Unveiling the phloem: a battleground for plant pathogens

Abstract

Phloem is the primary conduit for transporting photosynthates and signaling molecules in plants, facilitating communication between various plant organs. As an ancient vascular tissue, phloem transports sugars, proteins, and hormones from source tissues to sinks over long distances. However, this vital transport system also serves as a battlefield where plants and pathogens compete for survival. The phloem’s nutrient-rich environment offers pathogens a secure habitat, protecting them from external threats while providing ample metabolic resources. Phloem-feeding insects, bacteria, fungi, and viruses exploit this system to access nutrients, leading to widespread diseases and yield losses. These insects can also transmit pathogens, such as viruses, which can evade the plants’ defense systems, causing systemic damage throughout the transport network. This review describes the mechanisms by which pathogens invade and colonize the phloem, the plant’s defense strategies, and their dynamic interactions. Understanding the phloem’s structural intricacies, physiological functions, and defense mechanisms provides a foundation for comprehending phloem–pathogen interactions. Insights into these interactions at the molecular level are crucial for developing innovative and effective disease management strategies. Genomics, proteomics, and bioinformatics advances have elucidated the interactions between phloem defenses and pathogen offenses. Finally, this review discusses integrated disease management strategies to counteract these pathogens, paving the way for improving plant health and resilience.

Background

Plants are unique organisms capable of synthesizing their food and transporting it internally through a network of vascular bundles, consisting of the xylem and phloem. The phloem is a critical component of this system, facilitating the transport of nutrients from sources to sinks, ensuring proper growth and survival. However, it also serves as a habitat and a source of nourishment for numerous harmful pathogens. The phloem transports essential compounds, including sugars, organic acids, amino acids, proteins, small RNAs, mRNAs, and hormones, from source tissues like mature leaves to various sinks such as buds, flowers, seeds, and roots (Zimmermann 1960). The phloem’s structural complexity and the presence of sieve elements, companion cells, and parenchyma cells make it an ideal environment for pathogens. It provides a steady abundance of metabolic resources within a secure habitat that shields them from external elements, other organisms, and pesticides (Jiang et al. 2019; Van Bel and Musetti 2019). This protective environment makes direct invasion by plant pathogens challenging, leading many pathogens to rely on insect vectors for transmission. When plants are attacked, they activate defense mechanisms, but the phloem acts as an avenue for mobile pathogens to escape, damaging the transport network and often leading to diseases (Lough and Lucas 2006; Gross et al. 2022). Phloem-invading prokaryotes include wall-less Mollicutes, such as phytoplasmas, and walled bacteria, such as Candidatus Liberibacter spp (Gonella et al. 2019). These pathogens have adapted to the phloem’s advantageous environment, causing severe crop damage. This review explores the structure and physiology of the phloem in relation to pathogen biology, seeking comprehensive insights to develop innovative strategies for combating these detrimental plant pathogens.

Phloem structure

The phloem is a highly developed vascular tissue comprising companion cells, sieve elements, sieve plates, plasmodesmata, sieve tubes, and sieve plate pores (Lewis et al. 2022) (Fig. 1). Phloem structure can vary among plant species and tissues within the same plant. However, the basic components and functions of the phloem remain consistent across most vascular plants. Vascular bundles are scattered throughout the stem in monocot plants, with no apparent difference between the cortex and pith. The phloem is located outside the xylem in these bundles (Scarpella and Meijer 2004; Pandey et al. 2011). In contrast, dicot plants typically have vascular bundles arranged in a ring around the central pith, with the phloem located on the outer side and the xylem on the inner side. Monocot phloem often lacks companion cells associated with sieve tube elements. Instead, specialized parenchyma cells called albuminous cells may fulfill some of the functions of companion cells (Mauseth 2003). In dicot plants, sieve tube elements are typically associated with companion cells, which provide metabolic support for sieve tube function (Metcalfe and Chalk 1979). The companion cell, located beside the sieve tubes, is crucial for transporting sugars and amino acids bidirectionally within sieve elements. These metabolically active cells, with dense cytoplasm and numerous mitochondria, are mainly observed in certain species (Lalonde et al. 2007). Specialized plasmodesmata link sieve elements to companion cells (Oparka and Turgeon 1999). Sieve elements, essential components of the sieve tube structure in the phloem, originate from uneven mother cell division. The larger cell transforms into the sieve element, while the smaller cell becomes its companion cell(s). The transformation process is marked by the rapid growth of specific protein structures called P-proteins (Cronshaw 1975; Wergin and Newcomb 1970). The sieve element is filled with a concentrated blend of substances resulting from organelle degradation.

Fig. 1

Structure of phloem: Pictorial representation of phloem components viz. companion cell, sieve element, sieve tube, sieve plate, sieve plate pore, and plasmodesmata. The left image shows the translocation of photoassimilates from source cells (leaves) to sink cells (flowers, buds, and roots)

The final stage in forming a sieve tube involves opening the sieve plate pores in the end walls, connecting them to two neighboring sieve elements. Sieve plate pores link adjacent sieve elements to create functional sieve tubes within the phloem for transportation. Plasmodesmata are pores that facilitate material movement between cells. On the sieve tube side, they have one large pore, while on the companion cell side, the cell wall branches connect to the pore, termed pore-plasmodesmata. These structures allow larger proteins to penetrate sieve elements, given their significant size exclusion limit of approximately 70 kDa (Paultre et al. 2016). Plasmodesmata, initially deposited during cell division, are crucial for the developmental processes. According to developmental studies, each plasmodesmata is expected to form a pore in the progeny sieve plate (Esau and Thorsch 1985). Once pores open, the developmental process concludes, and the mature sieve element integrates into the sieve tube. The translocation stream removes residues from degraded organelles and is present in significant amounts in the sieve tube exudates (Knoblauch et al. 2018). Fully developed sieve elements, regardless of location, possess a basic set of cellular components, including mitochondria, P-proteins, plastids specific to sieve elements (SE-plastids), and a distinctively shaped sieve element ER—a stacked smooth endoplasmic reticulum. This maturation process includes the breakdown of organelles such as the vacuole, nucleus, ribosomes, and cytoskeleton.

