Xylella fastidiosa is a Gram-negative bacterium characterized by its stringent growth requirements. It can infect a wide range of plant species up to 700 (European Food Safety Authority (EFSA) et al., 2023) either causing disease or persisting asymptomatically. The bacterium is non-motile and non-flagellated, with rod-shaped, strictly aerobic cells that have rounded or tapered ends and exhibit numerous irregular ridges or folds on the cell wall surface. Its optimal growth temperature ranges between 26–28°C (Wells et al., 1987). X. fastidiosa colonizes the xylem vessels of roots, stems, and leaves, obstructing the transport of water and mineral nutrients by forming bacterial aggregates known as biofilms. These biofilms develop in two main environments: within the host plant and in the foregut of the insect vector (Chatterjee et al., 2008). This dual habitat ensures that the pathogen is consistently protected within hosts, making it largely inaccessible to antimicrobial treatments.

Moreover, X. fastidiosa is capable of both upstream and downstream movement via twitching motility, which is mediated by type IV pili (Meng et al., 2005). Twitching motility refers to surface translocation across moist environments that does not rely on flagella. Specifically, pili of types I and IV are involved in twitching, biofilm formation, and cell-to-cell adhesion (Li et al., 2007).

Currently, the scientific community recognizes three main subspecies of X. fastidiosa, fastidiosa, multiplex, and pauca as the primary taxonomic divisions (Marcelletti and Scortichini, 2016). Additional subspecies, such as sandyii, morus, and tashke, have been proposed, and the taxonomy remains dynamic due to the continuous accumulation of genomic data and differentiation through multilocus sequence typing (MLST) (Maiden et al., 1998; Burbank and Ortega, 2018).

A particularly destructive subspecies, pauca, has evolved in Italy over the past decade generating an unprecedented plant health crisis, severely affecting olive trees. However, in United States, the fastidiosa subspecies has posed significant challenges to grapevines over the past 140 years. The timeline of X. fastidiosa’s detection and global spread underscores the pathogen’s complex biology and highlights the obstacles faced in diagnosis and disease management. It took 70 years to confirm that the pathogen is insect-transmitted (Winkler, 1949), nearly a century to determine that it is a bacterium rather than a virus (Goheen et al., 1973), and over 130 years to recognize its ability to spread via asymptomatic, infected plant material (Saponari et al., 2013). A recent economic analysis by the European Union estimated that, under a full-spread scenario, X. fastidiosa could cause annual damage of approximately €5.5 billion across Europe (European Commission, 2023). As Europe transitions toward more sustainable agriculture, the use of chemical agents previously employed to manage bacterial diseases is being restricted or banned (Boix-Fayos and de Vente, 2023). A recent comprehensive review (Wang et al., 2024) identified diseases caused by X. fastidiosa as among the most significant threats to plant health in the 21^st century.

Although the global outbreak of this pathogen has spurred considerable research into its biology and control, major knowledge gaps persist. The quest for an effective remedy remains a collective challenge that involves not only researchers and agricultural experts but also farmers and the general public. The urgency of the outbreaks and the associated economic burden underscore the need for a viable solution that will naturally garner widespread support among stakeholders.

In this review, we first assess the global economic impact of X. fastidiosa. We then compile key findings from recent studies on biocontrol and management practices, strategies to limit pathogen spread, and the implementation of phytosanitary measures. Finally, we highlight critical challenges that must be addressed in the future to achieve effective and sustainable disease control.

The insect-transmitted bacterium X. fastidiosa has a broad host range and poses significant economic and social threats to the agricultural and horticultural sectors. Major outbreaks have been recorded in Italy, Spain, France, and Portugal regions previously unaffected by this pathogen, which was historically restricted to the Americas.

The outbreak in Apulia, Italy, since 2013 has devastated more than 100 kilometers of olive-growing territory, affecting approximately 54,000 hectares and around 5 million olive trees, resulting in a 10% reduction in national olive oil production (White et al., 2020; Frem et al., 2021b). Estimated economic losses over the next 50 years range from €1.5 to €5.9 billion, accounting for reduced production as well as damage to landscapes and cultural heritage (D’Attoma et al., 2019; Schneider et al., 2020). Between 2016 and 2018 alone, production losses amounted to €390 million, while socio-ecological damages were estimated at €1,059 per hectare (Olivicola and Nazionale, 2019; Frem et al., 2021b).

