Introduction
The United Nations Department of Economic and Social Affairs, Population Division, projected in 2017 that the world’s population, currently 7.6 billion, will rise to 8.6 billion in 2030, 9.8 billion in 2050 and 11.2 billion in 2100 (UN Department of Economic and Social Affairs, 2021). A meta-analysis revealed that global food demand will increase by 35–56% from 2010 to 2050, while the number of people at risk of hunger could fluctuate between −91% and +8% (van Dijk et al., Reference Van Dijk, Morley, Rau and Saghai2021). Substantial yield reductions due to crop pests and diseases are evident, with average losses of approximately 40% in wheat, rice, maize, potato, and soybean, significantly contributing to food insecurity (Savary et al., Reference Savary, Willocquet, Pethybridge, Esker, McRoberts and Nelson2019).Yield losses of up to 100% are possible without effective control measures, leading to widespread destruction. Globally, plant diseases caused by viruses, nematodes, bacteria, and fungi result in annual losses of approximately $220 billion (Savary et al., Reference Savary, Willocquet, Pethybridge, Esker, McRoberts and Nelson2019). In addition, Germany lost €25 million, and Italy lost approximately €100 million due to a phytoplasma epidemic in apple trees in 2001 (Strauss, Reference Strauss2009).
Phytoplasmas are wall-less bacteria belonging to the class Mollicutes that reside in the phloem sieve elements of diseased plants (Lee et al., Reference Lee, Gundersen-Rindal, Davis and Bartoszyk1998). Taxonomy and identification of phytoplasmas rely on molecular methods and gene sequences, as these pathogens cannot be cultured in cell-free conditions. Currently, 48 ‘Candidatus Phytoplasma’ species have been named based on several criteria, including <98.65% sequence identity in the 16S rRNA gene, <95–96% whole genome similarity, or ecological separation (Bertaccini et al., Reference Bertaccini, Arocha-Rosete, Contaldo, Duduk, Fiore, Montano and Zamorano2022; Wei and Zhao, Reference Wei and Zhao2022). Wei and Zhao (Reference Wei and Zhao2022) classified genetically diverse phytoplasmas into 37 groups and over 150 subgroups using restriction fragment length polymorphism (RFLP) profiles of the F2nR2 region of the 16S rRNA gene. Many phytoplasmas have been linked to newly emerging diseases worldwide in recent years (Huang et al., Reference Huang, Wang, Zhang, Li, Li, Shan and Wang2023).
Phytoplasmas-associated diseases affect over 1000 plant species worldwide (Hiruki and Wang, Reference Hiruki and Wang2004; Maejima et al., Reference Maejima, Oshima and Namba2014; Wang et al., Reference Wang, Bai, Li, Wang, Huang, Wu and Zhao2024). As a threat to food security, their infestation may cause substantial yield losses of up to 100% in cucumber, tomato, pepper, potato and Navratil crops (Bogoutdinov et al., Reference Bogoutdinov, Valyunas, Navalinskene and Samuitene2008; Rao and Kumar, Reference Rao and Kumar2017). Over the last four decades, millions of coconut palm trees in the Caribbean have been wiped out by a deadly lethal yellowing disease (LYD) associated with phytoplasmas (Brown et al., Reference Brown, Been and McLaughlin2006). In Jamaica alone, more than seven million palm trees died by 1980 due to LYD (Roca de Doyle, Reference Roca De Doyle2001). In Africa, similar diseases were observed and collectively referred to as lethal yellowing-like disease (Eden-Green, Reference Eden-Green1997). Eight million coconut palms, or 38 % of Tanzania’s total hectarage, have been destroyed due to phytoplasma-associated-lethal disease since the 1960s (Mugini, Reference Mugini, Eden-Green and Ofori2002). Furthermore, an outbreak of LYD in Côte d’Ivoire damaged 350 hectares of coconut and destroyed 12,000 metric tonnes of copra annually, with an additional 7,000 hectares at risk (Arocha-Rosete et al., Reference Arocha-Rosete, Konan Konan, Diallo, Allou and Scott2014).
The incidence of phytoplasmas-associated plant diseases has been on the rise (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). Experts predict that this trend will continue in the future due to climate change in the geographic distribution of phytoplasmas and the increased international trade of host plants for planting (Al Ruheili et al., Reference Al Ruheili, Boluwade and Al Subhi2021; Aidoo et al., Reference Aidoo, Cunze, Guimapi, Arhin, Ablormeti, Tettey and Yankey2021; EFSA Panel on Plant Health (PLH), Reference Bragard, Dehnen-Schmutz, Gonthier, Jaques Miret, Justesen and Jacques2020). Moreover, efficient management of phytoplasmas can improve and sustainably increase agricultural yields (Bertaccini, Reference Bertaccini2021), thereby contributing to global food security. This review sheds light on phytoplasmas as plant pathogens, the threats they pose, factors contributing to their spread, global collaborative research efforts, management strategies and surveillance and detection. We present case studies that highlight management practices, lessons learned, and future research directions for phytoplasma-mediated diseases.
Understanding phytoplasma plant pathogens
Phytoplasmas, previously identified as mycoplasma-like organisms (MLOs) are one of the smallest known pathogens infecting several plant species worldwide. They are prokaryotic plant pathogenic bacteria, with size ranging from 200 to 1000 nm (McCoy et al., Reference McCoy, Caudwell, Chang, Chen, Chiykowski, Whitcomb and Tulley1989). The phytoplasma’s cell lacks a wall and their outer covering is made up of a triple layered single unit membrane (Lee and Davis, Reference Lee, Davis, Maniloff, McElhaney, Finch and Baseman1992). They have genomic sizes ranging from 0.53 to 1.2 kb (Bai et al., Reference Bai, Zhang, Ewing, Miller, Jancso Radek, Shevchenko, Tsukerman, Walunas, Lapidus, Campbell and Hogenhout2006; Oshima et al., 2004), with a low G+C content (Kollar and Seemuller, Reference Kollar and Seemuller1989), being descended from an ancestral Gram-positive bacteria in the Bacillus – Clostridium group (Zhao et al., Reference Zhao, Wei, Lee, Shao, Suo and Davis2009). They live and multiply in the functional phloem sieve tube elements of their hosts, producing disease symptoms such as virescence, phyllody and witches’ broom (Bertaccini et al., Reference Bertaccini, Arocha-Rosete, Contaldo, Duduk, Fiore, Montano and Zamorano2022; Lee et al., Reference Lee, Davis and Gundersen-Rindal2000). Until their first isolation in pure culture, they were previously thought to be obligate parasites. Moreover, there is a gradual improvement in the methods for applicability to a wider range of ‘Ca. Phytoplasma’ species (Contaldo et al., Reference Contaldo, Bertaccini, Paltrinieri, Windsor and Windsor2012; Contaldo et al., Reference Contaldo, Satta, Zambon, Paltrinieri and Bertaccini2016).