Phloem: an exclusive domain for pathogens and piercing-sucking insects

Deep within the plants, the phloem is a vital nutrient source for insects and pathogens. Responsible for long-distance molecule transport, the phloem facilitates movement from mature leaves (source tissues) to buds, flowers, seeds, and roots (sink tissues) as a component of the plant’s vascular system. This nutritionally rich environment attracts harmful pests and pathogens, causing substantial financial losses in key crops. For example, citrus greening disease incurs annual costs of up to 418 million dollars in Florida alone (The National Academies Press 2018). Similarly, the yearly economic impact of the brown plant hopper (Nilaparvata lugens, BPH) surpasses 300 million dollars in Asia (Min et al. 2014). Sieve elements also have pores on their side walls, allowing cytoplasmic connections to neighboring companion cells to move photosynthates and other molecules (Kempers et al. 1998; Martens et al. 2006). Companion cells serve as a ‘power supplier’ for sieve elements in adaptation because they have many organelles, especially highly active mitochondria (Van Bel and Knoblauch 2000). As the radial parenchyma cells enveloping phloem tissue engage in physical interactions with companion cells and sieve components through intercellular spaces, they can modify the chemical composition of the apoplastic phloem sap. Numerous pathogens and insects have developed strategies to reach the phloem, which serves as a nutrient-rich habitat. Unlike insects that feed on phloem, prokaryotes cannot enter actively and instead depend on phloem-feeding insects for entry. Phloem-limited pathogenic prokaryotes typically have small genomes, lacking complete metabolic pathways. As a result, many rely on phloem tissues for essential nutrients (Jiang et al. 2019).

Why do some plant pathogens prefer phloem as a habitat?

Some plant pathogens prefer the phloem tissue as a habitat for several reasons: 1) Pathogens restricted to the phloem possess small genomes, lacking essential genes for various metabolic functions, including those involved in the tricarboxylic acid cycle and amino acid production. 2) The phloem serves as a nutrient-rich environment for pathogens due to the abundance of sugars, amino acids, hormones, and essential elements in the transported sap, making it an attractive habitat (Brodbeck et al. 1993; Gündüz and Douglas 2009). 3) Phloem-limited plant pathogens are mainly spread by insect vectors feeding on phloem, acquiring and transmitting prokaryotic pathogens from infected to healthy plants (Gray et al. 2014; Ng and Zhou 2015). 4) Safe location: The phloem tissue is located deep within the plant and is protected by other cell layers, making it a relatively protected and unreachable site for competing pathogens. This physical barrier can protect pathogens from external threats like environmental stress and immunological responses (Lewis et al. 2022). 5) The phloem acts as a long-distance ‘highway’, facilitating the movement of nutrients and signaling chemicals within the plant. Phloem-invading pathogens utilize this network for widespread dissemination and establishment in different plant parts (Lucas et al. 2013). 6) Reduced immunological response: Unlike other plant tissues, the phloem exhibits a lower concentration of immune cells and defense-related compounds. Certain infections can evade or suppress the plant’s defense mechanisms, enabling their effective colonization and establishment within the phloem (Rosen et al. 2015; Perilla-Henao and Casteel 2016). Pathogens can manipulate plant physiology by altering nutrient composition and disrupting hormonal signaling in the phloem, facilitating their growth and survival (Sugio et al. 2011). Several plant pathogens prefer the phloem as a habitat due to the nutrient-rich sap, protection from external factors, opportunity for systemic spread, reduced immune response, and ability to alter plant physiology (Garnier and Bove 2001).

Disruption of phloem transport during infection or defense

According to Cronshaw (1975), the phloem is a microaerophilic habitat rich in carbohydrates and nutrients and provides a suitable environment for plant diseases. Phloem transport is oriented from sugar-producing (photosynthetic) source leaves toward growing or storing sink tissues that assimilate sugars. Phloem transport typically involves the movement of assimilates, including sugars produced in source leaves, towards various sink tissues for growth, storage, or other metabolic processes (Ainsworth and Bush 2011; De Schepper et al. 2013). While this directional flow pattern is typical in many plant species, it is essential to note that phloem transport dynamics can vary depending on developmental stage, environmental conditions, and physiological demands (Van Bel 2003). Therefore, while the general trend involves transport from source to sink tissues, exceptions to this pattern may occur under certain circumstances (Knoblauch and Oparka 2012). By providing a more generalized description of phloem transport directionality, we aim to accurately convey the variability and complexity inherent in plant vascular systems (De Schepper et al. 2013). Although hydrostatic pressure produced by osmosis is assumed to be the primary force behind long-distance phloem movement, its physical characteristics are still poorly understood (Knoblauch and Peters 2010). Hormones, RNA, and proteins are among the signaling and defense substances the phloem delivers across long distances (Dinant and Lemoine 2010; Van Bel et al. 2013). Few molecules have been demonstrated to function in sink tissues, and phloem transport might lack selectivity (Paultre et al. 2016). The phloem’s role in long-distance transport involves systemic defense responses, with hormones like jasmonic and salicylic acid playing a pivotal role (Fu and Dong 2013; Wasternack and Hause 2013). Phloem-transported signals trigger systemic acquired resistance (SAR) and systemic wound response (SWR) (Gao et al. 2015) along with electrophysiological changes (linked to calcium fluxes) that act as defense signals, which propagate rapidly through the plant (Van Bel et al. 2013; Zhang et al. 2014; Hedrich et al. 2016). Phloem-specific defense responses, such as forisomes and P-proteins, involve sealing sieve plates after damage (Gaupels and Vlot 2012; Bataille et al. 2012; Ernst et al. 2012). Callose deposition at sieve plates and companion cell plasmodesmata is a critical response to wounding and pathogens, thus limiting pathogen dispersal (Hao et al. 2008; Voigt 2014). While these deposits do not entirely seal openings, they play a vital role in the plant’s viral defense mechanisms (Zavaliev et al. 2011; Brunkard et al. 2013). Certain pathogens limited to the phloem focus on influencing the synthesis or buildup of secondary metabolites, as their insect vectors are susceptible to these compounds. For instance, secondary metabolites like glucosinolates and pyrrolizidine alkaloids protect plants against herbivores. Thus, some phloem-limited pathogens target their synthesis (Bekaert et al. 2012; Savage et al. 2016). As a result, altered source-sink relationships due to herbivory or infection lead to changes in the distribution of nutrients, thus influencing the accumulation of defense compounds in phloem sinks (Frost and Hunter 2008; Savage et al. 2016).

When the pathogen is delivered into sieve tubes via insect vectors, the phloem is disrupted. This shows a contrast between uninfected and normal phloem movement.

