Since the emergence of plant-pathogen interactions, a relentless co-evolutionary arms race has unfolded between pathogens and their plant hosts (Zhang et al., 2022). Plant pathogens represent a diverse collection of organisms that possess the capability to infect their hosts. Pathogens, ranging from fungi, bacteria, and nematodes to parasitic plants, exploit host resources for survival and reproduction. Pathogens that can infect seemingly healthy plants are known as primary pathogens. Secondary pathogens opportunistically colonize tissues weakened by prior infection or stress (Termorshuizen, 2017). Pathogenic microorganisms extract nutrients from host cells for survival and reproduction, whereas host plants utilize numerous defense mechanisms to restrict pathogen proliferation (Ngou et al., 2022). Among these adversaries, fungal pathogens constitute the predominant category of plant pathogens, whereas other significant plant pathogens encompass bacteria, protists, chromists, nematodes, and some plants (Termorshuizen, 2017). Currently, about 10,000 fungal species are recognized as pathogens of plants (Agrios, 2005; Koeck et al., 2011). Fungi have endophytic, parasitic, saprotrophic or mutualistic relationships with plants (Jayawardena et al., 2018; Zeilinger et al., 2016). Fungal plant pathogens potentially incite devastating ecological and economic damage to agriculture and forestry, and can also cause severe damage to natural ecosystems (Fisher et al., 2012; Hyde et al., 2018; Jayawardena et al., 2021). The development of plant disease is a result of the tripartite interaction of host, pathogen and environment (Jayawardena et al., 2021). Fungal plant pathogens establish compatibility with the host through various ways (Marcato et al., 2017). Fungi can (i) evade detection by the plant monitoring system (Pel and Pieterse, 2013), (ii) release effector molecules capable of suppressing or manipulating the host defense mechanisms (Doehlemann and Hemetsberger, 2013; Dou and Zhou, 2012), (iii) counteract the antifungal chemicals generated by their host plants (Osbourn, 1999). All these processes may be employed concurrently or sequentially throughout the plant-fungus interaction, together facilitating a successful infection (Marcato et al., 2017). The outcome of these interactions hinges a delicate balance influenced by the host, pathogen, and environmental conditions, setting the stage for a complex molecular arms race.

To counter pathogen attacks, plants are capable of identifying microbes through pattern recognition receptors (PRRs) in the host cells. Upon recognizing the adversary, these receptors initiate effective immune responses in the invaded tissue (Pel and Pieterse, 2013). Microbial recognition is facilitated by conserved structures known as microbe-associated molecular patterns (MAMPs) (Pel and Pieterse, 2013). Furthermore, host-derived signals produced during pathogen infection or mechanical injury, known as damage-associated molecular patterns (DAMPs), represent an additional mechanism by which the host detects pathogen invasion (D'Ovidio et al., 2004; Dou and Zhou, 2012; Huffaker et al., 2006). Receptors that detect pathogen associated molecular patterns (PAMPs) and damage-associated molecular patterns (DAMPs) are commonly referred to as pattern recognition receptors (PRRs). In contrast to animal pattern recognition receptors (PRRs), which include both plasma membrane-localized Toll-like receptors (TLRs) and cytoplasmic NOD-like receptors (NLRs), plant PRRs are only composed of plasma membrane-localized receptor-like kinases or receptor-like proteins (Monaghan and Zipfel, 2012). Plants possess a substantial quantity of NLR proteins; yet, they seemingly do not identify PAMPs or DAMPs (Dou and Zhou, 2012). In contrast, NLRs solely identify intracellular pathogen effector proteins and initiate immune responses with high specificity. However, pathogens continually adapt, secreting effector proteins that manipulate host cells to take their advantage (Tsuda and Katagiri, 2010). These effectors can disrupt host metabolism, suppress immune responses, or alter gene expression, depending on whether they act in apoplast (extracellular) or cytoplasm (intracellular).