The inability to obtain axenic culture of phytoplasmas in the past made their identification using cultural, morphological and biochemical methods challenging (Makarova et al., Reference Makarova, Contaldo, Paltrinieri, Kawube, Bertaccini and Nicolaisen2012). Consequently, their identification has relied primarily on molecular methods (Bertaccini and Duduk, Reference Bertaccini and Duduk2009) particularly using the 16S ribosomal RNA (16S rRNA) gene. This approach has been used to create two parallel classification systems. In one system all strains of the pathogen are placed in the provisional genus ‘Ca. Phytoplasma’ and are separated into species based on variations in the nucleotide sequences of the 16S rRNA gene (IRPCM, 2004; Harrison et al., Reference Harrison, Gundersen-Rindal, Davis, Krieg, Staley, Brown, Hedlund, Paster, Ward, Ludwig and Whitman2011). In the second system, phytoplasmas are classified into groups and subgroups based on RFLP patterns obtained from PCR-amplified products of unknown isolates (Zhao et al., Reference Zhao, Wei, Lee, Shao, Suo and Davis2009; Lee and Davis, Reference Lee, Davis, Maniloff, McElhaney, Finch and Baseman1992). Other investigators prefer to first sequence the PCR-amplified 16S rRNA-encoding gene products of the phytoplasma, after which the assembled nucleotides are used in a BLAST search to identify the species and phylogenetic analysis used to assign them to groups and sub-groups. In some instances, the gene sequences can be digested in silico and computer programs such as the iPhyclassifier can be used to delineate the 16Sr group and subgroups of the unknown isolates (Zhao et al., Reference Zhao, Wei, Lee, Shao, Suo and Davis2009; Wei et al., Reference Wei, Davis, Jomantiene and Zhao2008). Multilocus analysis involving the 16S ribosomal gene, the 16S–23S intergenic spacer region and secA and groEL genes have been used to identify the species status of some phytoplasma isolated from palms in Florida (Soto et al., Reference Soto, Helmick, Harrison and Bahder2021).
Phytoplasmas can infect a wide range of plant species (Seemüller et al., Reference Seemüller, Garnier, Schneider, Razin and Herrmann2002; Lee et al., Reference Lee, Davis and Gundersen-Rindal2000; Olivier et al., Reference Olivier, Lowery and Stobbs2009). According to Hemmati et al. (Reference Hemmati, Nikooei and Al-Sadi2021a), more than 164 plant species made up of fruit crops, vegetables, cereal and oilseed crops, trees, ornamental plants and weeds in the Middle East region have been associated with fourteen 16Sr phytoplasma strains. In Mexico, phytoplasmas have been associated with diseases of different species of palm causing wilting of fronds and eventual death of plants (Hernandez et al., Reference Hernandez, Gordillo, Oropeza Saın, Ortiz Garcıa, Magana Alejandro, Sanchez Soto and Garcıa Estrada2020).
Transmission of phytoplasmas occurs via vegetative propagation, dodder (Cuscuta spp.), and insect vectors (Aryan et al., Reference Aryan, Musetti, Riedle-Bauer and Brader2016; Kaminska and Korbin, Reference Kaminska and Korbin1999). There have been studies on possible transmission of phytoplasma through alfafa seeds and the embryo of coconut fruits obtained from infected palms (Kahn et al., Reference Khan, Botti, Paltrinieri, Al-Subhi and Bertaccini2002; Cordova et al., Reference Cordova, Jones, Harrison and Oropeza2003). Though some studies could not confirm seed transmission of phytoplasmas (Nipah et al., Reference Nipah, Jones and Dickinson2007; Cordova et al., Reference Cordova, Jones, Harrison and Oropeza2003), recent studies have confirmed seed transmission of phytoplasmas in coconut (Narvaez et al., Reference Narváez, Nic-Matos and Oropeza2022). Worldwide, leafhoppers, planthoppers and psyllids are known to transmit phytoplasmas (Weintraub and Beanland, Reference Weintraub and Beanland2006). These insects feed on plant phloem, ingest the pathogen, which then colonizes their guts and salivary glands, multiplies, and is subsequently released into new hosts during feeding (Ammar and Hogenhout, Reference Ammar, Hogenhout, Kostas and Miller2006). Demonstrating insect transmission of phytoplasmas has been challenging due to the difficulty of producing pure cultures. However, recent methodological advances have enabled transmission studies linking specific insect species to pathogen spread. For example, Austroagallia sinuata collected from infected fields transmitted ‘Ca. Phytoplasma aurantifolia’ to Aerva javanica in periwinkle cages (Hemmati et al., Reference Hemmati, Nikooei and Bertaccini2019). Similarly, the pathogen responsible for lethal bronzing disease (LB) of palm was successfully transmitted from infected spear leaves to a sucrose medium by Haplaxius crudus (Mou et al., Reference Mou, Di-Lella, Herbert, Bextine, Helnick and Bahder2022), and H. crudus has recently been experimentally confirmed to transmit LYD (Narvaez et al., Reference Narváez, Nic-Matos and Oropeza2022). As axenic culture methods for phytoplasmas continue to improve, more studies on insect transmissibility are expected in the future.
Threats posed by emerging phytoplasma pathogens
Evidence first appeared in 1967 linking prokaryotes that morphologically resembled mycoplasmas colonising phloem tissue (then termed mycoplasma-like organisms, MLOs) to yellowing-type plant diseases previously assumed to be caused by viruses (Doi et al., Reference Doi, Teranaka, Yora and Asuyama1967). Today, phytoplasmas are recognised as major plant pathogens associated with diseases that have serious environmental and economic consequences. A wide range of plant species, including ornamentals, timber trees, shade trees, and economically important food, vegetable, and fruit crops, are affected by phytoplasma-associated diseases (Bertaccini et al. Reference Bertaccini, Duduk, Paltrinieri and Contaldo2014; Gasparich, Reference Gasparich2010). Varying degrees of phytoplasma incidence on vegetables have been documented in 47 nations, spanning five continents (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). Phytoplasmas have been linked to 164 plant hosts, including feed crops, cereals, fruit crops, medicinal plants and shade trees. Fourteen of the 34 identified phytoplasma ribosomal groups have been reported across the Middle East and other regions worldwide (Hemmati et al., Reference Hemmati, Nikooei, Al-Subhi and Al-Sadi2021b). While specific phytoplasmas may have limited host ranges, phytoplasma-related disorders impact a diverse range of crops worldwide. Examples include pigeon pea witches’ broom (16SrIX) in Brazil (Chen et al., Reference Chen, Pu, Deng, Liu, Li and Civerolo2008) and the citrus huanglongbing disease in China, which is linked to the aster yellows phytoplasmas (16SrI) (Teixeira et al., Reference Teixeira, Wulff, Martins, Kitajima, Bassanezi, Ayres, Eveillard, Saillard and Bové2009). Over 300 different plant diseases that have been connected to phytoplasmas have impacted hundreds of plant taxa (Bertaccini and Duduk, Reference Bertaccini and Duduk2009). Woody plant diseases such as coconut lethal yellowing, peach X-disease, grapevine yellows (GY) and apple proliferation, are particularly important due to their commercial significance. Notable phytoplasma diseases that have been recorded in Southeast Asia include rice yellow dwarf, peanut witches’ broom, Bermuda grass white leaf and sugarcane white leaf and grassy shoot (Win and Jung, 2012). The phytoplasma group 16SrIX, which affects almond crops, is particularly problematic in the Middle East. Since the 1990s, almond production in Lebanon and Iran has been severely impacted by a fatal disease associated with this group. Thousands of almond trees have been lost in Lebanon since the initial outbreak in the south of the country 15 years ago (Abou-Jawdah et al., Reference Abou-Jawdah, Dakhil, El-Mehtar and Lee2003). Diseases linked to phytoplasma have long been known to cause significant financial harm to a range of domestic and wild plants. The threat posed by phytoplasma diseases is growing on a global scale due to two main causes: severe epidemics in the rest of the world that affect grapevines, citrus, forest trees, oil-seed crops, alfalfa, stone and pome fruits; and emerging diseases in Latin America, Asia, Africa and the Caribbean that primarily affect sugarcane, corn, cassava, coconuts, papaya and vegetables. In both scenarios, these diseases have the potential to expand to new crop species and significantly affect international trade. Although phytoplasmas are highly metabolically dependent on their host plant, they generally do not cause rapid death. However, in exceptionally cold climates, infected plants die, while in tropical climates, asymptomatic plant presence is common and can have serious epidemiological repercussions (Bertaccini, Reference Bertaccini2008).