Normal phloem transport involves a variety of pathways, including the following:

• 1) Active phloem loading The process by which sugar or sucrose is transported from mesophyll cells to sieve elements through intercellular spaces.

• 2) Passive phloem loading Involves the transfer of organic solutes from cell to cell and through plasmodesmata in companion cells to sieve tubes. It also requires a high plasmodesmata density.

• 3) Long-distance transport via pressure flow The phloem transports food over a long distance due to the high osmotic pressure inside the vascular tissue. The phloem uses sieve tube elements with perforated end walls, known as sieve plates, to facilitate the transport of food particles.

• 4) Plasmodesmata connect the cell cytoplasm Food material is transported via plasmodesmata after passing through sieve plate pores.

• 5) Unloading pathways The final stage involves phloem unloading (sucrose/sugar) from source to sink tissue, i.e., from sieve tube elements to roots or other storage cells. However, inside the infected phloem, where phloem-limited pathogens are delivered via insects, plants produce effectors, which increase the production of defense molecules (such as callose, P-protein, and others) and cause sieve element occlusion (SEO). This reduces long-distance transport and causes partial blockage of the sieve plate and plasmodesmata.

The mechanism by which phloem-limited pathogens infect plants and insects

When phytoplasmas are borne by the insect vectors, the extracellular membrane proteins of the phytoplasmas are thought to have a pivotal role in interactions with the insect host. These membrane proteins are transported to the cell surface through the Sec protein secretion system (Kakizawa et al. 2004). Notably, one such membrane protein, the antigenic membrane protein (AMP), is predominantly located on the surface of phytoplasmas (Kakizawa et al. 2009). AMP has been identified as a way to form complexes with host microfilaments. The formation of these AMP-microfilament complexes affects the insect’s ability to transmit phytoplasmas (Hoshi et al. 2007). Furthermore, AMP-microfilament complexes contain the ATP synthase O-subunit of vector insects (Galetto et al. 2011). These studies have contributed to a better understanding of the molecular mechanisms through which specific insect vectors transmit harmful pathogens affecting plants and animals. Another phytoplasma membrane protein, immunodominant membrane protein (IMP), has been found to bind to the plant actin. The absence of movement proteins in phytoplasmas suggests that actin binding facilitates the transit of phytoplasmas through sieve elements and sieve plates, enabling movement within the phloem and ensuring successful colonization of the plant host (Boonrod et al. 2012).

Phloem defense mechanism

Sieve element-specific defense mechanism

Mature sieve elements, vital for cell integrity, protein turnover, and chemical defense, rely on companion cells for support. These sieve elements exhibit unique structural and/or functional relationships and employ mechanical defense mechanisms alongside biochemical methods (Dalio et al. 2021). While a pathogen infecting a single leaf may not threaten the entire plant, specific pathogens that infiltrate neighboring cells and reach the phloem for systemic infection pose a significant danger. Programmed cell death mechanisms, such as those discussed by Dalio et al. (2021), hinder the pathogen’s movement to adjacent cells, preventing its access to the sieve tube system for systemic spread. Sieve elements also implement specific defense strategies, halting the flow and isolating the affected tube section. The rapid increase in sap viscosity and/or reductions in sieve tube or pore radius effectively stop the flow within a few seconds. Two specialized phloem-specific defense mechanisms are:

• 1. Long-term occlusion by the accumulation of callose Callose, a β-1, 3-glucan polymer, acts universally in plants in response to cellular damage (Verma and Hong 2001). CalS7, a callose synthase near plasmodesmata, induces sieve element occlusion during injury (Fig. 2). Extracting sugars from the sieve tube lumen, the enzyme produces callose for the extracellular environment (Verma and Hong 2001). The process of sieve element occlusion through callose deposition is relatively slow (Noll et al. 2022). Studies have also reported that callose deposition rates on the sieve pore cell wall range from 25 to 60 nm/s (Oparka and Turgeon 1999).

• 2. Short-term occlusion by the accumulation of P-protein and forisomes Short-term occlusion in plants can result from the accumulation of P-proteins and forisomes. P-proteins, such as PP1 and PP2 in cucurbits, play a role in repairing phloem tissue wounds by forming a gel-like substance that temporarily blocks sap flow (Golecki et al. 1999). PP2, a phloem lectin protein, binds filaments to the plasma membrane or sieve element endoplasmic reticulum (ER) via glycoproteins. At the same time, PP1 is a filament connected to PP2 by disulfide bridges, with both containing genes associated with sieve element occlusion (SEOR) (Clark et al. 1997). Forisomes in legumes control sap flow in response to stimuli by transforming into a condensed shape, leading to reversible phloem occlusion. This redirection of sap aids in optimizing nutrient distribution and facilitates wound healing. Both P-proteins and forisomes, with their respective genes (SEO-F), contribute to short-term phloem blocking under various conditions, ensuring plant defense and efficient nutrient distribution.

Fig. 2

Callose deposition in sieve pores. Diagrammatic illustration of sieve plates and callose deposition in sieve pores. On the left, there is little or no callose deposition, and the sieve pores are at the maximum aperture; on the right, extracellular callose deposition between the sieve plate cell wall and plasmalemma constricts the functional aperture of the sieve pores

Plant defense mechanisms against phloem-feeding insects and pathogens

Our current knowledge of plant interactions with leaf mesophyll cell-infecting pathogens reveals the activation of two main branches of immunity: pathogen-associated molecular pattern (PAMP) triggered immunity (PTI) and effector-triggered immunity (ETI). PTI is initiated by plasma membrane-localized pattern recognition receptors (PRRs) detecting PAMPs (Couto and Zipfel 2016). Virulent pathogens employ effectors to suppress PTI defense responses (Toruno et al. 2016). A list of reported gene products associated with host interactions in the case of vector-borne plant pathogens has been enlisted in (Table 1). Plants employ ETI mainly through nucleotide-binding leucine-rich repeat (NLR) proteins recognizing pathogen effectors (Jones et al. 2016). Plants respond to insect feeding through a PTI-like mechanism, where herbivore-associated molecular patterns (HAMPs) and damage-associated molecular patterns (DAMPs) trigger immune responses (Howe and Jander 2008). For example, AtPeps induce PTI-like responses in Arabidopsis through PEP-Receptors 1 and 2 (PEPR1 and PEPR2) (Howe & Jander 2008). GroEL homologues from aphid endosymbiont bacteria induce PTI responses (Chaudhary et al. 2014). FlaLas from Ca. Liberibacter asiaticus (CLas) initiates PTI responses, and phytoplasmas may elicit PTI-like reactions through internal PAMPs (Shi et al. 2019) (Fig. 3).

