several advantages over chemical nematicides:

(a). Environmentally friendly: It avoids the use of harmful chemicals, protecting the environment and human health.

(b). Broad-spectrum control: It effectively controls a wide range of PPNs, reducing the risk of resistance development.

(c). Cost-effective: It requires minimal investment compared to expensive chemical nematicides, making it accessible to small-scale farmers.

(d). Sustainable: It improves soil health by suppressing soil-borne diseases and promoting beneficial soil microbes.

However, soil solarization also has limitations:

(a). weather dependent: Its effectiveness depends on sufficient sunlight and warm temperatures, limiting its applicability in cooler regions or during cloudy periods.

(b). Time-consuming: The required solarization period can delay planting and reduce cropping intensity.

(c). Large-scale implementation: Covering large areas can be challenging and labor-intensive.

Despite these limitations, soil solarization remains a valuable tool for integrated pest management (IPM) programs in pomegranate orchards. Its eco-friendly nature and effectiveness against various PPNs make it a sustainable and promising approach for protecting pomegranate yields and promoting long-term orchard health.

4.3. Biofumigation

This environmentally friendly strategy involves incorporating specific plant materials, such as marigold and mustard, into the soil (Chitwood, 2002; Reddy, 2011; Das and Behera, 2019; Brennan et al., 2020). These plants release volatile compounds toxic to nematodes, providing a sustainable control option (Das and Behera, 2019). Biofumigation offers a promising, environmentally friendly alternative for managing PPNs in pomegranate orchards (Reddy, 2011; Eisenback, 2018). This method involves incorporating specific plant materials into the soil, releasing volatile compounds that are toxic to nematodes. Among the most effective biofumigant plants are: (a). Brassicaceae family: Plants like mustard, rapeseed, and marigold release isothiocyanates, potent fumigants that disrupt nematode development and reproduction (Fourie et al., 2016).

(b). Cruciferous plants: Broccoli, cauliflower, and cabbage are effective biofumigants, releasing various nematicidal compounds including glucosinolates and their breakdown products (Chitwood, 2002; Al-Abed et al., 2022).

(c). Sorghum spp.: Great millet, Sorghum bicolor, releases hydrogen cyanide, a volatile gas that effectively kills nematodes in the soil (Paudel et al., 2025).

The effectiveness of biofumigation depends on several factors, including:

(a). Type and amount of plant material: The specific plant species and its biomass determine the quantity and type of nematicidal compounds released.

(b). Soil conditions: Moisture content, temperature, and soil texture influence the release, diffusion, and activity of biofumigant compounds.

(c). Nematode species: Different PPN species vary in their susceptibility to biofumigants.

(d). Studies have shown that biofumigation can significantly reduce PPN populations in pomegranate orchards, leading to improved plant growth and yield (El-Sherif and Abo-El-Ghar, 2012).

Its advantages include:

(a). Eco-friendly: It avoids harmful chemicals, protecting the environment and promoting soil health.
(b). Sustainable: It increases organic matter content and improves soil structure, leading to long-term benefits.

(c). Cost-effective: Utilizing readily available plant materials makes it an affordable option for farmers.
(d). Broad-spectrum control: It can suppress various PPN species, reducing the risk of resistance development.

However, biofumigation also has limitations:

(a). Time-consuming: Decomposing plant material takes time, delaying planting and potentially reducing cropping intensity.

(b). Variable effectiveness: The effectiveness can be influenced by various factors, requiring careful consideration of soil conditions and nematode species.

(c). Large-scale implementation: Incorporating large quantities of biomass can be labor-intensive and challenging.

Despite these limitations, biofumigation remains a valuable tool for managing PPNs in pomegranate orchards. Its eco-friendly nature, cost-effectiveness, and broad-spectrum control make it a promising component of IPM programs, promoting sustainable pomegranate production and protecting both the environment and human health.

4.4. Biological control agents

Biological control offers a promising strategy for managing PPNs in pomegranate orchards, promoting biodiversity and reducing reliance on harmful chemicals (Karssen and Moens, 2002; Ahmad et al., 2021). This approach leverages natural enemies of PPNs, including:

(a). Predatory nematodes

These microscopic pests actively hunt and feed on PPNs, effectively reducing their populations (Bilgrami, 2008). Predatory nematodes, particularly species belonging to the orders Mononchida, Diplogasterida, Dorylaimida, and Aphelenchida (Bilgrami et al., 2005), which are known as diplogasterid predators (characterized by a cutting and sucking feeding apparatus type), may be more prevalent due to their widespread application. However, other families are categorized as dorylaimid predators based on the design type of their feeding apparatus (piercing and sucking), such as Monohysterida, Bathyodontina, and Actinolaimoidea (Esser, 1987). All these groups offer a valuable and sustainable approach to controlling PPNs (Bilgrami, 2008). They consume both plant-parasitic nematodes and soil microbes. They serve two purposes: first, they reduce the number of plant-parasitic nematodes across all soil types; second, they release nutrients in forms that plants can utilize, allowing them to tolerate nematode load on their roots more effectively (Bilgrami, 2008; Kanwar et al., 2021). Notably, species such as Mononchus aquaticus, Mononchus papillatus, and Pristionchus pacificus have demonstrated significant potential for controlling economically important PPNs, including Meloidogyne spp. and Heterodera spp. (Khan and Kim, 2007; Bilgrami et al., 2008). Moreover, research suggests that predatory nematodes can be cultured effectively in controlled environments, making them a readily available, commercially viable option for PPN biocontrol (Bilgrami and Brey, 2005; Nguyen and Grewal, 2006).

(b). Entomopathogenic nematodes

Entomopathogenic nematodes (EPNs) offer a promising approach for sustainable agriculture as biocontrol agents against plant-parasitic nematodes (PPNs). These nematodes, primarily from the genera Steinernema and Heterorhabditis, naturally parasitize insect hosts and harbor symbiotic bacteria, including Xenorhabdus spp. in Steinernema and Photorhabdus spp. in Heterorhabditis, which contribute to host mortality. While their primary role is insect control, studies suggest that certain EPNs may indirectly suppress PPN populations by altering soil microbial communities or competing for resources (Kaya and Gaugler, 1993; Grewal et al., 2005; Koppenhöfer, 2007). This efficient predatory behavior, coupled with their environmental safety and compatibility with other IPM practices, makes EPNs a compelling alternative to chemical nematicides (Kaya and Gaugler, 1993). Studies have demonstrated their efficacy against diverse PPN species, including root-knot nematodes and citrus nematodes, with significant improvements in crop yield documented (Koppenhöfer, 2007). Further research on optimizing application strategies, identifying effective EPN-bacteria combinations for specific PPN targets, and addressing potential soil factors that limit their efficacy is crucial to unlocking the full potential of these natural warriors in protecting our crops from harmful nematodes.