Similar to the identification of phytoplasma strains on the American continent, which comprised strains from 12 subgroups within 10 ribosomal groups, strains from ten (10) ribosomal groups and 16 subgroups on the Asian continent have been documented. The phytoplasma group 16SrIII affects 10 types of vegetable crops, whereas the group 16SrI affects 14. Apart from the few incidences of the pathogen on tomatoes in Mexico, the 16SrIII phytoplasma group seems to be limited to countries such as Bolivia, Brazil, Argentina, Chile and Costa Rica. The 16SrI phytoplasmas group of the aster yellows category is the most common in various genera, followed by ‘Ca. Phytoplasma solani’ (Stolbur phytoplasma) (16SrXIIA), clover proliferation (16SrVI) and the 16SrII group of peanut witches’ broom (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). Analyses of NCBI database records show that phytoplasma groups 16SrI, 16SrII, 16SrIV, 16SrV, 16SrVI, 16SrIX, 16SrXI, 16SrXII, and 16SrXIV are prevalent in India (Ayman et al., Reference Ayman, Kumar, Hallan and Zaidi2010; Priya et al., Reference Priya, Chaturvedi, Rao and Raj2010). In both Iran and India, 16SrI and 16SrII phytoplasmas significantly reduce squash yields (Salehi et al., Reference Salehi, Siampour, Alireza, Hosseini and Bertaccini2015; Rao et al., Reference Rao, Gopala and Rao2017b).
Phytoplasmas also represent a major limiting factor for several economically important crops in Europe and North America. For instance, in North America and Europe, the aster yellow phytoplasma significantly reduces the value of ornamental plants such as gladiolus, hydrangea, purple coneflower and China aster, as well as vegetable crops such as lettuce, carrots and celery (Bertaccini and Duduk, Reference Bertaccini and Duduk2009). Apple proliferation, European stone fruit yellows and pear decline are fruit tree phytoplasma diseases that are economically significant in Europe (Marcone et al., Reference Marcone, Valiunas, Salehi, Mondal and Sundararaj2023). Interestingly, in some cases, phytoplasmas infection in ornamental plants may provide desirable and valuable traits, such as the free-branching phenotypes in most commercial poinsettia varieties resulting from infection by phytoplasmas (Lee et al., Reference Lee, Chu and Chu2021).
Apple proliferation is widespread across Europe, where affected Malus domestica Borkh. trees produce undersized, unmarketable apples. Fruit quality is diminished, size is reduced by approximately 50%, and weight losses range from 63% to 74%. Additionally, reduced tree vigour increases susceptibility to powdery mildew. Three subgroups (16SrII-A, -C and -D) are widely distributed over the African continent and infect faba beans, squash, tomatoes, brinjal and chiles (Omar and Foissac, Reference Omar and Foissac2012; Alfaro-Fernández et al., Reference Alfaro-Fernández, Cebrián, Villaescusa and Font-San–Ambrosio2011, Reference Alfaro-Fernández, Ali, Abdelraheem, Saeed and FontSan-Ambrosio2012). In Australia, only three (16SrII, 16SrV and 16SrXII) out of the seven phytoplasma groups (16SrI, 16SrII, 16SrIII, 16SrV, 16SrX, 16SrXI and 16SrXII) have been recorded, and these are known to infect vegetable crops. Nevertheless, there are few reports of phytoplasma disease affecting vegetable crops in Australia. The global analysis of phytoplasma and their threat to food security around the globe is presented in Table 1.
The global analysis of phytoplasma and their threat to food security
Factors contributing to spread of phytoplasma
Biotic and abiotic factors contribute immensely to phytoplasma transmission. The biotic factors transmit phytoplasma in persistent-propagative mechanism through multiplication within the vector after acquisition (Christensen et al., Reference Christensen, Axelsen, Nicolaisen and Schulz2005; Weintraub and Beanland, Reference Weintraub and Beanland2006; Jarausch and Weintraub, 2013; Mou et al., Reference Mou, Di-Lella, Herbert, Bextine, Helnick and Bahder2022). The transmission of phytoplasmas by insect vectors begins with the acquisition of the pathogen from an infected plant via feeding. The pathogen spreads from the vector’s gut to its salivary glands and reproduces within the vector. After reproduction, the vector transfers the pathogen to another plant via feeding thereby infecting the plant. Insects, specifically the phloem-feeding insects such as leafhoppers, planthoppers and psyllids are major vectors of phytoplasma spread (Weintraub and Beanland, Reference Weintraub and Beanland2006). For example, the planthopper Haplaxius crudus is a confirmed vector of ‘Ca. Phytoplasma aculeata’, a phytoplasma responsible for lethal bronzing of palms in Mexico and Florida (Halbert et al., Reference Halbert, Wilson, Bextine and Youngblood2014; Narváez et al., Reference Narváez, Vázquez-Euán, Harrison, Nic-Matos, Julia, Dzido, Fabre, Dollet and Oropeza2018; Mou et al., Reference Mou, Humphries, Soto, Helmick, Ascunce, Goss and Bahder2020a; Dzido et al., Reference Dzido, Sánchez, Dollet, Julia, Narvaez, Fabre and Oropeza2020). Recent studies have also demonstrated transovarial transmission, where offspring of infected vectors carry the pathogen. For instance, the progeny of Matsumuratettix hiroglyphicus were found to harbour the sugarcane white leaf phytoplasma and could transmit it to healthy plants (Hanboonsong et al., Reference Hanboonsong, Choosai, Panyim and Damak2002; Weintraub and Beanland, Reference Weintraub and Beanland2006). In addition, phytoplasma can spread through agricultural and horticultural planting materials such as rootstocks, cuttings and grafting materials, especially in woody plants. Plant shoots and roots, such as basal shoots, stems, rhizomes, tubers, stolons, corms, buds and bulbs, can all vegetatively spread phytoplasma (Caglayan et al., Reference Caglayan, Gazel, Škorić, Bertaccini, Weintraub, Rao and Mori2019; Reference Çağlayan2023). Seed transmission has been reported in both herbaceous and woody plant species (Satta et al., Reference Satta, Paltrinieri, Bertaccini, Bertaccini, Weintraub, Rao and Mori2019). The seeds from phytoplasma-infected alfalfa (Medicago sativa), lime (Citrus aurantiaca) and tomato (Lycopersicum esculentum) from Oman and Italy were found to contain phytoplasmas belonging to ribosomal groups 16SrI, 16SrXII and 16SrII (Khan et al., Reference Khan, Botti, Paltrinieri, Al-Subhi and Bertaccini2002; Botti and Bertaccini, Reference Botti and Bertaccini2006).
Abiotic factors also facilitate the spread and prevalence of phytoplasmas. The weather influences the life cycle, behaviour and abundance of insect vectors responsible for phytoplasma transmission. Galetto et al. (Reference Galetto, Marzachì, Marques, Graziano and Bosco2011) found that two phytoplasma – chrysanthemum yellows (vector: Euscelidius variegatus, host: daisy) and ‘Flavescence dorée’ (vector: Scaphoideus titanus, host: broad bean) multiplied faster in insects when it was cooler and in plants when it was warmer. Similarly, Maggi et al. (Reference Maggi, Galetto, Marzachì and Bosco2014) discovered that the epidemics of chrysanthemum yellows phytoplasma in Chrysanthemum carinatum plants were faster at higher temperatures, with a linear increase in spreading rate from 0.2 plants infected per day at 15°C to about 0.7 plants per day at 30° Ca. Phytoplasma infections are also influenced by prevailing winds and geographical factors, such as mountain ranges, which determine their spread and direction of lethal yellowing of coconut palm (Mpunami et al., Reference Mpunami, Tymon, Jones and Dickinson2000; Mora-Aguillera, Reference Mora-Aguillera2002).