Table 1 Reported gene products associated with host interactions for vector-borne plant pathogens

Fig. 3

A diagram illustrating plant cellular responses to phloem-feeding insects and prokaryotic pathogens. a In resistant plant cells, the membrane-localized PRR Bph3, in collaboration with the coreceptor BAK1, identifies elicitors from insects and pathogens, initiating PTI by recognizing PAMPs and HAMPs. ETI is activated in plants harboring disease-resistant proteins such as Mi-1.2, Bph14, and Bph9, which recognize specific effectors. The interaction between EXO70E1 and Bph6 promotes plant cell wall resistance to brown plant hoppers (BPHs) feeding. The key molecules involved included PAE9, EXOCYST70E1, ACETYLESTERASE 9, SIEVE ELEMENT-LINING CHAPERONE1, and PECTIN SLI1. b In susceptible plant cells lacking disease-resistant proteins and ETI, effectors from insects and pathogens facilitate various phloem cellular processes, promoting pathogen proliferation and insect fecundity. Effectors targeting plant components include SDE1 (Sec-delivered effector 1), SAP11 (secretes AY-WB protein 11), TCPs (TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR), SAP54 (secreted AY-WB protein54), JA (jasmonic acid), MTFs (MADS domain transcription factors), PHYL1 (phytoplasma-secreted protein 1), Mp1 (saliva protein 1 of M. persicae), TENGU (tengu-su inducer), ARF6/8 (AUXIN RESPONSIVE FACTOR 6/8), VPS52 (Vacuolar Protein Sorting Associated Protein 52), Me10 (saliva protein 10 of M. euphorbiae), TFT7 (tomato 14–3–3 isoform 7), NcSP84 (84-kDa calcium-binding effector protein of N. cincticeps), BPH (brown plant hopper, N. lugens), NlSEF1 (an EF-hand calcium-binding motif of N. lugens), Ca2 + (calcium), Bt56 (a whitefly B. tabaci salivary protein), NTH202 (a tobacco)

Phloem-limited plant pathogens

Phloem-restricted pathogens pose a considerable threat due to their elusive presence in plants and the delayed or latent development of symptoms in infected plants. Moreover, these pathogens often engage in complex tri-trophic interactions involving plant hosts and insect vectors. The inability to satisfy Koch’s postulates and the challenge of culturing most phloem-limited bacteria in vitro have led to classifying these bacterial species as Candidatus. Nevertheless, many of them have been identified as causative agents of plant diseases (Fredericks and Relman 1996).

List of phloem-limited plant pathogens

Phloem-limited plant pathogens include Phytoplasma, Spiroplasma, Ca. Liberibacter, Arsenophonus, Serratia, and viruses. Phytoplasma, Ca. Liberibacter, and Arsenophonus are designated as preface Candidatus, which means they are nonculturable, whereas Serratia and Spiroplasma spp. are culturable. Some notable phloem-limited pathogens are listed in Tables 2 and 3.

Table 2 Phloem-limited plant pathogens

Table 3 Walled and wallless phloem-limited bacteria

Phloem-limited vector-borne bacteria

Phloem-limited bacteria enter the phloem via (1) propagation of infected plant material (Caglayan et al. 2019), (2) transmission via seeds (Satta et al. 2019), (3) vascular connections through mechanisms such as parasitic plants like dodder (Cuscuta spp.) (Mikona and Jelkmann 2010; Khanchezar et al. 2012) or root connections (Baric et al. 2008), and (4) transmission via vector insects (Jarausch et al. 2019; Weintraub et al. 2019). This review discusses the crucial entry mechanism of vector-borne phloem-limited bacteria. Vector-borne bacteria exhibit shared characteristics, including an affinity for plant vascular tissues, symbiotic interactions with vectors, and a complete reliance on hosts resulting from genome reduction (Nadarasah and Stavrinides 2011). Various phylogenetic clusters converge in phloem specificity and transmission by hemipterans, and it is suggested that these characteristics have independently evolved multiple times during bacterial evolution (Orlovskis et al. 2015). Most liberibacters and phytoplasmas (classes: Mollicutes) are vector-borne plant pathogens (Bressan 2014; Fagen et al. 2014). In contrast, few species of Spiroplasmas (class: Mollicutes) are plant pathogens. Phloem-limited vector-borne bacteria, such as phytoplasmas and liberibacters, share characteristics such as phloem specialization and intracellular colonization of insect vectors and host plants. These bacteria traverse the gut barrier, circulate in the vector body, and eventually reach the salivary glands for transport (Gasparich 2010; Thebaud et al. 2009). Three major groups of phloem-limited pathogens include phytoplasmas, liberibacters, and spiroplasmas. We will discuss them in the following sections.

Phytoplasmas as phloem-limited plant pathogens

Classification:

Phylum: Firmicutes.

Class: Mollicutes.

Order: Acholeplasmatales.

Family: Acholeplasmataceae.

Genus: Candidatus Phytoplasma.

Phytoplasmas are bacteria that lack cell walls but have a compact genome (680 to 1600 kb) and mostly thrive in isotonic environments within tissues of phloem and insect hemolymph. They exhibit pleomorphism, and their size ranges between 200 and 800 nm (Hogenhout et al. 2008). These microorganisms are implicated in more than 600 plant diseases globally, and their transmission primarily occurs through phloem-feeding insects, particularly leafhoppers and plant hoppers (Bertaccini et al. 2014). Various symptoms are associated with the presence of phytoplasmas, such as stunting, virescence, shorter internodes, enlarged buds, reduced leaf size, witches’ broom, giant calyx, phyllody, vascular discoloration, and floral deformities (Bertaccini et al. 1996; Lee et al. 1997; Bertaccini et al. 2014; Asudi et al. 2021). In certain situations, a plant’s infection can result in its decline and eventual death, leading to a significant loss of yield (Bai et al. 2009; Asudi et al. 2021; Kirdat et al. 2023). Notably, phytoplasmas exhibit significant divergence in geographic distribution and taxonomic categories, including associated subgroups. The 16S rRNA gene sequences of many bacteria have led to their reclassification and renaming (Moore et al. 1997; Woo et al. 2008). The threshold for identifying different phytoplasma species based on 16S rRNA gene sequence identity has been adjusted twice, first from 97.5% to 98.7% and then to 98.65% (Wei and Zhao 2022). The changes include extending the length of the 16S rRNA gene sequence, changing the threshold of 16S rRNA gene identity, proposing a whole-genome ANI criterion, and suggesting the use of an MLSA approach to demarcate new species (Bertaccini et al. 2022). additionally, a Latin double nomenclature for the Ca. Phytoplasma species have been developed, resulting in 48 identified species (Wei et al. 2022).