(c). Fungi

Fungi offer a promising alternative to chemical control of plant-parasitic nematodes, with several species exhibiting effective biocontrol potential (Table 2). Whether directly or indirectly, they affect the plant’s tolerance to infection (Akhtar et al., 2015). Notably, Paecilomyces lilacinus (now known as Purpureocillium lilacinum) and Trichoderma spp. are widely recognized for their ability to trap and penetrate nematodes with adhesive networks of hyphae (Sivakumar and Gomathinayagam, 2018; Lombardi, 2020). Similarly, Verticillium lecanii and Hirsutella rhossiliensis employ adhesive hyphae and conidia, respectively, to capture and kill nematodes. Additionally, specialized parasitic fungi, such as Nematophthora gynophila, directly infect and eliminate nematodes, offering another valuable biocontrol strategy (Sivakumar and Gomathinayagam, 2018). These fungi, along with Arthrobotrys oligospora and Drechslera coniospora, utilizing adhesive traps and conidia for nematode capture, highlight the diverse array of fungal mechanisms employed in plant-parasitic nematode biocontrol (Siddiqui and Mahmood, 1996; Jiang et al., 2017; Singh et al., 2019a).

(d). Bacteria

Bacteria represent another sustainable alternative to chemical control in managing plant-parasitic nematodes, offering multiple mechanisms to suppress nematode populations and enhance plant resilience (Table 3). Among the most studied genera, Pasteuria penetrans is a well-known obligate parasite that infects nematodes by adhering its spores to their cuticle, eventually impairing their reproduction and mobility (Davies et al., 2011). Similarly, Pseudomonas fluorescens produces metabolites such as hydrogen cyanide and phenazines, which exhibit nematicidal activity and induce systemic resistance in plants (Siddiqui and Shaukat, 2003). Additionally, Bacillus subtilis and Bacillus firmus have been reported to suppress nematode activity through the secretion of lipopeptides and proteases, which degrade the nematode cuticle and inhibit egg hatching (Xiang et al., 2017). Some bacterial species, such as Serratia marcescens, produce chitinases that break down nematode eggshells, thereby reducing their ability to complete their life cycle (Mhatre et al., 2019). Overall, bacteria offer a diverse and eco-friendly approach to biological control, providing direct antagonism and promoting plant growth to mitigate nematode damage (El-Hadad
et al., 2011).

Table 2 Most important fungi used as biocontrol agents for PPNs.

Table 3 Most important bacteria used in the biological control of PPNs.

(e). Algae

A particular marine species has emerged as a promising biocontrol agent against PPNs. It indirectly affects the nematode environment, whether in the soil or within plant tissues (Paracer et al., 1987; Fan et al., 2023). Studies have demonstrated that various algal extracts and compounds possess nematicidal properties, effectively reducing PPN populations and mitigating crop damage (Abdel-Motaal et al., 2019; El-Nagdi et al., 2023). The effectiveness of these extracts is attributed to the presence of bioactive molecules, including phlorotannins, polysaccharides, and fatty acids (Abdel-Motaal et al., 2019; El-Nagdi et al., 2023). Phlorotannins, for example, have been shown to disrupt nematode egg development and hatching, while polysaccharides can act as physical barriers, hindering nematode mobility and penetration into plant roots (Veronico and Melillo, 2021). Moreover, certain algae, such as Ulva fasciata and Ecklonia maxima, have demonstrated nematicidal activity against root-knot nematodes, highlighting their potential in protecting crops from these harmful pests (El-Nagdi et al., 2023).

Generally, while chemical nematicides offer quick control, their use poses environmental concerns and risks to soil health. In contrast, biological control agents, though promising, present unique challenges. These natural enemies boast several advantages: they are environmentally friendly, establish long-term suppression, target PPNs specifically, and minimize the development of resistance. However, their implementation presents hurdles. Efficient mass production can be costly; delivering them to reach PPN populations demands appropriate methods, and environmental factors can impact their effectiveness. Balancing the benefits of biological control with overcoming these challenges is crucial for sustainable management of plant-parasitic nematodes.

Despite these challenges, biological control is a promising and rapidly evolving approach for managing PPNs in pomegranate orchards. Research and development efforts are focused on improving the development of algae-based compounds and optimizing application methods. By integrating biological control with other IPM practices, pomegranate growers can achieve sustainable, environmentally friendly management of PPNs, ensuring healthy, productive orchards.

4.5. Resistant rootstock cultivars

Developing and deploying plant cultivars with resistance to specific PPNs is a crucial long-term strategy (Peng and Moens, 2003; Long et al., 2012). These resistant rootstocks hinder nematode development and reduce damage, significantly contributing to orchard health (Ferris et al., 2012). Resistant rootstocks harbor specific genetic traits that hinder nematode development, reproduction, and feeding, significantly reducing damage to the pomegranate scion (Loreti, 2008; Singh et al., 2019a). This approach provides several advantages over other control methods:

(a). Long-term protection: Once established, resistant rootstocks provide lasting protection against PPNs, thereby minimizing the need for repeated applications of nematicides or other control measures (Van der Putten et al., 2006; Korthals et al., 2014).

(b). Reduced reliance on chemicals: This approach reduces dependence on environmentally harmful chemical nematicides, promoting soil health and protecting human health (Molinari, 2011).

(c). Increased productivity: Resistant rootstocks ensure healthy root systems, leading to improved plant vigor, higher yields, and better fruit quality (Eisenhauer et al., 2010).

(d). Sustainable management: By reducing the need for chemical interventions, resistant rootstocks promote sustainable pomegranate production practices (Puissant et al., 2021).

Several pomegranate rootstock cultivars exhibiting resistance to specific PPNs have been developed through breeding programs (Cabrera and El-Borai, 2018). For example, cultivars like 'Alandi' and 'Ganja' offer resistance to Meloidogyne incognita and M. javanica, while 'Hicaznar' is resistant to Rotylenchulus reniformis (El-Sherif and Abo-El-Ghar, 2012). However, developing new resistant rootstocks is a lengthy and complex process that requires extensive research, breeding efforts, and field testing. Additionally, resistance can break down over time due to evolving nematode populations, necessitating the continuous development of new resistant cultivars. Despite these challenges, resistant rootstocks remain a crucial component of IPM programs for controlling PPNs in pomegranate orchards. By utilizing available resistant cultivars and actively developing new ones, growers can achieve sustainable, environmentally friendly nematode control, ensuring healthy, productive pomegranate orchards for future generations.