Surveillance and detection of phytoplasmas
The surveillance of phytoplasmas encompasses various techniques aimed at monitoring their presence and distribution in plant populations. Historically, methods like symptom profiling, microscopy, serology and dodder transmission studies have been employed for disease detection (Nair and Manimekalai, Reference Nair and Manimekalai2021; Gupta et al., Reference Gupta, Handa, Brakta, Negi, Tiwari, Lal and Kumar2023). However, recent advances in molecular techniques, such as PCR and loop-mediated isothermal amplification (LAMP), have revolutionized early detection capabilities (Jawhari et al., Reference Jawhari, Abrahamian, Sater, Sobh, Tawidian and Abou-Jawdah2015; Parnell et al., Reference Parnell, van den Bosch, Gottwald and Gilligan2017). Additionally, biosensing techniques and innovative surveillance methods like remote sensing and citizen science initiatives have enhanced the ability to monitor phytoplasma populations (Dyussembayev et al., Reference Dyussembayev, Sambasivam, Bar, Brownlie, Shiddiky and Ford2021; Parnell et al., Reference Parnell, van den Bosch, Gottwald and Gilligan2017). These developments have significantly improved early detection and monitoring strategies. Various surveillance strategies, such as airborne surveillance and habitat monitoring, offer valuable insights into vulnerable plant hosts and habitats, aiding in resource allocation and decision-making for habitat restoration and biosecurity (Mitchell, Reference Mitchell2024). Moreover, effective monitoring and surveillance methods, informed by statistical analyses such as geographic information systems (GIS), are critical for timely detection and management of phytoplasma diseases (Mitchell, Reference Mitchell2024; Parnell et al., Reference Parnell, van den Bosch, Gottwald and Gilligan2017).
The implementation of PCR and nested-PCR assays enables the broad detection of phytoplasma presence, including instances of mixed infection, in field-collected samples (Bertaccini et al., Reference Bertaccini, Duduk, Paltrinieri and Contaldo2014). Utilizing conserved gene sequences has represented a significant breakthrough in detecting, identifying and categorizing phytoplasmas. A barcode system was previously utilized for the detection and identification of phytoplasmas (Bertaccini et al., Reference Bertaccini, Duduk, Paltrinieri and Contaldo2014). Additionally, the introduction of diagnostic tests based on quantitative PCR assays (qPCR) has proven highly sensitive, reducing the risk of amplicon contamination and eliminating the need for gel-based post-PCR product analysis, thus establishing qPCR as a reliable alternative method to nested-PCR assays in routine testing (Pérez-López et al., Reference Pérez-López, Rodríguez-Martínez, Olivier, Luna-Rodríguez and Dumonceaux2017). PCR assays employing primers sourced from phytoplasma-specific DNA probes or sequences from the 16S rRNA gene have demonstrated superior sensitivity in detecting phytoplasmas within infected plant or insect hosts. Identification and classification have typically involved the use of RFLP analysis of this genetic locus, leading to the delineation of over thirty 16Sr groups designated as 16SrI – 16SrXXXIII (Pérez-López et al., Reference Pérez-López, Rodríguez-Martínez, Olivier, Luna-Rodríguez and Dumonceaux2017). Using a primer pair (P1/Tint) identified in a portion of the tRNAIle region within the spacer region resulted in a universal phytoplasma detection involving a secondary PCR product of approximately 200 bp (Smart et al., Reference Smart, Schneider, Blomquist, Guerra, Harrison, Ahrens, Lorenz, Seemuller and Kirkpatrick1996). Universal PCR primers targeting the 16S rRNA gene have also facilitated the detection of known phytoplasma strains (Gundersen and Lee, Reference Gundersen and Lee1996; EPPO, 2018). However, alternative genes, such as groEL which is also known as cpn60, have been utilized as supplementary markers for phytoplasma identification and classification (Pérez-López et al., Reference Pérez-López, Rodríguez-Martínez, Olivier, Luna-Rodríguez and Dumonceaux2017). The cpn60 universal target (cpn60 UT), spanning approximately 550 bp, resides within the Cpn60-encoding gene, recognized as a molecular barcode for the Bacteria domain, and serving as a taxonomic marker for characterizing microbial communities (Pérez-López et al., Reference Pérez-López, Rodríguez-Martínez, Olivier, Luna-Rodríguez and Dumonceaux2017).
Despite significant progress, persistent limitations primarily stem from the intricate nature of phytoplasma infections and their accelerated spread through global plant trade (Pierro et al., Reference Pierro, Semeraro, Luvisi, Garg, Vergine, De Bellis and Gill2019). Agricultural practices face substantial consequences due to challenges in early identification (Dyussembayev et al., Reference Dyussembayev, Sambasivam, Bar, Brownlie, Shiddiky and Ford2021). Statistical methodologies play a crucial role in guiding surveillance endeavours, aiding in resource allocation and decision-making for habitat restoration and establishment (Mitchell, Reference Mitchell2024; Parnell et al., Reference Parnell, van den Bosch, Gottwald and Gilligan2017). Nonetheless, the challenge of detecting phytoplasmas in late spring may be attributed to their proliferation time on stems, branches and new foliage (Gupta et al., Reference Gupta, Handa, Brakta, Negi, Tiwari, Lal and Kumar2023). Addressing these constraints necessitates ongoing research and innovative detection technologies to mitigate the impact of phytoplasma diseases on agriculture and ecosystems. Despite advancements in surveillance and detection techniques, several challenges persist, particularly in early identification due to inconspicuous symptoms and the erratic distribution of phytoplasmas within infected plants (Dyussembayev et al., Reference Dyussembayev, Sambasivam, Bar, Brownlie, Shiddiky and Ford2021; Gupta et al., Reference Gupta, Handa, Brakta, Negi, Tiwari, Lal and Kumar2023). Moreover, predicting phytoplasma effectors remains challenging, hindering effectorome comparisons (Carreón-Anguiano et al., Reference Carreón-Anguiano, Vila-Luna, Sáenz-Carbonell and Canto-Canche2023). Table 2 shows techniques and principles of phytoplasma detection. The difficulty in detecting phytoplasmas during late spring may be attributed to their proliferation on stems, branches and new leaves (Gupta et al., Reference Gupta, Handa, Brakta, Negi, Tiwari, Lal and Kumar2023). When examining a pear tree, symptoms indicative of pear decline might easily be misinterpreted as signs of other problems like graft-incompatibility, chlorosis, virus-related diseases, or even drought (Errea et al., Reference Errea, Aguelo and Hormaza2002). However, enhancing early detection capabilities necessitates reliable detection methods and a deeper comprehension of phytoplasma biology. Table 3 depicts the challenges and solutions for early detection of phytoplasma.