For instance, phytoplasmas from the 16SrII-V group cause symptoms such as Citrus witches’ broom (Rastegar et al. 2021; Yu et al. 2022). However, different phytoplasma groups in other regions, such as aster yellows (16SrI) (Bai et al. 2006) and floral bud distortion syndrome (FBD) (16SrVI) in Iran (Zamharir et al. 2022), Glycine max witches broom (16SrII) in Australia (Rodrigues et al. 2024), elm yellows (16SrV) in Mauritius (Lee et al. 2004a, b), clover proliferation (16SrVI) in the United States (Lee et al. 2004a, b; Hiruki and Wang 2004), and ‘stolbur’ (16SrXII) in Russia (Quaglino et al. 2013), have been associated with the manifestation of big bud disease in tomatoes (Kumari et al. 2018). Additionally, several studies have identified more different phytoplasma groups. Yu et al. (2022) identified Citrus maxima phytoplasma strains linked to the 16SrII-V group, Palm lethal wilt from the 16SrXXXIX group (Jones et al. 2021), and Florescence dorée from the 16sr V-A (Debonneville et al. 2022). Moreover, phytoplasmas in vegetable crops might be linked to nonspecific symptoms such as fruit deformity, leaf curl, vein clearing, reddening, and yellowing (Pereira et al. 2016). Below are the classifications of phytoplasmas based on RFLP analyses and sequencing of 16SrRNA (Table 4).

Table 4 Classification of phytoplasmas based on RFLP analyses and/or sequencing of 16S rRNA

The dual host life cycle of Phytoplasma

Phytoplasmas follow a dual host life cycle, parasitizing both plants and insects. Phloem-feeding insects, such as leafhoppers, planthoppers, and psyllids, are carriers that transfer phytoplasmas between plants while residing within the phloem. Due to their wide plant host range, phytoplasmas are commonly found in various crops and wild plants where insect vectors feed. When phytoplasma-infected insects feed on plants, the phytoplasmas are initially injected into phloem sieve tubes. Subsequently, they disperse from the phloem tissues of the infected leaf to the main stem, roots, and leaves through the bipolar movement of phloem fluid, occurring both day and night. The survival of phytoplasmas in the natural environment relies on the presence or absence of insect hosts, showing a restricted host range in the case of insects (Weintraub and Beanland 2006). Within insects, phytoplasmas migrate from the gut to the hemocoel and then to the salivary gland, each serving as a barrier to insect transmissibility (Nakajima et al. 2009). The life cycle is illustrated in the figure below (Fig. 4).

Fig. 4

Life cycle of phytoplasmas: The dual host life cycle of phytoplasmas is completed through four steps. Initially, the leafhopper acquires phytoplasmas from the plant phloem (via stylets) and then enters the insect gut (through acquisition feeding), which systemically infects the leafhopper. Then, the phytoplasmas are again introduced into another plant via the leafhopper. Phytoplasmas are transmitted from the insect to the phloem of another plant through inoculation feeding. Subsequently, they multiply and establish a systemic infection, producing various distinctive symptoms

Candidatus Phytoplasma that alters plant morphology

Phytoplasmas, which impact more than 1000 plant species globally, are associated with diseases in agricultural, horticultural, and ornamental plants and weed species (Rao et al. 2017). Ahmed et al. (2022) reported that phytoplasmas associated with sesame phyllody affect sesame plants by reducing plant water content, chlorophyll pigments, and deteriorating oil physio-biochemical properties. Buoso et al. (2019) studied the effects of Candidatus Phytoplasma solani infection on tomato plants, revealing disruptions in the photosynthetic machinery and interference with signals from leaves to roots. Wei et al. (2022) explored the impact of Candidatus Phytoplasma trifolii on potato plants, which causes purple top disease. They observed starch breakdown, chloroplast degradation, and altered gene expression related to leaf senescence and phytohormones. Additionally, they identified specific genes, such as squamosa promoter-binding proteins (Sl-SBP1) and BRANCHED1 (Sl-BRC1a and Sl-BRC1b), associated with axillary bud release and their roles in purple top disease induction.

Liberibacters as phloem-limited plant pathogens

Liberibacters, classified within the phylum Proteobacteria, class Alphaproteobacteria, and order Rhizobiales, are gram-negative bacteria that are nonculturable with a spherical to rod-shaped morphology. They are 1–2 µm in diameter and possess a small genome ranging from 1.2 to 1.5 Mb (Wang et al. 2017a,b). Their multiplication is confined to the plant host or the insect vector, primarily in the phloem, and largely depends on a specific psyllid species for transmission (Casteel et al. 2012). Liberibacters induce various symptoms in infected plants, including stunting, upright growth of new foliage, upward leaf curling, leaf purpling, chlorosis, and shortened and swollen terminal internodes, leading to leaf rosettes, enlarged nodes, axillary branches, aerial tubers, and an abundance of small, irregular fruits (Mishra and Ghanim 2022).

Diseases caused by Liberibacters are currently associated with a limited range of crop families, including Rutaceae, Solanaceae, Umbelliferae, and Rosaceae. The spectrum of plant species affected by Liberibacters is restricted by the host preferences of their psyllid vectors. Citrus greening disease caused by Candidatus Liberibacter asiaticus (Huanglongbing bacteria [HLB)] is a global concern. Ca. L. asiaticus (CLas) is found in Asia and the Americas, Ca. L. africanus in Africa, and Ca. L. americanus in Brazil significantly impact citrus production and associated industries and economies (Wang et al. 2017a, b). Other economically important diseases include Zebra chip disease in potatoes, which is transmitted by Bactericera cockerelli in the Americas and New Zealand; various diseases of carrots and celery vegetables, which B. trigonica transmits in the Mediterranean and the Middle East; and Trioza apicalis in northern Europe, which is caused by distinct genetic variations of Ca. L. solanacearum (CLso) (Wang et al. 2017a, b) (Table 5). The initial natural transmission of Liberibacter in citrus plants was observed through the citrus psylla Trioza erytreae in Africa (McClean et al. 1965) and the Asian citrus psyllid Diaphorina citri in Asia. citri serves as the primary insect vector for CLas in Asia, Brazil, and the United States (Ammar et al. 2016).