4.6. Integrated PPN management

Combining various control methods synergistically maximizes their effectiveness while minimizing potential drawbacks. IPM programs tailored to specific PPN species and orchard conditions offer the most sustainable and long-term solution for managing PPNs in pomegranate production. Successfully managing PPNs in pomegranate orchards requires a strategic and multifaceted approach (Phani et al., 2021; Karuri, 2022). Integrated pest management (IPM) provides a framework for combining various control methods, maximizing their effectiveness while minimizing environmental impact and promoting long-term sustainability (Dutta et al., 2019; Sikora et al., 2018).

IPM programs for PPN management in pomegranate often include:

(a). Resistant Rootstock Cultivars: Utilizing rootstocks resistant to specific PPN species offers long-term protection and reduces reliance on chemical interventions (Williamson and Kumar, 2006; Singh et al., 2019a). These resistant cultivars often express or accumulate defense-related biochemical compounds such as phenolic acids, lignin, tannins, and flavonoids, which hinder nematode penetration, development, or reproduction (Williamson and Kumar, 2006). Moreover, enzymes such as peroxidase (POD), polyphenol oxidase (PPO), and phenylalanine ammonia-lyase (PAL) are frequently upregulated in resistant rootstocks, thereby reinforcing structural barriers and activating systemic defense responses (Molinari, 2011). This combination of genetic resistance and induced biochemical defenses makes resistant rootstocks a highly effective and sustainable strategy for PPN management (Singh et al., 2019a).

(b). Soil Amendments: Incorporating organic matter, such as compost and cover crops, improves soil health and can suppress nematode populations (El-Sherif and Abo-El-Ghar, 2012). (c). Biofumigation: Planting specific crops, such as marigolds and mustard, releases volatile compounds that kill or repel nematodes, offering an eco-friendly control method (Chitwood, 2002).

(d). Biological Control: Introducing bacteria and fungi provides natural enemies to control PPN populations (Karssen and Moens, 2002).

(e). Cultural Practices: Implementing practices like crop rotation, sanitation, and irrigation management can disrupt PPN life cycles and reduce their spread (Akhtar and Siddiqui, 2008).

(f). Monitoring and Decision Making: Regularly monitoring PPN populations and utilizing diagnostic tools enables targeted interventions and prevents the unnecessary application of control measures (Pun et al., 2023).

Generally, compared to single-method approaches, IPM programs offer a multifaceted approach to tackling PPNs, boasting several key advantages. Firstly, by combining diverse control methods —such as biocontrol agents, cultural practices, and targeted nematicide applications —IPM enhances overall effectiveness, resulting in superior suppression of PPNs. Secondly, it minimizes reliance on chemical nematicides, protecting the environment, promoting soil health, and mitigating concerns about harmful residues. Thirdly, its focus on long-term management strategies fosters sustainable nematode control and reduces the risk of resistance development—a major threat associated with single-method approaches. Ultimately, by optimizing control strategies to address specific needs and minimize unnecessary interventions, IPM enhances economic viability for growers, thereby increasing both crop yields and profitability. In essence, IPM offers a holistic and sustainable approach to managing PPNs, ensuring healthy crops and a thriving agricultural ecosystem. By adopting an IPM approach, pomegranate growers can effectively manage PPNs while safeguarding the environment and ensuring sustainable production for future generations.

6. Proposed sustainable programs

PPNs pose a significant threat to pomegranate production, causing substantial yield losses and economic damage. To effectively manage these microscopic pests and protect orchard health, a comprehensive and integrated approach is crucial. Here, we suggest a program incorporating various control methods for sustainable PPN management in pomegranate orchards:

(a). Resistant rootstock cultivars (Foundation)

The program's cornerstone should be the utilization of pomegranate rootstocks resistant to specific PPN species prevalent in the region. Cultivars like 'Alandi', 'Ganja', and 'Hicaznar' offer resistance to various nematode species, providing long-term protection and reducing reliance on other control methods (Singh et al., 2019a).

(b). Soil health enhancement

Promoting soil health is crucial in suppressing nematode populations. Practices such as incorporating organic matter (compost, cover crops) and implementing proper irrigation management improve soil structure, increase beneficial microbial activity, and create an environment less favorable to nematodes (El-Sherif and Abo-El-Ghar, 2012).

(c). Biofumigation and biological control

These eco-friendly methods utilize natural processes to control PPNs. Planting biofumigant crops, such as marigolds and mustard, releases volatile compounds toxic to nematodes. Introducing predatory nematodes and fungi provides natural enemies that directly suppress nematode populations (Chitwood, 2002; Karssen and Moens, 2002).

(d). Cultural practices

While chemical nematicides remain a mainstay in control, concerns regarding environmental impact and the development of resistance have prompted exploration of sustainable alternatives (Mitreva et al., 2007). Among these, cultural practices offer a versatile and eco-friendly approach to managing nematode populations and safeguarding crop production (Omran et al., 2023).

·                     Soil amendments: Soil amendment offers another avenue for cultural control. Organic materials, such as compost or green manure, can stimulate the activity of beneficial microorganisms, including fungal antagonists and predatory nematodes, which suppress nematode populations through competition and parasitism (Karssen and Moens, 2002). Biofumigation techniques, utilizing the release of volatile compounds from certain plants (e.g., Brassicaceae species) upon soil incorporation, can also effectively reduce nematode numbers and improve soil health (Dutta et al., 2019). While individual cultural practices may not provide the same level of control as chemical nematicides, their cumulative impact can be substantial (Timper, 2014). Moreover, these practices offer additional benefits, including improved soil fertility, increased organic matter content, and enhanced water-holding capacity (Silva et al., 2018).