Effector proteins are secreted by pathogens to manipulate the host to their advantage (Sperschneider et al., 2015). Effectors are molecules that modify the structure and function of host cells, thereby facilitating infection (virulence factors or toxins) and/or initiating defense responses (avirulence factors: Avr). These proteins can be divided into two types according to their target sites in the host plant (Selin et al., 2016). Apoplastic effectors are secreted into the plant apoplast, where extracellular effectors engage with extracellular targets including surface receptors, while cytoplasmic effectors are translocated into the plant cell (Selin et al., 2016). Efficient transport of effectors to the plant is essential for the infection process, irrespective of the effector type. Pathogenic fungi have evolved unique lifestyles and consequently created various effector delivery systems during infection (Selin et al., 2016). The effector proteins are able to alter protein transcription or modify the metabolic pathways of the host cell thereby enhancing pathogenicity (Salehzadeh and Dehghanpour Farashah, 2019). A key unresolved question in plant pathology is how eukaryotic pathogens, particularly (fungi), manipulate host processes to promote infection, highlighting the need for deeper mechanistic insights into these interactions (Whisson et al., 2007).

Many researchers have examined the ways in which host-pathogen relationships are impacted by the evolutionary conflict between plants and diseases (Langin et al., 2020). Effectors are necessary for plant disease development because they are key players in the induction of susceptibility. Plants build immunological receptors by natural selection with pathogens to detect particular effectors that activate defense responses. The outcome between diseases depends on the continuous interaction between effectors and the host immune system (Lovelace et al., 2023). Understanding the molecular basis of this interaction provides essential knowledge to determine viral disease principles which will guide resistance development. The characterization of particular pathogen-driven effectors has been the major target of scientific research during multiple years (Lovelace et al., 2023). The use of genetic methods has discovered pathogenicity or virulence factors through which scientists gained better insights into the functioning of host–pathogen relationships. Plants have evolved resistance (R) gene-encoding proteins that combat pathogen effectors to initiate immune defense known as effector-triggered immunity ETI ( Figure 1 ) (Wang et al., 2015). The primary defense mechanism of plants involves pattern recognition receptors (PRRs) that detect pathogen-associated molecular patterns (PAMPs) to initiate pattern-triggered immunity (PTI) responses, thereby preventing pathogen proliferation (Zhang et al., 2022).

Plant pathogens receive their classifications through analysis of their nutritional behaviors (Abera Gebrie, 2016). Plant fungal infections pose severe dangers to both the worldwide food supply system and environment stability. Plant pathogenic fungi are classed as biotrophs, hemi-biotrophs, or necrotrophs according to their lifestyle (Wang et al., 2014). Growth patterns of biotrophic pathogens involve obtaining nutrients from living host cells and tissues through low-level excretion of cell wall-degrading enzymes and effectors to suppress host immune responses (Dean et al., 2012). Necrotrophic pathogens pursue growth on the dead host tissues by degrading them before or during colonization period; to provoke cell necrosis, they frequently excrete phytotoxic secondary metabolites (SMs) and peptides, and generate reactive oxygen species (ROS) (Horbach et al., 2011). Hemi-biotrophic pathogens exhibit a biotrophic phase initially during infection, transitioning to a necrotrophic phase thereafter; these pathogens generate toxins exclusively at the final stages to eliminate host cells and complete their life cycle on necrotic tissues (Horbach et al., 2011; Wang et al., 2014).

The main differentiating factor between hemibiotrophs and necrotrophs rests on their ability to form haustoria or haustoria-like structures from intracellular hyphae which makes hemibiotrophs similar to biotrophic pathogens ( Table 2 ). During the pathogenic process hemibiotrophs produce a bulged intracellular hypha first which is enclosed by the host plasma membrane then transforms into a flatter intracellular hypha resulting in necrosis [66]. Necrotrophic fungi show extracellular hyphal growth that does not include intracellular multiplication while they gain access through stomatal apertures or hydathodes. Both hemibiotrophic and necrotrophic lifestyles encompass an early biotrophic phase succeeded by necrosis. The duration of the biotrophic phase exhibits variability among hemibiotrophs and may exhibit even greater variability in necrotrophs. This duration can be influenced by numerous external environmental factors. These necrotrophic pathogens can create either appressoria or appressoria-like structures (ALS) while some also produce bulbous hyphae that resemble structures observed in hemibiotrophic pathogens [67].