Techniques and principles of phytoplasma detection
Challenges and solutions for early detection of phytoplasma
Case studies on selected phytoplasma-related disease outbreaks
The global impact of phytoplasma diseases on crops and other environmentally significant plants is profoundly concerning (Bertaccini, Reference Bertaccini2021). These pathogens have caused substantial economic losses and continue to pose significant threats to agricultural sustainability (Pierro et al., Reference Pierro, Semeraro, Luvisi, Garg, Vergine, De Bellis and Gill2019). Multiple cases of devastating consequences of these diseases on various categories of crop species including tree crops (e.g. grapevines, apples, coconuts), vegetables (tomatoes, potatoes, carrots), cereals (maize) and legumes have been reported across different regions of the world (Pierro et al., Reference Pierro, Semeraro, Luvisi, Garg, Vergine, De Bellis and Gill2019; Siampour et al., Reference Siampour, Izadpanah, Salehi, Afsharifar, Olivier, Dumonceaux and Pérez-López2019). The outbreak of phytoplasma-related diseases highlights the high vulnerability of global cropping sysems and stresses the importance of continuous research in developing resistant varieties and innovative control methods (Hemmati et al., Reference Hemmati, Nikooei and Al-Sadi2021a). Currently, there is a continuous effort to control the impact of phytoplasma diseases in several crop cultivation areas across the globe (Wang et al., Reference Wang, Bai, Li, Wang, Huang, Wu and Zhao2024). Knowledge about previous outbreaks of the disease, management practices and current status of these diseases is essential in facilitating research and development efforts. A case study of selected phytoplasma diseases is briefly presented below:
Grapevine yellows diseases
The Grapevine yellow (GY) diseases are a group of phytoplasma-associated diseases affecting grapevines worldwide. Twelve ‘Ca. Phytoplasma’ species, distributed across 17 16SrRNA subgroups, are reported to be associated with these diseases (Bertaccini et al., Reference Bertaccini, Arocha-Rosete, Contaldo, Duduk, Fiore, Montano and Zamorano2022). In Europe, the most significant GY diseases are Flavescence dorée and Bois noir (BN), both of which have caused severe damage to viticulture over several decades (Jarausch et al., 2021; Belli et al., Reference Belli, Bianco and Conti2010). Flavescence dorée is linked to phytoplasmas belonging to the 16SrV-C and 16SrV-D subgroups, while BN disease is associated with phytoplasmas of the 16SrXII-A subgroup (Bertaccini et al., Reference Bertaccini, Calari and Felker2007; Reference Bertaccini, Duduk, Paltrinieri and Contaldo2014). GY outbreaks, particularly in Europe, have led to significant economic losses, reduced grape, apple, and peach yields, and quality deterioration, adversely affecting the wine industry (Ember et al., Reference Ember, Bodor, Zsófi, Pálfi, Ladányi, Pásti and Bisztray2018). Severe outbreaks in Italy, France, and Spain have produced symptoms such as leaf rolling, vine decline, shrivel.
Management strategies
Effective management of GY disease involves a comprehensive approach, including cultural practices such as removing infected vines planting disease-resistant cultivars, and implementing rigorous monitoring using molecular diagnostic tools (Oliveira et al., Reference Oliveira, Roriz, Vasconcelos, Bertaccini and Carvalho2019). Chemical control is limited due to the feeding behaviour of insect vectors (primarily leafhoppers), but integrated pest management strategies, incorporating biological controls such as predatory insects, are being explored, though further research is needed for widespread application (Bianco et al., Reference Bianco, Romanazzi, Mori, Myrie, Bertaccini, Bertaccini, Weintraub, Rao and Mori2019; Belli et al., Reference Belli, Bianco and Conti2010; Boudon-Padieu, Reference Boudon-Padieu2003). Early detection and removal of infected vines, combined with strict quarantine measures, remain crucial for preventing further spread (Krüger et al., Reference Krüger, Pietersen, Pietersen, Stiller, Engelbrecht, Rensburg and Bertaccini2022). Current research focuses on pathogen diversity, vector ecology, and host-pathogen interactions, aiming to develop sustainable management strategies and resilient grape cultivars through coordinated global efforts (Krüger et al., Reference Krüger, Pietersen, Pietersen, Stiller, Engelbrecht, Rensburg and Bertaccini2022; Zambon et al., Reference Zambon, Canel, Bertaccini and Contaldo2018; Abu Alloush et al., Reference Abu Alloush, Bianco, Busato, Alkhawaldeh, Alma, Tedeschi and Quaglino2023; Bertaccini, Reference Bertaccini2021).
Witches’ broom disease of lime
Witches’ broom disease of lime (WBDL), caused by ‘Ca. Phytoplasma aurantifolia’ (16Sr II-B), has severly affected Mexican lime production. The disease originated in Oman and subsequently spread to Brazil, the Middle East, and India (Hemmati et al., Reference Hemmati, Nikooei and Al-Sadi2021a; Al-Yahyai et al., Reference Al-Yahyai, Al-Sadi, Al-Said, Al-Kalbani, Carvalho, Elliot and Bertaccini2015). The outbreak destroyed over 50% of lime cultivation in some areas, leading to significant economic losses. Early symptoms include proliferation of multiple small pale-green leaves, which later dry and drop, leaving dead twigs (Donkersley et al., Reference Donkersley, Silva, Carvalho, Al-Sadi and Elliot2018a).
Management strategies
Control measures for WBDL involve a combination of cultural, biological, and chemical approaches (Donkersley et al., Reference Donkersley, Blanford, Queiroz, Silva, Carvalho, Al-Sadi and Elliot2018b). Cultural measures include pruning infected branches, removing severely affected trees, and controlling weed hosts. Biological control methods, including the use of natural enemies of the psyllid vector and entomopathogenic fungi, have shown promise (Siampour et al., Reference Siampour, Izadpanah, Salehi, Afsharifar, Olivier, Dumonceaux and Pérez-López2019). However, insecticide-based chemical control is challenging due to the rapid reproduction of psyllids. Complete removal of infected trees in endemic areas is recommended to reduce disease spread (Hemmati et al., Reference Hemmati, Nikooei and Al-Sadi2021a). WBDL management underscores the importance of early detection and rapid response. The persistence of ‘Ca. Phytoplasma aurantifolia’ in alternative hosts and wild plant species complicates eradication efforts (Bertaccini, Reference Bertaccini2023). Despite extensive control strategies, challenges persist due to the pathogen’s wide host range, difficulty in controlling psyllid populations, and its capacity to infect multiple citrus species (Golmohammadi et al., Reference Golmohammadi, Khankahdani and Rastegar2023). Research on WBDL focuses on understanding pathogen epidemiology, transmission dynamics, and genetic diversity (Bertaccini, Reference Bertaccini2023). Studies of psyllid vector behaviour also support efforts to breed resistant cultivars and develop biocontrol agents (Mankin and Rohde, Reference Mankin and Rohde2020). Advances in diagnostic tools and epidemiological modelling are contributing to improved management strategies (Santos et al., Reference Santos, Mora-Ocampo, de Novais, Aguiar and Pirovani2023). Collaboration among researchers, growers, and regulatory agencies remains essential in combating WBDL.
Lethal yellowing diseases
Lethal yellowing disease (LYD) is a devastating phytoplasma-mediated condition affecting about 35 palm species and characterized by similar symptoms (Gurr et al., Reference Gurr, Johnson, Ash, Wilson, Ero, Pilotti and You2016). LYD was first observed in the Caribbean Island at the end of the 19th century. In Jamaica and the Americas, the disease is simply referred to as LYD, and as lethal yellowing-like diseases in other parts of the globe. LYD poses major impacts on palm trees, especially coconut trees, thus affecting global coconut production (Oropeza-Salín et al., 2020). LYD and related diseases lead to rapid palm death, causing premature fruit shedding, necrosis, and leaf yellowing, with no known cure (Gurr et al., Reference Gurr, Johnson, Ash, Wilson, Ero, Pilotti and You2016; Dollet et al., Reference Dollet, Quaicoe and Pilet2009). These outbreaks, spanning over five decades in various countries worldwide, have caused extensive losses, even affecting previously resistant coconut cultivars in some regions, threatening coconut cultivation globally (Gurr et al., Reference Gurr, Johnson, Ash, Wilson, Ero, Pilotti and You2016; Eziashi and Omamor, Reference Eziashi and Omamor2010). The disease is associated with ‘Ca. Phytoplasma palmae’ (16SrIV-A, -B, -D, E and -F) in the Caribbeans and Americas (EFSA PLH Panel, Reference Jeger, Bragard, Candresse, Chatzivassiliou, Dehnen-Schmutz and Caffier2017). ‘Ca. Phytoplasma palmicola’ (16SrXXII-A, -B) in West Africa and Mozambique (Harrison et al., Reference Harrison, Davis, Oropeza, Helmick, Narvaez, Eden-Green and Dickinson2014) and ‘Ca. Phytoplasma cocostanzaniae’ (16SrIV-C) in Kenya and Tanzania. In Papua New Guinea, ‘Ca. Phytoplasma noviguineense’ (16SrIV) is associated with Bogia Cococnut Syndrome (Miyazaki et al., Reference Miyazaki, Shigaki, Koinuma, Iwabuchi, Rauka, Kembu and Namba2018).