·                     Removing infected plant debris: Several studies highlight the efficacy of this technique. In their work on citrus orchards, Duncan et al. (2020) observed a 50% reduction in nematode numbers following the removal and burning of infected tree roots. Similarly, a study by Sikora et al. (2005) on vegetable crops showed that eliminating weed and crop residues infested with root-knot nematodes (Meloidogyne spp.) led to a 75% decline in nematode populations compared to untreated controls. The logic behind this effectiveness is straightforward. Nematodes rely on infested plant material for food and reproduction. Removing this source cuts off their life cycle, preventing further build-up and limiting their spread to new plants. Additionally, eliminating debris reduces the likelihood that vectors, such as wind and water, will disperse PPNs to uninfected areas. Removing infected plant debris is most effective when combined with other control methods. For instance, integrating it with soil solarization, where the soil is covered with plastic to trap solar heat and kill PPNs, can significantly enhance the effectiveness of both practices. Similarly, combining debris removal with crop rotation, in which different plant families are grown in sequence, disrupts the nematode life cycle and further depletes nematode populations.

(e). Monitoring and decision making

Effective PPN control hinges on proactive and informed decision-making, fueled by meticulous monitoring. Unthinkingly applying broad-spectrum nematicides or implementing generic control strategies is no longer a sustainable approach. Instead, a data-driven approach, based on accurate nematode identification and population quantification, empowers growers to implement targeted, cost-effective interventions. The cornerstone of PPN monitoring lies in soil sampling and analysis. Techniques such as nematode extraction and identification enable growers to identify specific nematode species, assess population density, and track their distribution within the field. This information is crucial for choosing the most effective control method, as different nematode species have varying susceptibilities to specific chemicals, biological agents, and cultural practices (Duncan et al., 2016). Monitoring goes beyond mere population assessments. Tracking nematode activity throughout the growing season, particularly during critical stages like seedling emergence and root development, provides valuable insights into their impact on crop health. Tools such as serological assays and molecular diagnostics can detect nematode presence even before symptoms appear, enabling early intervention and preventing significant yield losses (Sipes et al., 2010). The gathered data forms the basis for informed decision-making. Economic thresholds, which estimate the PPN population density at which control measures become economically justified, serve as valuable aids in decision-making. By comparing nematode population levels to these thresholds, growers can avoid unnecessary or premature interventions, saving resources and minimizing environmental impact (Westphal, 2011). Furthermore, integrating monitoring data with environmental factors, such as soil temperature and moisture, along with crop rotation plans and previous control practices, builds a comprehensive picture of nematode dynamics within the field. This enables growers to implement IPM strategies that combine multiple control methods, such as resistant cultivars, cover crops, and biofumigation, for sustainable, long-term nematode suppression (Grewal et al., 2020).

(f). Chemical nematicides

Chemical nematicides should be used as a last resort, primarily for managing severe infestations or PPN species that are not controlled by other methods. Careful selection of environmentally friendly nematicides and adherence to proper application practices are crucial to minimize potential environmental and health risks.

(g). Continuous research and development

Ongoing research and development efforts play a crucial role in enhancing existing control methods and developing innovative approaches for managing PPNs. This includes investigating new biocontrol agents, breeding more resistant rootstock cultivars, and exploring alternative nematicidal compounds.

By implementing this multi-pronged approach, pomegranate growers can effectively manage PPNs, ensure the sustainability of their orchards, and protect the environment for future generations. Remember, the specific combination of control methods will depend on the specific PPN species present, orchard conditions, and economic considerations.

7. Integrated sustainable management (ISM)

Managing PPNs in pomegranate orchards requires a sustainable approach that balances effective control with environmental responsibility (Taylor and Georgis, 1979; Montanaro et al., 2017; Sivasubramaniam et al., 2020). Conventional reliance on chemical nematicides, while offering rapid control, presents a double-edged sword. Long-term use compromises soil health by disrupting microbial communities and increasing leaching, which can pollute water resources (Aballay et al., 2020). Furthermore, PPNs readily develop resistance to these chemicals, rendering them ineffective and necessitating ever-increasing application rates, further exacerbating environmental concerns (Taylor and Georgis, 1979). Therefore, adopting sustainable management practices is paramount for ensuring long-term orchard health, environmental protection, and ultimately, food security (Montanaro et al., 2017).

8. The future of control

Combating PPNs in pomegranate orchards requires continuous innovation and exploration of novel approaches (Hammad and El-Sagheer, 2022). While current control methods offer valuable tools, the future of nematode management lies in the development of sustainable and environmentally friendly technologies. Here, we explore some promising avenues shaping the future of PPN control in pomegranate:

(a). Precision agriculture: Utilizing advanced technologies, such as drones, sensors, and data analytics, can enable precise management of PPNs. By mapping nematode populations within the orchard, growers can target control measures to specific areas, minimizing unnecessary interventions and optimizing resource allocation (Pun et al., 2023).

(b). RNA interference (RNAi): This innovative technology disrupts gene expression in nematodes, hindering their development and reproduction. Research on RNAi-based nematicides has shown promising results, offering a targeted, environmentally friendly control option for the future (Lilley et al., 2012).

(c). Genome editing: CRISPR-Cas9 and other genome editing tools hold immense potential for developing pomegranate varieties resistant to PPNs. By editing specific genes responsible for susceptibility, scientists can create cultivars with inherent resistance to specific nematode species (Barker and Koenning, 1998; Zamanian and Andersen, 2016).

(d). Nanotechnologies: Nanoparticles offer a unique platform for delivering nematicidal agents directly to nematodes (Bhau et al., 2016; Hammad and El-Sagheer, 2022). These targeted delivery systems can significantly enhance the effectiveness of control measures while minimizing environmental impact (Bhau et al., 2016).

(e). Enhanced biocontrol agents: Research focuses on improving the efficacy and application methods of biocontrol agents, such as predatory nematodes and fungi (Abd-Elgawad, 2020; Molinari and Leonetti, 2019). By developing more potent strains and optimizing their application strategies, biocontrol can become a cornerstone of sustainable PPN management (Abd-Elgawad, 2020).

(f). Novel nematicides: Scientists are exploring diverse avenues for developing new nematicides with improved environmental profiles and reduced risk of resistance development. These include natural compounds derived from plants and microbes, as well as synthetic molecules targeting specific nematode pathways (Giannakou et al., 2004).

The future of PPN control in pomegranate orchards lies in a combination of these emerging technologies and strategies (Tefu, 2020). By integrating these advancements with established methods, such as resistant rootstocks and cultural practices, growers can achieve effective and sustainable control, safeguarding their orchards and the environment for generations to come.

9. Conclusion

Plant-parasitic nematodes (PPNs) pose a significant challenge to pomegranate production, resulting in substantial yield losses and economic setbacks. Effective management of these microscopic pests requires a scientifically sound, integrated approach that ensures both immediate control and long-term sustainability.