In California, losses include $104 million annually due to yield reductions, management efforts, and regulatory measures (Tumber et al., 2014). The Pierce’s Disease Control Program, established to mitigate X. fastidiosa-related impacts, invested approximately $544 million between 1999 and 2010, mostly funded by federal sources (Hopkins and Purcell, 2002). Farmers in California bear $51.1 million annually in plant losses, with potential total costs reaching $185 million per year (Hopkins and Purcell, 2002; Tumber et al., 2014).

In Brazil, X. fastidiosa has caused Citrus Variegated Chlorosis (CVC), resulting in 120 million citrus plant infections in the 2000s and associated losses of approximately $110 million (Bové and Ayres, 2007; Gonçalves et al., 2011).

Across the European and Mediterranean regions, significant yield reductions have been observed: 78% in olives, 16.1% in citrus, 5.3% in grapes, and 0.6% in almonds. This translates into an estimated $12.44 billion in lost agricultural production (Cardone et al., 2022). The European Commission’s Joint Research Centre projects EU-wide costs could reach €5.5 billion annually, including €700 million in export losses.

In Lebanon, if infected grapevines are not replaced, revenue losses are projected to range from $11 million over four years to $82.44 million over 30 years (Frem et al., 2021a). In the Balearic Islands, almond orchard area declined from 29,789 ha in 2010 to 11,814 ha in 2019, primarily due to fastidiosa infection (Olmo et al., 2021). Additionally, X. fastidiosa subsp. pauca ST80 poses a significant threat to olive production, with symptoms resembling those caused by the aggressive Italian ST53 strain (Giampetruzzi et al., 2017). The California control program has demonstrated the importance of intergovernmental collaboration (e.g., USDA and state authorities) in mitigating economic losses (Tumber et al., 2014). In Europe, effective disease management is crucial, as subspecies multiplex, pauca, and fastidiosa continue to show expansion potential, driven more by human trade and vector dynamics than by climatic factors (Godefroid et al., 2019; Schneider et al., 2021). X. fastidiosa not only transforms landscapes but also endangers centuries-old agricultural traditions, particularly in olive-growing regions of Italy. Resistance to eradication and control measures has emerged, complicating disease management efforts (Martelli et al., 2016; White et al., 2020). Proactive prevention and sustained research are essential to curb the pathogen’s spread and mitigate its impact. Global projections for wine industry losses due to X. fastidiosa range from $2.3 to $7.9 billion over the next 50 years (Hafi et al., 2017). Indirect costs including job losses, reduced tourism, and trade restrictions further compound the pathogen’s socioeconomic impact (Schneider et al., 2021). Thus, X. fastidiosa exemplifies the urgent need for coordinated, cross-regional strategies to effectively confront one of the most pressing plant health crises of our time.

Xylella fastidiosa is a fast-spreading bacterial pathogen that poses a serious threat to global agriculture, with no effective cure currently available. Ongoing efforts to manage this phytopathogen include the application of control measures on infected plants, government-regulated interventions, and the use of advanced molecular diagnostic tools.

These strategies include the adoption of resistant or tolerant plant cultivars, the implementation of stringent quarantine and eradication measures to remove infected plants, and the control of insect vectors -such as sharpshooters- through chemical or biological methods. Cultural practices, including pruning and sanitation, contribute to reducing bacterial reservoirs. In parallel, ongoing research is investigating the potential of beneficial microbes and natural antagonists as effective biological control agents. Collectively, these integrated approaches aim to achieve sustainable management of X. fastidiosa outbreaks and to protect vulnerable crops and ecosystems.

Indeed, these approaches can be broadly categorized into four main approaches: management of infected plants, deployment of resistant cultivars, application of antimicrobial substances to inhibit bacterial growth, and control of insect vectors. Importantly, numerous research studies have investigated diverse control strategies, including the use of natural compounds and microbial antagonists ( Table 1 ).