Management strategies
LYD outbreaks have had devastating impacts on coconut palms and other susceptible species (Gurr et al., Reference Gurr, Johnson, Ash, Wilson, Ero, Pilotti and You2016). Management of LYD involves various approaches, including removal and destruction of infected palms to reduce spread of disease, controlling insect vectors and employing resistant palm species or varieties (Gurr et al., Reference Gurr, Johnson, Ash, Wilson, Ero, Pilotti and You2016). The persistence of phytoplasmas in alternative hosts and weed reservoirs complicates disease management. Application of antibiotics such as oxytetracycline and cultural practices via trunk injections have been attempted, though with limited success (Soto et al., Reference Soto, Helmick, Harrison and Bahder2021).
‘Candidatus Phytoplasma solani’
The outbreak of ‘Ca. Phytoplasma solani’ in Serbia and neighbouring regions posed a severe threat to crops, such as potatoes and tomatoes, causing stunting and leaf deformation (Mitrović et al., Reference Mitrović, Marinković, Cvrković, Jović, Krstić and Jakovljević2022; Kosovac et al., Reference Kosovac, Johannesen, Krstić, Mitrović, Cvrković, Toševski and Jović2018). The pathogen’s prevalence in Europe results in substantial economic losses, despite control efforts involving quarantine measures, crop rotation and insecticides application (Kosovac et al., Reference Kosovac, Ćurčić and Stepanović2023; Jakovljević et al., Reference Jakovljević, Jović, Krstić, Mitrović, Marinković, Toševski and Cvrković2020; Quaglino et al., Reference Quaglino, Zhao, Casati, Bulgari, Bianco, Wei and Davis2013). Challenges persist due to its varied host range, making vector control complex and necessitating separate disease management strategies in affected regions (Kosovac et al., Reference Kosovac, Ćurčić and Stepanović2023; Pierro et al., Reference Pierro, Panattoni, Passera, Materazzi, Luvisi, Loni, Ginanni, Lucchi, Bianco and Quaglino2020).
Management strategies
Managing outbreaks of ‘Ca. Phytoplasma solani’ involves integrated pest management practices, including the removal and destruction of infected plants, controlling insect vectors and implementing strict quarantine measures to limit disease spread (Carminati et al., Reference Carminati, Brusa, Loschi, Ermacora and Martini2021). Cultural practices such as crop rotation, planting disease-resistant cultivars and the use of healthy planting material, contribute to disease reduction (Sémétey et al., Reference Sémétey, Gaudin, Danet, Salar, Theil, Fontaine and Foissac2018). Chemical control targeting insect vectors may be employed, but effectiveness varies due to the diverse nature of the vectors and their habitats (Mitrović et al., Reference Mitrović, Marinković, Cvrković, Jović, Krstić and Jakovljević2022). Lessons learned from ‘Ca. Phytoplasma solani’ outbreaks stress early detection, rapid response and preventive measures (Nutricati et al., Reference Nutricati, De Pascali, Negro, Bianco, Quaglino, Passera and Luvisi2023). Understanding vector behaviour aids in targeted control. Quarantine and biosecurity are crucial (Chalam et al., Reference Chalam, Kumari, Deepika, Yadav, Kalaiponmani and Maurya2023). The current situation regarding ‘Ca. Phytoplasma solani’ outbreaks varies across affected regions, with sporadic occurrences reported in some areas while persistent outbreaks continue in others (Mitrović et al., Reference Mitrović, Marinković, Cvrković, Jović, Krstić and Jakovljević2022). Despite control efforts, challenges remain due to the complexity of vector-pathogen interactions, multiple potential reservoir hosts and environmental factors influencing disease spread (Kosovac et al., Reference Kosovac, Ćurčić and Stepanović2023). Research on ‘Ca. Phytoplasma solani’ emphasizes pathogen diversity, genetic studies and rapid diagnostics (Nutricati et al., Reference Nutricati, De Pascali, Negro, Bianco, Quaglino, Passera and Luvisi2023; Çağlar et al., Reference Çağlar, Şimşek, Dikilitas and Bertaccini2021).
Focus areas includes vector biology, biocontrol agents and breeding resistant plants. The outbreak highlights the critical importance of proactive disease management through surveillance, early detection, and eradication. Integrated methods and collaborations have proven crucial for successful control in vineyards (Kosovac et al., Reference Kosovac, Ćurčić and Stepanović2023; Mitrović et al., Reference Mitrović, Marinković, Cvrković, Jović, Krstić and Jakovljević2022). Figure 1 indicates representative phytoplasma diseases, countries of major reported occurrence, management strategies, lessons learnt, and current situations and research efforts. The integration of various control methods, including both cultural practices and chemical treatments, was vital for effective disease management. Furthermore, collaboration between researchers, vineyard owners and governmental agencies was essential to implement and sustain these control measures, successfully.
Representative phytoplasma diseases, countries of major reported occurrence, management strategies, lessons learnt and current situation and research effort.
International cooperation for phytoplasma disease control
The International Plant Protection Convention (IPPC) has outlined measures to curb the global outbreak of plant pests, aiming to mitigate negative impacts on food security, biodiversity, and economic prosperity. Currently, there is no effective curative treatment for LYD; however, thanks to the efforts of Michael Black, outbreaks have been maintained at manageable levels. As a palm grower in Jamaica, Black has significantly reduced the incidence of the disease on his farm by employing an integrated pest management approach. This includes on-farm quarantine measures, rigorous weekly surveillance, the removal and burning of palms exhibiting LYD symptoms, and the replanting of disease-resistant varieties. Also, by managing weeds and applying fertilizers effectively, as shown in the studies by Myrie et al. (2011), Serju (Reference Serju2012), and CARDI (2013), farmers can improve the health and yield of palm crops.
A large group of plant pests threaten global food production, forest productivity, biodiversity, and natural flora. Therefore, preventing the spread and establishment of these harmful pests in new countries and regions is the main task of national plant protection organizations (NPPOs) and the IPPC. These NPPOs are reliable entities entrusted with responsibilities to provide and receive government-to-government phytosanitary assurances, and should be resourced to accomplish this core mandate successfully. Myrie et al. (2011) and Serju (Reference Serju2012) documented that an extensive comparison of seven selected farms over several years revealed a significant reduction in LYD incidence on four farms that implemented Black’s management practices. In contrast, three farms that did not adopt any management strategies continued to suffer severe losses due to the disease. Globally, it is recommended that infected palms be promptly removed and destroyed. Eradication programs should be enhanced with natural barriers to prevent vector movement, along with the application of insecticides and antibiotic treatments via trunk injection using tetracycline products (McCoy et al., Reference McCoy, Carroll, Poucher and Gwin1976; Eziashi and Omamor, Reference Eziashi and Omamor2010; Wang et al., Reference Wang, Bai, Li, Wang, Huang, Wu and Zhao2024). Figure 2 shows a network diagram showing international research collaboration under EU-funded TROPICSAFE Project (Adapted from Final Handbook with Innovation Factsheets).