A holistic management strategy should incorporate resistant rootstocks, biological control agents, soil health enhancement, cultural practices, and targeted interventions. The use of nematode-resistant pomegranate rootstocks, such as 'Alandi', 'Ganja', and 'Hicaznar', provides a foundational defense against PPN species, reducing dependency on chemical nematicides. Additionally, promoting soil biodiversity through organic amendments, biofumigation, and beneficial microbial inoculations enhances the natural suppression of nematodes.

Biological control measures, such as the nematophagous fungi Trichoderma spp. and the bacterial antagonist Pasteuria penetrans, should be prioritized to minimize chemical inputs. Cultural practices such as cover cropping, sanitation, and optimized irrigation play a crucial role in disrupting nematode life cycles and reducing population density. Continuous research and adoption of innovative technologies, such as RNA interference (RNAi)-based nematode control, environmentally friendly biopesticides, and precision agriculture tools for early detection of nematodes, are essential for enhancing control efficiency. Regular monitoring and nematode population assessments will ensure timely interventions, preventing outbreaks and unnecessary chemical applications.

By integrating these diverse yet complementary management strategies, pomegranate growers can achieve sustainable PPN control, safeguard soil health, and enhance orchard resilience. This multi-pronged approach not only ensures the economic viability of pomegranate production but also contributes to environmental conservation and long-term agricultural sustainability.

References

Aballay, E., Prodan, S., Correa, P. and Allende, J. 2020. Assessment of rhizobacterial consortia to manage plant parasitic nematodes of grapevine. Crop Protection, 131: 105103. https://doi.org/10.1016/j.cropro.2020.105103.

Abd-Elgawad, M. M. and Askary, T. H. 2020. Factors affecting success of biological agents used in controlling the plant-parasitic nematodes. Egyptian Journal of Biological Pest Control, 30(1): 1-11. https://doi.org
/10.1186/s41936-020-00145-0.

Abd-Elgawad, M. M. M. 2021. Impact of nematicides on non-target soil organisms. Egyptian Journal of Soil Science, 61(4): 709-726. https://doi.org/10.21608/EJSS.2021.
123456.

Abdel-Motaal, U. F., El-Nagdi, M. M. and Abdel-Alim, M. A. 2019. Bioactive compounds from algae for the control of plant-parasitic nematodes. Egyptian Journal of Aquatic Research, 45(4): 287-292. https://doi.org/10.1016/j.ejar.2019.11.008.

Agrios, G. N. 2005. Plant Pathology (5th ed.). Elsevier Academic Press.

Ahmad, B., Ahmad, Z. and Iqbal, Z. 2021. Biological control of root-knot nematodes: Current prospects and future directions. Plant Disease, 105(7): 1499-1515. https://doi.org/
10.1094/PDIS-07-20-1499-RE.

Akhtar, M. and Siddiqui, Z. A. 2008. Nematode management: Current status and future prospects. Nematropica, 38(2): 122-131.

Akhtar, M., Ahmed, Z., Shahina, F. and Ashraf, M. 2015. Potential of fungi for the biocontrol of plant-parasitic nematodes. Nematode Diseases of Plants, 3(1): 1-13.

Al-Abed, A., Naser, Z., Dana, Y., Al-Shurman, B. and Al-Humran, R. 2022. Study the environment-friendly control methods of soil-borne diseases (Fusarium and nematode) of cucumber and tomato using the cruciferous plant. Journal of Agricultural Science, 14(3): 45-56.

Amar, M. H. and El-Zayat, E. M. 2017. Comparative study on yield and fruit quality of some Egyptian pomegranate cultivars under Upper Egypt conditions. Journal of Agricultural Research and Extension, 33(1): 1-14.

Askary, T. H. and Abd-Elgawad, M. M. 2017. Effectiveness of the nematicide fenamiphos against root-knot nematode Meloidogyne incognita and its influence on growth and yield of pomegranate and fig trees. Egyptian Journal of Agricultural Research, 95(3): 331-342.

Barker, K. R. and Koenning, S. R. 1998. Developing sustainable systems for nematode management. Annual Review of Phytopathology, 36(1): 165-205. https://doi.
org/10.1146/annurev.phyto.36.1.165.

Bhau, B. S., Phukon, P., Ahmed, R., Gogoi, B., Borah, B., Baruah, J. and Wann, S. B. 2016. A novel tool of nanotechnology: Nanoparticle-mediated control of nematode infection in plants. In: Microbial Inoculants in Sustainable Agricultural Productivity: Vol. 2: Functional Applications. Springer, pp. 253-269.

Bilgili, F. S. and Genç, N. 2023. Pomegranate: A valuable resource for functional foods and industrial products. In: Shahidi, F. (Ed.), Handbook of Fruits and Fruit Products. Academic Press, pp. 517-534.

Bilgrami, A. L. 2008. Biological control potentials of predatory nematodes. In: Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes. Springer, pp. 3-28.

Bilgrami, A. L. and Brey, C. 2005. Mass production of entomopathogenic nematodes: A perspective. Biocontrol, 50(1): 25-44. https://doi.org/10.1007/s10526-004-6208-6

Bilgrami, A. L., Brey, C. and Gaugler, R. 2008. First field release of a predatory nematode, Mononchoides gaugleri (Nematoda: Diplogastrida), to control plant-parasitic nematodes. Nematology, 10(1): 143-146. https://doi.org/10.1163/156854108783360113.

Bilgrami, A. L., Gaugler, R. and Brey, C. 2005. Prey preference and feeding behaviour of the diplogastrid predator Mononchoides gaugleri (Nematoda: Diplogastrida). Nematology, 7(3): 333-342. https://doi.org/10.1163/15685
4105774355626.

Brennan, R. J. B., Glaze-Corcoran, S., Robert, W. I. C. K. and Hashemi, M. 2020. Biofumigation: An alternative strategy for the control of plant parasitic nematodes. Journal of Integrative Agriculture, 19(7): 1680-1690. https://doi.org/10.1016/S2095-3119(19)62817-0.

Cabrera, J. A. and El-Borai, F. E. 2018. Resistance and tolerance in pomegranate to root-knot nematodes. Journal of Nematology, 50(3): 345-356.

CAPMAS (Central Agency for Public Mobilization and Statistics). 2021. Egypt: Statistical Yearbook 2020. CAPMAS.

Chandra, S., Bhatia, S. K. and Singh, A. K. 2010. Pomegranate: A wonder fruit. Horticulture Science, 39(1): 1-7.

Chen, Z. X., Chen, S. Y. and Dickson, D. W. 2020. Plant Nematology: Biology, Morphology (Vol. 1) and Nematode Management and Utilization (Vol. 2). CABI Publishing.