The absence of curative treatments for plants infected by Xylella fastidiosa makes vector management the primary strategy for mitigating the spread of the pathogen in affected areas. One promising strategy to limit the spread of X. fastidiosa involves targeting its insect vectors, particularly Philaenus spumarius, which is responsible for transmitting the pathogen to a wide range of host plants. Due to the unique characteristics of its transmission persistent, non-circulative, and lacking a latency period X. fastidiosa is difficult to disrupt once acquired by its insect vectors. Therefore, vector control efforts aim to reduce transmission by lowering or eliminating vector populations, particularly those that visit susceptible host plants.

Biological control agents (BCAs), especially those based on predatory insects and entomopathogenic organisms, have emerged as effective tools for vector management. Studies have demonstrated that the predatory insect Zelus renardii can significantly reduce P. spumarius populations and, consequently, lower the incidence of X. fastidiosa infections in olive trees, supporting the use of natural predators as biocontrol agents (Liccardo et al., 2020). The biocontrol model proposed by Liccardo et al. (2020) is based on both laboratory and field trials, highlighting the effectiveness of a dual approach that combines predation and inundation techniques to mitigate the threat posed by X. fastidiosa. However, the introduction of predatory insects also raises ecological concerns, including the risk of unintended environmental consequences such as uncontrolled proliferation of the biocontrol agent or disruption of existing ecological balances within olive groves.

In a similar vein, another study emphasized the value of integrating chemical and physical control methods with biological interventions to manage vector populations more effectively (Picciotti et al., 2021).

Beyond predatory insects, entomopathogenic nematodes (EPNs) and fungi have also gained prominence as potential BCAs targeting the X. fastidiosa vector. El-Khoury et al., 2024 evaluated the pathogenicity of different EPN and fungal strains, demonstrating the efficacy of species such as Beauveria bassiana and Lecanicillium muscarium against P. spumarius (El-Khoury et al., 2024).

Numerous measures to reduce nymphal populations have been tested through experimental trials in Italy and Spain. Dongiovanni et al., 2018 conducted a three-year study comparing the efficacy of different foliar sprays targeting weed and ground vegetation management as a means to reduce juvenile populations of Philaenus spumarius and Neophilaenus campestris (Dongiovanni et al., 2018b). The authors also demonstrated that the application of orange oil significantly reduced nymphal populations, suggesting its effectiveness in managing early vector stages (Dongiovanni et al., 2018b). However, its efficacy appears limited to nymphs inhabiting herbaceous ground cover and may be less practical in environments where undergrowth control is difficult or once vectors reach adulthood.

In Portugal, vector control strategies include the use of plant protection products that comply with safety standards for human health and the environment. Recently, certain plant protection products have been granted exceptional authorization for use in vector management. Dongiovanni et al., 2018 reported that acetamiprid a neonicotinoid insecticide exhibited substantial toxicity against P. spumarius. Nevertheless, the overuse of contact insecticides can accelerate resistance development in pest populations and negatively impact beneficial arthropods (Dongiovanni et al., 2018a).

In another study, Dongiovanni et al. (2017) showed that citrus oil was effective against nymphs when applied at high volumes (2,000 L/ha), although its efficacy was confined to immature stages. Despite its toxicity, some publications argue that acetamiprid does not significantly interfere with bacterial inoculation, as vectors exposed to this insecticide showed lower susceptibility compared to those treated with other insecticides (Lago et al., 2022). Similarly, Bethke et al., 2001 documented the effectiveness of a neonicotinoid in reducing vector populations in California (Bethke et al., 2001).

Behavioural studies by (di Domenico et al., 2019) found that male and female P. spumarius responded differently to varying doses of citrus oil, demonstrating either at-traction or repulsion. Additionally, Lago et al., 2022 evaluated the protective effects of kaolin, a clay-based particle film, which acts as a mechanical barrier against insect vectors such as Homalodisca vitripennis, a known X. fastidiosa vector. Kaolin was shown to deter insect feeding and oviposition, ultimately leading to vector mortality (Lago et al., 2022).

More recently, interest in natural enemies of spittlebugs has grown in Europe. For instance, Reis et al. (Reis et al., 2018) reported the identification of egg parasitoids in Portugal, while Mesmin et al. (Mesmin et al., 2020) documented the presence of the egg parasitoid Ooctonus vulgatus Haliday in Corsica.