A Network Map showing international research collaboration involved in the TROPICSAFE Project (Adapted from Final Handbook with Innovation Factsheets, www.tropicsafe.eu). A=The Americas, B=Africa, C=Europe.
Research initiatives and funding
Phytoplasma research projects have received a substantial amount of financial support from funding agencies to study pathogen identification on different crops across the globe. The European Union’s Horizon 2020 programme (2014–2020) allocated nearly €80 billion to research and innovation. The TROPICSAFE Project, involving 22 partners from 12 countries, received €4 million of this funding. The project focuses on identifying insect-borne prokaryote-associated diseases in tropical and subtropical perennial crops (www.tropicsafe.eu). Major diseases under this funding include lethal yellowing in palms (‘Ca. Phytoplasma’ species), yellows in grapevines (‘Ca. Phytoplasma’ species), and Huanglongbing in citrus (‘Ca. Liberibacter’ species). The aims include: (1) generating data on epidemiological cycles, insect vectors, and alternative host plants; (2) developing rapid, reliable detection methods and holistic management approaches; and (3) scaling up demonstration activities and field trials to improve farmers’ livelihoods. Researchers from Canada and Côte d’Ivoire are also exploring ways to reduce coconut crop losses from lethal yellowing, which devastates plantations in West Africa. Improved understanding of the disease, plant breeding, and replanting efforts will help preserve the livelihoods of Côte d’Ivoire’s coconut farmers. Table 4 shows funding allocation for phytoplasma research. The Canadian International Food Security Research Fund (CIFSRF) has contributed CA$2.57 million to this work.
Funding allocation for Phytoplasma research
Management strategies of phytoplasma-mediated diseases
The lack of a cell wall by phytoplasmas makes them difficult to target with traditional bactericides (Hogenhout et al., Reference Hogenhout, Oshima, Ammar, Kakizawa, Kingdom and Namba2008). Consequently, managing phytoplasma-mediated diseases primarily involves targeting the insect vectors responsible for transmitting these pathogens, rather than directly treating infected plants (Bianco et al., Reference Bianco, Romanazzi, Mori, Myrie, Bertaccini, Bertaccini, Weintraub, Rao and Mori2019). As there is currently no effective cure, mitigation strategies emphasize preventive cultural practices (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). Cultural practices play a pivotal role in managing phytoplasma diseases and include adopting resistant plant varieties, rogueing (removing and destroying infected plants), ensuring the use of clean propagating material, and controlling insect vectors known to transmit phytoplasmas (Bertaccini, Reference Bertaccini2021).
Antibiotics and other molecules
Even though antibiotics such as tetracyclines have been used in the field to control phytoplasma diseases in some high-value crops, their extensive use is limited by costs, emergence of resistant microbial strains, potential hazards to humans and concerns with environmental pollution (Tanno et al., Reference Tanno, Maejima, Miyazaki, Koinuma, Iwabuchi, Kitazawa, Nijo, Hashimoto, Yamaji and Namba2018). Other molecules such as ribosome-inactivating proteins, plant hormones and resistance inducers have been tested and shown to exhibit some level of efficacy (Bertaccini, Reference Bertaccini2021). Additionally, essential oils and ribosome-inactivating proteins have demonstrated promising results in eliminating phytoplasmas in micro-propagated infected plant shoots (Bertaccini, Reference Bertaccini2021). In vitro systems have also been utilized to produce phytoplasma-free germplasm, which can be further propagated in insect-proof conditions before deployment in open fields (Hogenhout, Reference Hogenhout2009). These diverse strategies offer a multifaceted approach to mitigate the impact of phytoplasma diseases on crops while minimizing reliance on traditional antibiotics.
Resistant plant varieties
Resistant plant varieties play a crucial role in reducing the susceptibility of crops to phytoplasma infections (Gorshkov and Tsers, Reference Gorshkov and Tsers2022). Several species have been identified for their resistance to specific phytoplasma infections, contributing to crucial insights for disease management and breeding programs (Wei et al., Reference Wei, Trivellone, Dietrich, Zhao and Ivanauskas2021). For example, S. mulayanum and S. alatum have been identified as being resistant to sesame phyllody, with S. alatum specifically noted for possessing a dominant gene linked to phyllody resistance (Yadav et al., Reference Yadav, Kalia, Rangan, Pradheep, Rao, Kaur, Pandey, Rai, Vasimalla, Langyan, Sharma, Thangavel, Rana, Vishwakarma, Shah, Saxena, Kumar, Singh and Siddique2022). In temperate fruit trees, various Prunus species, including European plum, sour and sweet cherry, demonstrated reduced susceptibility to European Stone Fruit Yellows (ESFY) phytoplasma infections, with some exhibiting tolerance and resistance (Cieślińska, Reference Cieślińska2011). Additionally, several Prunus species, such as P. betulifolia, P. calleryana, P. nivalis, P. elaeagrifolia, P. syriaca, P. pashia and P. dimorphophylla, were found to be resistant to Pear Decline phytoplasma infections (Marcone et al., Reference Marcone, Valiunas, Salehi, Mondal and Sundararaj2023). These resistant cultivars are essential for long-term disease management and breeding efforts aimed at developing elite plant lines with enhanced resistance (Roy et al., Reference Roy, Sahu, Das, Bhattacharyya, Raina and Mondal2023). Natural resistance mechanisms, including non-host resistance, are also valuable in managing phytoplasma diseases (Hogenhout, Reference Hogenhout2009). While resistant plant varieties play a crucial role in reducing the susceptibility of crops to phytoplasma diseases, their effectiveness may diminish over time. This may can be due to the emergence of new phytoplasma strains or changes in environmental conditions that can overcome these resistance mechanisms.
Use of disease-free materials
The use of disease-free planting material is crucial to minimizing phytoplasma contamination (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). This approach aligns with the principles of integrated pest management, emphasizing sustainable and holistic practices in agriculture (Deguine et al., Reference Deguine, Aubertot, Flor, Lescourret, Wyckhuys and Ratnadass2021). Ongoing research and adaptive strategies remain crucial to staying ahead of evolving challenges posed by phytoplasma diseases and their vectors.
Rogueing
Rogueing, the removal and destruction of infected plants, helps prevent the spread of phytoplasmas to healthy plants (Jeger and Gilligan, Reference Jeger and Gilligan2007). The primary objective of rogueing is twofold. Firstly, it aims to suppress the disease by preventing the dissemination of phytoplasmas (Bertaccini, Reference Bertaccini2021). In doing so, it disrupts the transmission cycle, especially considering the common mode of transmission through insect vectors. Secondly, rogueing serves as a vigilance monitoring tool, enabling the early detection of infected plants (Sisterson and Stenger, Reference Sisterson and Stenger2013). Early identification is crucial for swift action, preventing the disease from establishing and spreading extensively within the crop. However, rogueing is labour-intensive and costly, especially for small-scale farmers (Welbaum, 2017). Training and awareness programmes are therefore essential to ensure accurate symptom recognition.