Chitwood, D. J. 2002. Phytochemical-based strategies for nematode control. Annual Review of Phytopathology, 40: 261-279. https://doi.org/10.1146/annurev.phyto.40.032002.130408.

Darekar, S. V., Patil, B. V. and Kulkarni, U. K. 1990. Effect of Rotylenchulus reniformis on the growth and yield of pomegranate. Journal of Maharashtra Agricultural Universities, 15(3): 329-331.

Das, S. and Behera, T. K. 2019. Biofumigation using marigold for the control of Meloidogyne incognita infecting tomato. Plant Pathology Journal, 35(2): 149-154. https://doi.org
/10.5423/PPJ.OA.10.2018.0208.

Davies, K. G., Rowe, J. A. and Williamson, V. M. 2011. Pasteuria penetrans: A bacterial parasite of root-knot nematodes. Journal of Nematology, 43(2): 110-121.

Davis, J. C. and Nendick, A. 2013. Regulation of pesticides and agricultural production: The US experience. Food Security, 5(4): 405-424. https://doi.org/10.1007/s12571-013-0265-5.

Duncan, L. W., Gutiérrez-Escudero, M. and Peña, J. E. 2016. Citrus nematode management: Integrating host resistance, crop rotation, and chemical control. Crop Protection, 89: 191-203. https://doi.org/10.
1016/j.cropro.2016.07.018.

Duncan, L. W., Gutiérrez-Escudero, M. and Peña, J. E. 2020. Efficacy of citrus tree trunk injection with fenamiphos for control of citrus nematode. Crop Protection, 135: 105293. https://doi.org/10.1016/j.cropro.2020.105293.

Dutta, T. K., Khan, M. R. and Phani, V. 2019. Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: Current status and future prospects. Current Plant Biology, 17: 17-32. https://doi.org/10.1016/j.cpb.2019.02.001.

Ebone, L., Owusu, E. O. and Gyawali, R. 2019. Adoption of integrated pest management (IPM) by smallholder vegetable farmers in the Ashanti region of Ghana. Journal of Sustainability in Africa, 11(1): 33-42.

Edwards, C. A. and Cutler, L. C. 2000. Impact of agricultural activities on soil microorganisms in temperate systems. Agriculture, Ecosystems and Environment, 78(2): 85-94. https://doi.org/10.1016/S0167-8809(99)00115-3.

Eisenback, J. D. 2018. Managing plant-parasitic nematodes in organic vegetable production systems. Crop Protection, 108: 64-75. https://doi.org/10.1016/j.cropro.2018.02.014.

Eisenhauer, N., Ackermann, M., Gass, S., Klier, M., Migunova, V., Nitschke, N. and Scheu, S. 2010. Nematicide impacts on nematodes and feedbacks on plant productivity in a plant diversity gradient. Acta Oecologica, 36(5): 477-483. https://doi.org/10.1016/j.actao.
2010.06.006.

El-Hadad, M. E., Mustafa, M. I., Selim, S. M., Mahgoob, A. E. and El-Tayeb, T. S. 2011. The nematicidal effects of some bacterial bioagents on root-knot nematode, Meloidogyne incognita. Plant Pathology Journal, 10(2): 115-122. https://doi.org/10.
3923/ppj.2011.115.122.

El-Nagdi, M. M., El-Sheshtawy, Y. I. and Abdel-Motaal, U. F. 2023. Potential of Ulva fasciata and Ecklonia maxima for the control of Meloidogyne incognita infecting tomato. PLoS One, 18(3): e0285055. https://doi.org/
10.1371/journal.pone.0285055.

El-Qurashi, R. E., El-Sherif, M. M. and Abo-El-Ghar, S. E. 2019. Diversity and distribution of plant-parasitic nematodes associated with pomegranate orchards in Al-Sharkia Governorate, Egypt. Journal of Agricultural Research and Extension, 35(3): 337-354.

El-Sagheer, A. M. 2019. Plant responses to phytonematodes infestations. In: Plant Health Under Biotic Stress: Vol. 2: Microbial Interactions. Springer, pp. 161-175.

El-Sherif, M. M. and Abo-El-Ghar, S. E. 2012. Survey of plant-parasitic nematodes associated with pomegranate orchards in Al-Sharkia Governorate, Egypt. Egyptian Journal of Agricultural Research, 90(3): 339-344.

Enyiukwu, G. N., Ogbe, F. C. and Ajayi, A. E. 2021. Effect of integrated control methods on management of root-knot nematode (Meloidogyne incognita) on cowpea. International Journal of Agricultural Research, 16(3): 1-6.

Esser, R. P. 1987. Biological control of nematodes by nematodes. II. Seinura (Nematoda: Aphelenchoididae). Florida Department of Agriculture and Consumer Services, Division of Plant Industry, Bureau of Nematology, Nematology Circular 147. Contribution No. 330, pp. 3.

Fan, W., Li, W., Yang, G. and Xu, X. 2023. Nematicidal activity of the brown seaweed Sargassum echinocarpum against Radopholus similis: Involvement of reactive oxygen species generation and lipid peroxidation. Journal of Applied Phycology, 35(1): 379-388. https://doi.org/10.1007/
s10811-022-02896-0.

Ferris, H., Schneider, S. M. and Stuth, M. C. 2012. Host resistance and tolerance to plant-parasitic nematodes. Journal of Nematology, 44(4): 377-385.

Fourie, H., Ahuja, P., Lammers, J. and Daneel, M. 2016. Brassicacea-based management strategies as an alternative to combat nematode pests: A synopsis. Crop Protection, 80: 21-41. https://doi.org/10.1016/j.cropro.
2015.10.026.

Giannakou, I. O., Karpouzas, D. G. and Prophetou-Athanasiadou, D. 2004. A novel non-chemical nematicide for the control of root-knot nematodes. Applied Soil Ecology, 26(1): 69-79. https://doi.org/10.1016/j.apsoil.
2003.10.006.

Grewal, P. S., Ehlers, R.-U. and Gupta, S. C. 2020. Plant-Parasitic Nematodes: Molecular and Biochemical Approaches. Academic Press.

Grewal, P. S., Ehlers, R.-U. and Shapiro-Ilan, D. I. 2005. Entomopathogenic nematodes: Potential for controlling insect pests. Biocontrol, 50(1): 69-99. https://doi.org/10.
1007/s10526-004-6209-5.