Additionally, natural predation by birds and small reptiles targets both nymph and adult stages of Cicadellinae, while larvae of coccinellids and lacewings have been observed feeding on egg masses. These interactions support the development of sustainable integrated pest management (IPM) programs. Effective IPM will require precise timing of interventions, careful evaluation of novel formulations, and the optimization of treatment volumes and methods (Liccardo et al., 2020).

In France, Grandgirard et al., 2008 tested the release of natural enemies such as Gonatocerus spp., egg parasitoids of sharpshooter vectors. Their study reported a 95% reduction in vector populations within seven months of release (Grandgirard et al., 2008, 2009). In a complementary approach, other research explored the isolation of insect-specific viruses capable of reducing bacterial adhesion to vectors, indicating their potential as biopesticides (Stenger et al., 2009).

On the whole, these findings underscore a key challenge in biological control: ensuring the specificity and effectiveness of BCAs in targeting the appropriate insect vectors. In this context, microbial pathogens represent an environmentally friendly alternative to chemical insecticides and help reduce the ecological footprint of agricultural practices. The successful development and implementation of BCAs also require a deep understanding of X. fastidiosa ecology and genetics, particularly the genomic diversity among its subspecies. Research by Vanhove et al. (2019) revealed strain-specific traits that influence host range and vector interactions, emphasizing the importance of genomic analysis in optimizing biocontrol strategies.

These potential differences in strain susceptibility have significant implications for biocontrol program design, as variations in response to entomopathogenic agents could influence overall effectiveness. Additionally, X. fastidiosa possesses a remarkable capacity for horizontal gene transfer (HGT), further complicating its evolutionary trajectory. The acquisition of genetic material through conjugation may enhance virulence and promote adaptation to control strategies, thereby highlighting the need for continuous monitoring and adaptive management systems (Burbank and Van Horn, 2017). Understanding these evolutionary and ecological mechanisms enables researchers to select appropriate BCAs and incorporate them into comprehensive, integrated disease management frameworks. In this regard, Kyrkou et al. (2018) provide an overview of various control strategies, emphasizing the incorporation of BCAs into integrated pest management (IPM) systems that aim to balance crop protection with ecological sustainability and economic viability.

This review summarizes the principal strategies and ongoing challenges associated with the control of X. fastidiosa, a highly destructive and globally significant plant pathogen. For more than a century, the diseases caused by X. fastidiosa including Pierce’s disease in grapevines, Citrus Variegated Chlorosis (CVC), and more recently Olive Quick Decline Syndrome (OQDS) have threatened major agricultural systems. Despite decades of research, no curative solution has yet been found, and effective, long-lasting management strategies remain limited across the wide range of host species and diverse environmental contexts in which the bacterium thrives. Innovative and interdisciplinary approaches are urgently required to overcome the complex biology of X. fastidiosa, including its broad host range, efficient insect vector transmission, and ability to persist asymptomatically in reservoirs. A key component of progress will involve expanding research efforts beyond the best-studied pathosystems (e.g., grapevine, citrus, olive) to include under-researched hosts, such as almond, blueberry, coffee, and numerous ornamental or wild species that may act as silent reservoirs. The formulation of integrated disease management strategies must incorporate short-term, rapid-response measures such as vector suppression and phytosanitary containment with longer-term goals like breeding for resistance, endotherapy using microbial antagonists or bioactive compounds, and the development of environmentally sustainable biological control tools. These efforts should be supported by advanced technologies, including genomics, metagenomics, metabolomics, and precision agriculture platforms. Achieving tangible progress in the management of X. fastidiosa also requires robust collaboration among multidisciplinary research teams, policymakers, agricultural stakeholders, and growers. Effective knowledge transfer, shared surveillance data, and harmonized phytosanitary regulations across regions are vital for mitigating the spread and impact of this pathogen. Stakeholder engagement, particularly with farmers and local communities, is crucial to ensure the acceptance and practical implementation of control strategies. In conclusion, addressing the global threat posed by X. fastidiosa demands both scientific innovation and coordinated action. Through sustained collaboration and investment in research, it is possible to develop holistic, adaptive, and resilient solutions to safeguard plant health, agricultural productivity, and biodiversity in the face of this evolving pathogen.