Table 5 Diseases associated with Liberibacter, insect vectors, infected host plants, and other biological and molecular parameters

Pathogenicity of Liberibacter

Bacterial phytopathogens in the phloem possess smaller genomes than other phytopathogens (Fujiwara et al. 2018). Liberibacter species rely on their psyllid or plant hosts for both nutritional and essential metabolic functions. In systemic dissemination, they often exploit host proteins for survival and replication (Vyas et al. 2015). Typically, bacterial pathogens deploy virulence factors or effectors to establish themselves in the host. Several CLas effectors, such as Las5315 (Shi et al. 2019), LasAI, LasAII (as autotransporters), and LdtR for osmotic tolerance, have been shown to be secreted in plant cells. Gram-negative bacteria typically employ injectosomes, called type III secretion systems, for delivering effector proteins into host cells. CLas and CLso haplotype D are known to have incomplete type III and type IV secretion systems but possess a type I secretion system (T1SS) along with all the essential components of the Sec machinery (Li et al. 2018). The Sec machinery components, including SecA, SecB, SecE, SecY, and SecD, are conserved across all sequenced CLso haplotypes. Both CLas and CLso also feature flagella-like appendages and flagellar motor proteins, which could function as effector secretion systems (Fujiwara et al. 2018). Exploring protein–protein interactions in host–pathogen relationships, especially in psyllid-Liberibacter interactions, is crucial for understanding the molecular basis of pathogenicity and disease spread.

Citrus–HLB interaction

In addition to structural alterations, plants infected with HLB exhibit diverse metabolic changes and genetic reprogramming. Within the CaLas genome, a protein with potential salicylate hydroxylase activity has been identified, suggesting its ability to convert salicylic acid to catechol (Wang and Trivedi 2013). Salicylic acid, a hormone crucial for plant defense against biotrophic pathogen infections, might be manipulated by CaLas to evade host defenses, as indicated by the suppression of the salicylic acid pathway in HLB-susceptible citrus plants (Xu et al. 2015; Yusuf et al. 2013).

Spiroplasma as a phloem-limited pathogen

Spiroplasmas, which are colonies resembling fried eggs on nutrient-rich media, are helical, cell wall-free bacteria (Harne et al. 2020), lack a peptidoglycan layer, possess a minute genome ranging from 530–2000 kb (Liu et al. 2018; Sasajima and Miyata 2021), culturable and belong to the class Mollicutes, phylum Tenericutes, order Mycoplasmatacae, and family Spiroplasmatacae (Yokomi et al. 2008). With a 1–2 mm diameter, Symptoms of Spiroplasma infection include severe chlorosis, stunted growth, sterility of tassels, poor ear filling, chlorotic stripes on leaves, and smaller fruits (Jiang et al. 2019). However, only a few species, including Spiroplasma citri in citrus (Sagouti et al. 2022), Spiroplasma kunkelii in maize (Whitcomb et al. 1986), and Spiroplasma phoeniceum in aster (Saillard et al. 2008) have been identified as phytopathogens. Spiroplasma, are usually associated with insects but are mainly recognized as plant pathogens, which require an insect host for transmission (Garnier et al. 2001). Spiroplasma species are detected in various insects (Cisak et al. 2015; Kakizawa et al. 2022), some of which cause male-killing phenotypes in fruit flies and other insects. Gasparich (2010) reported that all plant pathogenic spiroplasmas belong to the Citri clade, indicating their phylogenetic relationship. Spiroplasma citri and its vectors, although found on various host plants, are primarily associated with substantial losses in citrus yield (Roistacher et al. 2004). Spiroplasma citri causes citrus stubborn and brittle root disease, impacting sesame, horseradish, and carrot plants (Zarei et al. 2017), has the largest genome of any Mollicutes investigated, with a genome size of roughly 1780 Kbp (Sagouti et al. 2022). Leafhoppers Circulifer tenellus and Circulifer hematoceps spread Spiroplasma citri in North America and the Mediterranean basin, respectively (Renaudin 2006). The Mediterranean nations of Europe, western Asia, and North Africa are strongly affected by S. citri-related infections, with the pathogen not present in South America. Spiroplasma kunkelii is another significant maize crop pathogen transmitted by Dalbulus maidis in the Nearctic and Neotropical regions, indicating tight coevolution with maize (Palomera et al. 2012). Spiroplasma phoenicium, obtained from periwinkle plants exhibiting yellow symptoms in Syria, is experimentally transmitted by the leafhopper Macrosteles fascifrons. However, there is currently no information on its natural vectors in infested areas (Saillard et al. 1987).

Candidatus Liberibacter that leads to patchy distribution in plants

Liberibacters possess a compact genome of approximately 1.2 Mb, and comparative genomics studies have revealed consistent gene organization across the genus, with indications of horizontal gene transfers in the form of integrated prophages (Thompson et al. 2015). Like phytoplasmas, liberibacters lack genes for amino acid, sugar, and nitrogenous base biosynthesis, suggesting their dependence on the host for these metabolic products (Thompson et al. 2015). The genomes of liberibacters encode numerous ABC transporters (Yan et al. 2013). Bernardini et al. (2022) showed that the buildup of Candidatus Liberibacter asiaticus in the phloem hinders the formation of callose and reactive oxygen species (ROS). They noted a decrease in callose and ROS levels in cells with CLas accumulation, allowing the bacteria to persist and move, in contrast to healthy plant SEs with a standard callose layer surrounding the sieve pore and normal physiological ROS levels. This study pinpointed CLas-secreted peroxiredoxin as a suppressor of the plant immune response, influencing callose and ROS.

Arsenophonus as phloem-limited plant pathogen

Arsenophonus are nonflagellated, gram-negative, rod-shaped bacteria with a compact 0.58 MB genome (Bressan 2014). They are nonculturable in nutrient-rich media and belong to the phylum Proteobacteria, class Gammaproteobacteria, order Enterobacteriales, and family Morganellacae. These bacteria commonly cause plant symptoms such as stunting, reddening of leaves, vascular tissue necrosis, chlorosis, and asymmetries in younger leaves (Dittmer et al. 2021). Two notable diseases associated with Arsenophonus bacteria are strawberry marginal chlorosis (caused by Candidatus Phlomobacter fragariae, transmitted by Cixius wagnerii) and reduced sugar beetroot yield (caused by Candidatus Arsenophonus phytopathogenicus, transmitted by the planthopper Pentastiridius leporinusi) (Gatineau et al. 2002).