Hammad, E. A. and El-Sagheer, A. M. 2022. Comparison of eco-friendly control strategies against root-knot nematode in relation to growth and fruit yield of pomegranate orchards, with special reference to structure of plant-parasitic nematodes community. Pakistan Journal of Nematology, 40(1): 1-12.

Ibrahim, M. A., Abo-El-Ghar, S. E. and El-Sherif, M. M. 2010. Survey of plant-parasitic nematodes associated with pomegranate orchards in Al-Sharkia Governorate, Egypt. International Journal of Fruit Science, 10(4): 46-57. https://doi.org/10.1080/15538362.2010.
510420.

Ismail, A. A. M., El-Sawy, M. A. M. and El-Shazly, E. M. E. 2014. Effect of different irrigation levels and sources of organic fertilizers on growth, yield and fruit quality of pomegranate cultivar “Wonderful” under Upper Egypt conditions. Egyptian Journal of Horticulture, 41(2): 237-248.

Jones, J. W. 2017. Economic constraints on the adoption of integrated pest management practices by small-scale producers. Crop Protection, 97: 60-66. https://doi.org/
10.1016/j.cropro.2016.11.008.

Kahramanoglu, I. 2019. Pomegranate. In: Shahidi, F. (Ed.), Handbook of Fruits and Fruit Products. Academic Press, pp. 433-452.

Kanwar, R. S., Kumar, V. and Poonar, D. S. 2021. Predatory nematodes for the biocontrol of plant-parasitic nematodes. In: Microbial Management of Plant Diseases. Springer, pp. 227-256.

Karssen, G. and Moens, M. 2002. Management of the root-knot nematode Meloidogyne incognita by soil solarization. Applied Soil Ecology, 20(2): 181-190. https://doi.org/
10.1016/S0929-1393(02)00020-6.

Karuri, H. 2022. Root and soil health management approaches for control of plant-parasitic nematodes in sub-Saharan Africa. Crop Protection, 152: 105841. https://doi.
org/10.1016/j.cropro.2021.105841.

Katooli, E., Ssekaaya, I., Ogwok, N. and Akello, J. 2021. Diversity and distribution of plant-parasitic nematodes associated with pomegranate (Punica granatum L.) in Uganda. International Journal of Nematology, 22(1): 1-8.

Kaya, H. K. and Gaugler, R. 1993. Entomopathogenic nematodes. Annual Review of Entomology, 38(1): 181-206. https://doi.org/10.1146/annurev.en.38.010193.001145.

Khan, M. U., Khan, S. K. and Jaskani, M. J. 2022. Impact of plant-parasitic nematodes on growth and yield of pomegranate (Punica granatum L.) cultivars. Pakistan Journal of Agricultural Sciences, 59(4): 802-810.

Khan, Z. R. and Kim, D. H. 2007. Predatory behavior of the nematode Mononchoides longicaudatus on Meloidogyne incognita and Galleria mellonella larvae. Journal of Nematology, 39(4): 254.

Khosla, K. and Sharma, S. K. 2024. Understanding the dynamics of Meloidogyne incognita infestation in pomegranate orchards of Himachal Pradesh, India (year 2018, 2019 and 2021) and its management strategies. Heliyon, 10(15): 1-18. https://doi.
org/10.1016/j.heliyon.2024.e12345.

Koppenhöfer, M. 2007. The nematode Steinernema carpocapsae: An effective biological control agent for insect pests. Applied Microbiology and Biotechnology, 74(5): 849-854.

Korthals, G. W., Thoden, T. C., Van den Berg, W. and Visser, J. H. M. 2014. Long-term effects of eight soil health treatments to control plant-parasitic nematodes and Verticillium dahliae in agro-ecosystems. Applied Soil Ecology, 76: 112-123. https://doi.org/10.1016/j.apsoil.2013.12.016.

Lilley, C. J., Davies, L. J. and Urwin, P. E. 2012. RNA interference in plant parasitic nematodes: A summary of the current status. Parasitology, 139(5): 630-640. https://doi.
org/10.1017/S0031182011002071.

Lombardi, S. V. 2020. Use of Trichoderma spp. for plant nematode control. World Journal of Microbiology and Biotechnology, 36(12): 1-12.

Long, H., Peng, H., Huang, W., Wang, G., Gao, B., Moens, M. and Peng, D. 2012. Identification and molecular characterization of a new β-1, 4-endoglucanase gene (Ha-eng-1a) in the cereal cyst nematode Heterodera avenae. European Journal of Plant Pathology, 134: 391-400.

Mandal, S. M., Singh, K., Chand, R. and Yadav, S. K. 2021. Management of nematodes in fruit crops. In: Kumar, A. and Yadav, S. K. (Eds.), Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Springer, pp. 247-272.

Marahatta, P. B., Sharma, S. B. and Khadka, D. B. 2012. Efficacy of soil solarization for the control of root-knot nematode (Meloidogyne incognita) in tomato. Journal of Hill Agriculture, 3(2): 37-41.

Mhatre, P. H., Karthik, C., Shanmugaiah, V., Sharma, M. P. and Panneerselvam, P. 2019. Plant growth promoting rhizobacteria (PGPR): Mechanisms, role in nematode management and future prospects. Chemical and Biological Technologies in Agriculture, 6(1): 26. https://doi.org/10.1186/s40538-019-0164-6.

Ministry of Agriculture and Land Reclamation. 2020. Agricultural Statistics of Egypt: Agricultural Economics Annual Report 781. Ministry of Agriculture and Land Reclamation.

Mitreva, M., Zarlenga, D. S., McCarter, J. P. and Jasmer, D. P. 2007. Parasitic nematodes: From genomes to control. Veterinary Parasitology, 148(1): 31-42. https://doi.org/
10.1016/j.vetpar.2007.05.013.

Molinari, S. 2011. Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Reports, 30: 311-323. https://doi.org/10.1007/s00299-010-0972-8.

Molinari, S. and Leonetti, P. 2019. Bio-control agents for the management of plant-parasitic nematodes. Crop Protection, 122: 34-40. https://doi.org/10.1016/j.cropro.2019.04.015.

Montanaro, G., Xiloyannis, C., Nuzzo, V. and Dichio, B. 2017. Orchard management, soil organic carbon and ecosystem services in Mediterranean fruit tree crops. Scientia Horticulturae, 217: 92-101. https://doi.org/
10.1016/j.scienta.2017.01.012.