Control of insect vectors
Phytoplasma diseases are primarily transmitted by insect vectors, particularly leafhoppers, planthoppers and psyllids (Kumari et al., Reference Kumari, Nagendran, Rai, Singh, Rao and Bertaccini2019). Identification of vector species transmitting specific phytoplasma strains is essential for targeted control strategies. For example, the cixiid planthopper Hyalesthes obsoletus is the main vector of the 16SrI-B phytoplasma strain causing sesame phyllody (Kosovac et al., Reference Kosovac, Johannesen, Krstić, Mitrović, Cvrković, Toševski and Jović2018). In the case of ESFY, the psyllid Cacopsylla pruni is the primary vector transmitting the 16SrX-B phytoplasma to temperate fruit trees (Riedle-Bauer et al., Reference Riedle-Bauer, Paleskić, Schwanzer, Kölber, Bachinger, Schönhuber, Elek, Stradinger, Emberger, Engel, Makay, Zajcsek and Brader2019). The control of insect vectors in the context of phytoplasma diseases requires a multifaceted and integrated approach (Weintraub and Beanland, Reference Weintraub and Beanland2006). By combining insect vector surveillance, biological control, and when necessary, targeted chemical interventions, farmers can effectively manage vector populations and minimize the risk of phytoplasma transmission (Skendžić et al., Reference Skendžić, Zovko, Živković, Lešić and Lemić2021). Sustainable and environmentally friendly strategies are essential to protect agricultural ecosystems. Chemical vector control should be used cautiously due to potential ecological and environmental impacts (Gurr et al., Reference Gurr, Bertaccini, Gopurenko, Krueger, Alhudaib, Liu, Fletcher and Wakil2015). Nevertheless, in certain situations, specific classes of pesticides may be considered. These include neonicotinoids, pyrethroids, organophosphates, insect growth regulators (IGRs) and botanical insecticides (Lalah et al., Reference Lalah, Otieno, Odira and Ogunah2022). Important considerations include managing resistance, minimizing harm to non-target organisms, environmental impact, adherence to legal regulations and precise application timing (Damalas and Eleftherohorinos, Reference Damalas and Eleftherohorinos2011).
Good Agricultural Practices (GAPs)
Good sanitation practices, such as proper pruning and propagation techniques, are important in preventing the spread of phytoplasma diseases (Bertaccini, Reference Bertaccini2021). Timely planting is also critical, as susceptibility can vary with planting dates (Marcone et al., Reference Marcone, Valiunas, Salehi, Mondal and Sundararaj2023). To effectively manage phytoplasma diseases, it is crucial to combine multiple cultural practices, as relying on a single method may prove insufficient. Figure 3 is an infographic showing phytoplasmas disease management approaches.
An infographic showing Integrated Pest Management Approaches.
Future perspectives
Human activities, such as monoculture farming and global trade, facilitate the rapid evolution of phytoplasmas, posing significant threats to global food security. Monitoring genetic diversity, mutation rates and potential host shifts is crucial for understanding and tackling emerging challenges. Expected trends include the development of more virulent strains and changes in host ranges (Venbrux et al., Reference Venbrux, Crauwels and Rediers2023). Research into vector ecology, particularly the role of insect species, is essential to understand the factors influencing pathogen evolution and gene flow.
Technological advancement is vital for enhancing detection and control of phytoplasma infections (Carvajal-Yepes et al., Reference Carvajal-Yepes, Cuervo, Kreuze, Alakonya, Kumar, Onaga and Bui2022). The collective employment of rapid and reliable diagnostic tools, molecular techniques such as PCR-based assays, advanced imaging technologies and omics Sciences such as genomics and proteomics offer promise for improved and accurate detection (Carvajal-Yepes et al., Reference Carvajal-Yepes, Cuervo, Kreuze, Alakonya, Kumar, Onaga and Bui2022). Control strategies should explore new antimicrobial agents, resistant crop varieties and environmentally sustainable practices. Collaboration among researchers, agriculturists and industry players is crucial for practical solutions.
Developing resilient agricultural systems is imperative to mitigate the impact of emerging phytoplasma on global food security (Altieri, Reference Altieri1999). Integrated pest management, crop diversification and rotation practices are essential for enhancing crop resilience. Fostering resilient farming communities through education and extension services, empowering farmers with knowledge on disease prevention and sustainable practices; these contribute to building a robust defence against phytoplasma threats.
Recent breakthroughs in machine learning, geospatial analytics and big data mining, present exciting possibilities in battling phytoplasma-mediated diseases (Buja et al., Reference Buja, Sabella, Monteduro, Chiriacò, De Bellis, Luvisi and Maruccio2021; Kasinathan et al., Reference Kasinathan, Singaraju and Uyyala2021; Ristaino et al., Reference Ristaino, Anderson, Bebber, Brauman, Cunniffe, Fedoroff, Finegold, Garrett, Gilligan, Jones, Martin, MacDonald, Neenan, Records, Schmale, Tateosian and Wei2021; Silva et al., Reference Silva, Tomlinson, Onkokesung, Sommer, Mrisho, Legg, Adams, GutierrezVazquez, Howard, Laverick, Hossain, Wei, Gold and Boonham2021; Zhang et al., Reference Zhang, Huang, Pu, Gonzalez-Moreno, Yuan, Wu and Huang2019). AI-driven monitoring systems can provide real-time alerts, contributing to proactive responses. Precision agriculture, guided by AI, optimizes resource use and enhances farm efficiency, providing adaptive management strategies against phytoplasma threats. These technologies also have the capacity to establish and strengthen global surveillance networks for phytoplasma for early detection and timely response (Carvajal-Yepes et al., Reference Carvajal-Yepes, Cardwell, Nelson, Garrett, Giovani, Saunders, Kamoun, Legg, Verdier, Lessel, Neher, Day, Pardey, Gullino, Records, Bextine, Leach, Staiger and Tohme2019). International collaboration, standardized surveillance protocols and remote sensing technologies are essential to prevent transboundary spread and ensure coordinated control measures.
In the long term, climate change may influence the spread of plant diseases, including phytoplasma infections (Chaloner et al., Reference Chaloner, Gurr and Bebber2021; Delgado-Baquerizo, Reference Delgado-Baquerizo2020; Dudney et al., Reference Dudney, Willing, Das, Latimer, Nesmith and Battles2021). Understanding the potential impact of climate change on the distribution and prevalence of phytoplasmas and their vectors is critical. Climate modelling combined with epidemiological studies can predict areas at heightened risk, enabling proactive mitigation strategies.
Public–private partnerships are effective for accomplishing extension and outreach objectives in plant pathology (Markell et al., Reference Markell, Tylka, Anderson and van Esse2020). Collaboration between academia, government, NGOs and agribusinesses expedites the development and implementation of new technologies and control strategies. Public-private collaborations enhance the accessibility and affordability of diagnostic tools, treatments and preventive measures, benefiting farmers globally.
Investing in capacity building and education programs is fundamental for building resilience plant protection (Gervais, Reference Gervais2004). Empowering individuals with knowledge and skills to identify, manage and prevent phytoplasma infections ensures a robust and adaptive agricultural sector. Training initiatives that cover integrated pest management, sustainable agriculture, and responsible technology use ensure a robust and adaptive agricultural sector capable of responding effectively to phytoplasma threats.
Conclusion
This review highlights the rising incidence of phytoplasma infections across diverse crops, ranging from staple grains to high-value cash crops, and their potential impact on food production. The adaptability of phytoplasmas to new environments and hosts, coupled with climate change, underscores the urgency of addressing this emerging agricultural challenge. The immediate and long-term implications for global food security necessitate a collaborative, multi-faceted approach to mitigate phytoplasma threats and safeguard future food supplies.
Data availability statement
All the data used and generated in the study can be found in this manuscript.
Author contributions
OFA: Study-conceived and designed, Writing-original draft, Review & Editing; AKD, JOH: Writing-original draft, Review & Editing; FKA, JO, AM, AFO, KO, FLS, NEY, HL: Writing-original draft; BAO: Formatting, Review & Editing.
Funding statement
Not applicable.
Competing interests
The authors affirm there were no financial or commercial ties that might be viewed as having a potential conflict of interest.
Ethics standards
Not applicable.