The Arsenophonus genus encompasses parasitic insects, symbionts, and plant pathogens. Arsenophonus bacteria were identified in 5% of the surveyed arthropod hosts, indicating their versatile associations with both beneficial and parasitic traits (Duron et al. 2008).

Two species within this genus infect sugar beet and strawberry plants, leading to plant diseases (Danet et al. 2003). The discovery of the first pathogenic agent causing marginal chlorosis in strawberries in France at the end of the last century initially led to the identification of Ca. Phlomobacter fragariae. However, subsequent sequencing data suggested that it was an Arsenophonus species (Bressan 2014). Another plant pathogen, Arsenophonus, Ca. Arsenophonus phytopathogenicus, affects sugar beet, causing ‘basses richesses syndrome’, which is characterized by lower sugar content in affected plants (Richard et al. 1995; Zübert and Kube 2021). Onion, as the new host, has been reported to be infected by Ca. Arsenophonus phytopathogenicus (Therhaag et al. 2024a). The pathogen is spread by Pentastiridius leporinus (Hemiptera: Cixiidae), and Therhaag et al. (2024b)confirmed that the vector completes its lifecycle on sugar beets and potatoes when reared under controlled conditions. Ca. Arsenophonus phytopathogenicus was also identified in strawberry, causing marginal chlorosis in Italy (Terlizzi et al. 2007), and Australia but never in North America (Bressan, 2014). Additionally, it was detected in Cixius wagneri vector, which can infect sugar beet plants but not strawberries (Bressan et al. 2009). The epidemiology of these diseases is intricate, as they can also be caused by phytoplasmas transmitted by Hyalesthes obsoletus (Gatineau et al. 2002). Despite being plant pathogens, bacteria resembling Arsenophonus display traits commonly associated with an insect symbiotic lifestyle, including colonization of reproductive tissues, vertical transmission, absence of entomopathogenic activity, high infection rates, and a life cycle closely tied to insect hosts (Bressan et al. 2009). These characteristics suggest the possibility for these bacteria to form new associations with various cixiid species. The intricate relationships with insects and plants, coupled with the adaptability of cixiids to fresh environments and host plants, may contribute to the growing incidence of emerging Arsenophonus-related diseases.

Serratia as phloem-limited plant pathogens

Serratia are gram-negative, walled, rod-shaped, culturable bacteria with cell walls. The yellow vine disease of pumpkin and squash, characterized by phloem discoloration, wilting, and foliage yellowing, is caused by Serratia marcescens, a phloem-limited pathogen (Rascoe et al. 2003). Recent studies have shown that Serratia marcescens creates a biofilm along the sidewalls of plant phloem tissues after entering its host. This biofilm hinders the movement of water and nutrients, leading to wilting and eventual death of the plant (Labbate et al. 2007). A genetic analysis aimed at identifying genes responsible for regulating biofilm formation in S. marcescens discovered the association of fimbrial genes, along with an oxyR homolog, which serves as a well-preserved bacterial transcription factor crucial for responding to oxidative stress (Shanks et al. 2007). The squash bug Anasa tristis, commonly distributed across the United States and from Canada to Central America, serves as a vector for Serratia marcescens (Alston and Barnhill 2008). With their piercing-sucking mouthparts, squash bugs penetrate intracellularly into plant tissues, target vascular bundles, and feed on the plant host. The extent and size of the bugs and the duration each bug spends on the plant and at the feeding site are linked to the observable signs and severity of feeding damage to squash plants. Prolonged feeding on the fruit results in fruit collapse, while leaf feeding induces isolated necrotic lesions (Neal 1993).

Phloem-limited viruses

Viruses, as obligate intracellular parasites, replicate through the phloem, causing systemic infections in host plants. Plant viruses possess either DNA or RNA genomes, can replicate, and can encode proteins within infected cells. Using the vasculature for systemic infection and plasmodesmata (PD) for cell-to-cell movement, viruses employ movement proteins (MPs) and coat proteins (CPs) to facilitate their spread within the plant (Hipper et al. 2013; Kumar et al. 2020). MPs play diverse roles, including modifying PD to facilitate the movement of viral genomes and proteins between cells. Viruses can move as encapsidated particles or ribonucleoprotein complexes, and many viruses exhibit various forms (Solovyev et al. 2012). Cell-to-cell movement through plasmodesmata (PD) allows the virus to spread from the initial infection site to neighboring cells and eventually access the vasculature for long-distance movement (Heinlein 2015; Meena et al. 2017). The long-distance movement in the phloem follows the conventional source-to-sink flow of sugars, enabling the bidirectional transportation of viruses from the entry point. Virus loading occurs in all vein types, whereas unloading is limited to the major sink tissue veins (Hipper et al. 2013). In plants, the Closteroviridae, Luteoviridae, Reoviridae, and Geminividae family members are predominantly phloem-limited viruses. Phloem-limited viruses induce cellular hyperplasia, leading to tumors or vein swelling, altering the cellular arrangement of sieve elements (SEs). Aphids, whiteflies, and, to a lesser extent, plant hoppers and leafhoppers also transmit phloem-limited viruses. Shen et al. (2016) explored the induction of neoplastic phloem tissues by a phloem-limited fijivirus, specifically rice black-streaked dwarf virus (RBSDV), in maize plants. Molecular and structural analyses revealed elevated transcript levels of the maize cdc2 gene, which regulates the cell cycle in tumor tissues. RBSDV was restricted to the phloem and tumor regions, thus multiplying in the tumor tissue. RBSDV infection induces the formation of tumors, creating a conducive environment for the virus to propagate within the host plant. The cdc2 gene and viral proteins (structural and nonstructural) play crucial roles in neoplastic tissue formation and are linked to alterations in physiological and metabolic processes induced by RBSDV. Wu et al. (2022) reported that a modified calcium-binding protein (CBP), which is a leaf hopper saliva protein, facilitates the horizontal transmission of rice gall dwarf virus (RGDV) into rice phloem tissues. Similarly, in a more recent study, Wang et al. (2024) found that the rice leaf hopper Nephotettix cincticeps efficiently transmits rice dwarf virus (RDV) in the phloem tissues through salivary vittelogenin, which contains the RDV-packaging exosomes, thus facilitating efficient virus transmission. A list of phloem-limited plant viruses is listed below (Table 6).