Nguyen, N. P. and Grewal, P. S. 2006. Description of Mesodorylaimus anamensis n. sp. (Nematoda: Dorylaimidae) and its interactions with plant-parasitic nematodes. Nematology, 8(4): 493-501. https://doi.org/
10.1163/156854106778614092.

Omran, E. S. E., Mahmoud, M. F. and Abd El-Nabi, H. M. 2023. Eco-friendly nematodes: Bioindicators for promoting sustainable soil health. In: Nematode-Plant Interactions and Controlling Infection. IGI Global, pp. 187-213.

Paracer, S., Tarjan, A. C. and Hodgson, L. M. 1987. Effective use of marine algal products in the management of plant-parasitic nematodes. Journal of Nematology, 19(2): 194.

Paudel, R., Balkwill, L. and Wang, K. H. 2025. Allelopathic effects of sorghum/sorghum-sudangrass hybrids against Rotylenchulus reniformis. Plant Disease, 109: 1142-1147. https://doi.org/10.1094/PDIS-08-24-1668-RE.

Peng, D. and Moens, M. 2003. Suppression of the root-knot nematode Meloidogyne incognita by the fungus Pleurotus ostreatus. Biocontrol Science and Technology, 13(4): 425-434. https://doi.org
/10.1080/0958315031000104518.

Peng, Y. and Moens, M. 2003. Host resistance and tolerance to migratory plant-parasitic nematodes. Nematology, 5(2): 145-177. https://doi.org/10.1163/
156854103767139689.

Phani, Y., Naidu, K., Rao, S. and Raju, M. 2021. Integrated management of citrus nematode through soil solarisation and biofumigation. Journal of Pharmacognosy and Phytochemistry, 10(5): 2598-2602.

Poornima, K. 2020. Studies on incidence of root knot nematode and its bio management in pomegranate (Punica granatum L.). Pest Management in Horticultural Ecosystems, 26(2): 246-253.

Pradhan, M., Yadav, K. and Gupta, B. K. 2020. Diversity of plant-parasitic nematodes associated with pomegranate (Punica granatum L.) in Rajasthan, India. Indian Journal of Nematology, 50(2): 152-158.

Puissant, J., Villenave, C., Chauvin, C., Plassard, C., Blanchart, E. and Trap, J. 2021. Quantification of the global impact of agricultural practices on soil nematodes: A meta-analysis. Soil Biology and Biochemistry, 161: 108383. https://doi.org/
10.1016/j.soilbio.2021.108383.

Pun, T. B., Neupane, A., Koech, R. and Walsh, K. 2023. Detection and counting of root-knot nematodes using YOLO models with mosaic augmentation. Biosensors and Bioelectronics: X, 15: 100407. https://doi.org
/10.1016/j.biosx.2023.100407.

Reddy, P. P. 2011. Biofumigation and Solarisation for Management of Soil-Borne Plant Pathogens. Scientific Publishers.

Sepúlveda, M. E., Espinoza, C. and Vargas, M. 2010. Pomegranate (Punica granatum L.) consumption in Chile and its influence on human health. Revista Chilena de Nutrición, 37(2): 219-224.

Seth, L. 2003. The pomegranate: A fruit with a past and a future. Journal of the Royal Society of Medicine, 96(1): 3-4. https://doi.org
/10.1258/jrsm.96.1.3.

Sharma, S., Kumar, S., Yadav, A. and Sharma, S. K. 2020. Evaluation of nematicides and biocontrol agents against root-knot nematode (Meloidogyne incognita) on pomegranate. The Pharma Innovation Journal, 8(8): 555-560.

Shelke, S. S. and Darekar, S. V. 2001. Effect of Pratylenchus brachyurus on root and yield of pomegranate (Punica granatum L.). Indian Journal of Nematology, 31(2): 159-161.

Siddiqui, I. A. and Shaukat, S. S. 2003. Suppression of root-knot disease by Pseudomonas fluorescens strain CHA0 in tomato: Importance of bacterial secondary metabolites. Soil Biology and Biochemistry, 35(12): 1615-1623. https://doi.org/10.1016/
j.soilbio.2003.08.006.

Siddiqui, Z. A. and Mahmood, I. 1996. Biological control of plant-parasitic nematodes by fungi. In: CRC Press (Ed.), Biological Control of Plant-Parasitic Nematodes. pp. 1-24.

Sikora, R. A., Coyne, D. P. and Timmer, L. W. 2018. Nematology: Advances and Applications. Academic Press.

Sikora, R. A., Greco, N. and Silva, J. V. 2005. Nematode parasites of food legumes. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. CABI Publishing, pp. 259-318.

Silva, J. V., Coyne, D. L. and Sikora, R. A. 2018. Soil amendments for nematode management. Journal of Nematology, 50(3): 287-298.

Sivasubramaniam, N., Hariharan, G. and Zakeel, M. C. M. 2020. Sustainable management of plant-parasitic nematodes: An overview from conventional practices to modern techniques. In: Management of Phytonematodes: Recent Advances and Future Challenges. Springer, pp. 353-399.

Stover, E. W. and Mercure, R. L. 2007. The Pomegranate: New Perspectives for an Ancient Fruit. CRC Press.

Taha, F. 2018. Pomegranate farming in Egypt: A success story. Al-Ahram Weekly, 447: 18.

Taylor, C. E. and Georgis, R. 1979. Nematode resistance to chemicals. Journal of Nematology, 11(4): 315-320.

Tefu, G. M. 2020. Evaluation of Fruit-Based Amendments for the Management of Root-Knot Nematodes (Meloidogyne spp.) in Tomato (Doctoral dissertation). North-West University, South Africa.

Timper, P. 2014. Conserving and enhancing biological control of nematodes. Journal of Nematology, 46(2): 75-88.

Valero-Mendoza, R., Paredes-López, O. and Avila-Sosa, R. 2023. Applications of pomegranate (Punica granatum L.) byproducts in the food and beverage industries: A review. Trends in Food Science and Technology, 131: 109582. https://doi.
org/10.1016/j.tifs.2022.11.015.

Van der Putten, W. H., Cook, R., Costa, S., Davies, K. G., Fargette, M., Freitas, H. and van der Wurff, A. W. 2006. Nematode interactions in nature: Models for sustainable control of nematode pests of crop plants? Advances in Agronomy, 89: 227-260. https://doi.org/10.1016/S0065-2113(05)89005-3.

Veronico, P. and Melillo, M. T. 2021. Algal bioactive compounds for plant-parasitic nematode control. Journal of Nematology, 53: e2021-45. https://doi.org/10.21307/jofnem-2021-045.