Table 6 List of phloem-limited plant viruses

Virus-induced reprogramming of phloem

Viruses typically invade plants through mechanical damage or insect vectors. Plant viruses commonly possess small genomes, depending heavily on their hosts for various functions. Infected host cells play a crucial role in supporting the replication and transcription of viral genomes and the translation of viral proteins. Local infection spreads from cell to cell through symplastic movement via plasmodesmata, a process facilitated by movement proteins (MPs) (Folimonova and Tilsner 2018). Viruses typically establish systemic infections upon entering the vasculature by following the source-to-sink movement of nutrients through the phloem. This requires viruses to traverse various cell types, including the bundle sheath, vascular parenchyma, companion cells, and sieve elements. Movement through the vasculature can occur as virions with coat proteins enveloping the viral genome or as viral replication complexes. Below are a few examples of virus-host interactions impacting systemic phloem movement. One example involves the tobacco mosaic virus (TMV) and auxin/indole acetic acid (IAA) proteins. Auxin/IAA proteins, which negatively regulate the auxin response in plants, interact with the helicase domain of the TMV 126/183-kDa protein. This disrupts the nuclear localization of IAA26 in companion cells, which is crucial for efficient vascular movement. A mutant of TMV, known as TMV-V1087I, featuring a modified helicase domain that disrupts the interaction with IAA26, demonstrated delayed phloem loading and systemic movement in comparison to wild-type TMV (Collum et al. 2016). Another interaction involves a cell wall-associated protein, cadmium (Cd) ion–induced glycine-rich protein (cdiGRP), which inhibits systemic phloem transport of turnip vein-clearing virus (TVCV) when overexpressed (Ueki and Citovsky 2002). Overaccumulation of cdiGRP in plants results in increased callose levels in the phloem and associated plasmodesmata, thus restricting virus movement (Iglesias and Meins 2000; Ueki and Citovsky 2005). Certain viral family members, such as Geminiviridae and Reoviridae, induce tumors derived from the phloem, such as RBSDV and southern rice black-streaked dwarf virus (SRBSDV). During rice black-streaked dwarf virus (RBSDV) infection, the increased proliferation of phloem cells triggers the activation of the cdc2 gene, which is associated with cell cycle regulation (Shen et al. 2016). These activated cells serve as locations for active virus replication, enhancing the interfaces of sieve elements to facilitate the phloem movement of the virus. Consequently, reprogramming the phloem cell cycle contributes to virus replication and movement. In a recent study, Khalilzadeh et al. (2024) reported that ‘stem-pitting’ symptoms produced by citrus tristeza virus are correlated with increased phloem occlusions. They found that, when the stem-pitting symptoms were more severe, there was a constant increase in callose deposition and phloem proteins, thus exacerbating the disease symptoms.

Management of phloem-limited plant pathogens

Various strategies have been proposed for managing phloem-associated diseases and their insect vectors, yet an optimal control method still needs to be identified (Firrao et al. 2007). Pesticide-based control of insect vectors is an effective measure to curb the spread of diseases in crops caused by phloem-limited pathogens. However, complete eradication is challenging even with high doses of insecticides. Another approach involves treating diseased plants with tetracycline, but this is not a sustainable long-term solution, and plants remain susceptible to reinfection upon exposure to insect vectors. Additionally, antibiotic use is constrained by cost and regulatory restrictions in many countries (Raychaudhuri et al. 1970). Despite the temporary relief of symptoms, tetracycline could not eliminate leaf diseases in brinjal, and the treated cultivars showed no signs of flowering or fruiting (Upadhyay 2016). Applying gibberellic acid to infected brinjal plants led to symptom recovery, with greater improvement observed when combined with ledermycin. Assessing the effectiveness of various antibiotics on phytoplasma-infected brinjal cultivars, such as biophenicol, chloramphenicol, enteromycelin, lycercelin, paraxin, roscillin, campicillin, oxytetracycline, chlorotetracycline, and rose/clove/eucalyptus oils, revealed limited efficacy in disease control (Chakrabarti and Choudhury 1975).

Another potential avenue involves the use of host defense inducers. Sanchez-Rojo et al. (2011) demonstrated that salicylic acid significantly alleviated symptoms in purple-top disease-infected potato plants. Pretreating tomato plants with salicylic acid prior to phytoplasma inoculation led to a considerable reduction in purple top disease symptoms, accompanied by an increase in the expression of defense-related genes (Wu et al. 2012). The development of cultivars resistant to phytoplasmas or their insect vectors represents a sustainable, long-term approach. Although modest progress has been made, some wild relatives of brinjal, such as Solanum integrifolium and S. gilo, have been identified as cultivars resistant to little leaf disease (Chakrabarti and Choudhury 1975). Additional management methods for phytoplasma-associated diseases include removing infected plants, adjusting sowing dates, using clean propagation materials, rotating with nonhost crops, weed removal, and vector control methods. Managing phytoplasmas requires an integrated approach that combines cultural, physical, biological, and chemical strategies, as they depend on a living host for survival, making chemical management strategies uneconomical (Firrao et al. 2007). An integrated approach for managing phloem-limited pathogens is described below.

Conclusions and future perspectives

Phloem-limited pathogens exert substantial physiological effects on the phloem, triggering callose deposition on sieve plates, modifying phloem loading capacity, impacting the composition of mobile proteins and small molecules, and ultimately resulting in necrosis. Despite being confined to the phloem, these pathogens utilize effector proteins to manipulate host immune signaling and induce disease. Effector proteins, which are small enough to unload from the phloem, move to other tissues, modulating host expression and enhancing virulence. Thus, developing cultivars resistant to these pathogens or their vectors, potentially from wild relatives, represents a long-term approach. Additionally, managing infected plants, using clean propagation materials, and managing vectors contribute to disease containment. Given the complexity of phloem-limited pathogen interactions, an integrated approach is required to manage these pathogens by combining cultural, physical, biological, resistance, and chemical strategies. A better understanding of phloem biology and developing flexible management systems for each phloem-limited pathogen category will be crucial for effective disease management in the modern era.