Apoplastic: E. Münch initially employed the term “apoplast” in his 1930 German scientific publication (Farvardin et al., 2020). The two fundamental elements of apoplast include intercellular spaces that comprise gas and water between cell membranes and the fibrils and micelles containing substances within cell walls and xylem structures. Plants possess the rhizoplane and cuticle areas and these regions together form an extension of the apoplast system ( Figure 5 ) (Farvardin et al., 2020). Filamentous microorganisms establish relationships with plants that vary from mutualistic (fungi) to pathogenic (fungi and oomycetes).The result of these interactions, whether compatibility or incompatibility, is frequently established in the apoplast, where the initial contact between microbial and plant cells occurs (Doehlemann and Hemetsberger, 2013; Rocafort et al., 2020). The apoplast constitutes a hostile environment, characterized by the constitutive production of proteases, protease inhibitors, secondary metabolites, and hydrolytic enzymes by plants to limit fungal and oomycete growth (Rocafort et al., 2020).Cell surface-localized immune receptors monitor the apoplast and recognize invasion patterns, activating the plant immune system (Cook et al., 2015; van der Burgh and Joosten, 2019). This activation inhibits or ceases fungal and oomycete proliferation by generating supplementary defensive chemicals and reactive oxygen species (ROS), with callose and lignin deposition, and, in certain instances, the hypersensitive response (HR). The apoplast is not a sterile environment; it contains various bacteria that struggle for space and nutrition (Rovenich et al., 2014; Snelders et al., 2018). These microorganisms utilize hydrolytic enzymes, antibiotics, toxins, and volatile compounds that can further inhibit the growth of fungi and oomycetes (Carrión et al., 2019).

Apoplastic effectors are released into the interfacial area between pathogen and plant cells, where “chemical warfare” transpires (Doehlemann and Hemetsberger, 2013; Harris et al., 2023). These effectors comprise protease inhibitors (Rooney et al., 2005) detoxification of secondary metabolites (Okmen et al., 2013; Singh et al., 2023), chitinase- binding effectors (van den Burg et al., 2006), and peroxidase inhibitors (Hemetsberger et al., 2012).These effectors concentrate on mitigating the pathogen’s surroundings and evading detection (Harris et al., 2023).

Cytoplasmic effector: Effectors are classified as cytoplasmic when they are translocated into the host cell to target host cellular processes (Dulal and Wilson, 2024). Cytoplasmic effectors are secreted proteins that facilitate fungal disease by targeting plant organelles and altering host defenses (Li et al., 2024; Sperschneider and Dodds, 2022; Zeilinger et al., 2016). They function within the host’s intracellular space, affecting numerous cellular processes and generally have a greater ratio of positively charged amino acids (Li et al., 2024; Sperschneider and Dodds, 2022; Zeilinger et al., 2016). ​ Fungal pathogens that utilize these effectors can severely impact forests by causing tree mortality, diminishing plant species diversity, and facilitating infection (Bi et al., 2021). Cytoplasmic effectors typically facilitate fungal disease by targeting plant organelles to alter various cellular processes within the host (Bi et al., 2021; Li et al., 2024; Sperschneider and Dodds, 2022). Cytoplasmic effectors are essential in fungal pathogenesis as they inhibit plant defense mechanisms and modify host cell structure and function. They enable pathogen colonization and alter host defenses to enhance infection ( Figure 6 ). For example, The BcCrh1 protein from Botrytis cinerea serves as a cytoplasmic effector and a trigger of plant defense mechanisms. Numerous effector-encoding genes are organized in clusters and are variably activated when various plant tissues are colonized (Bi et al., 2021; Li et al., 2024; Sperschneider and Dodds, 2022).

Effectors represent small molecules released by microbes that transform cell structures of their hosts to make pathogen-host communication possible (Fabro, 2022; Langin et al., 2020). The molecules produce physical along with physiological alterations within the target species while also influencing the producing microorganisms in select cases (Cai et al., 2023; Figueroa et al., 2021; He et al., 2020). Most effectors are proteins (Carreon-Anguiano et al., 2020; Sperschneider and Dodds, 2022), though some are secondary metabolites (Rangel and Bolton, 2022), or small RNAs (Yamankurt et al., 2020). The absence of conservation across different organisms among known effectors led to the creation of in silico predictive identification methods which use broader structural criteria. At least four screening criteria exist for potential phytopathogen effectors where (a) amino acid count remains lower than 400 amino acids, (b) signal peptides facilitate the protein’s escape from cellular secretion by phytopathogen cells (Carreon-Anguiano et al., 2020; Sperschneider et al., 2018), c) the amount of cysteine amino acid reflects effector enrichment and; and (d) transmembrane domains must be absent in candidates (Carreon-Anguiano et al., 2020). The identification process for such effectors becomes more streamlined because their specific expression patterns become evident when the phytopathogen interacts with its host (Tao et al., 2020; Toruno et al., 2016). The amino acid sequences of protein effectors in oomycetes often show recurring small sequence patterns named motifs which include RxLR, CHXC or LFLAK (Fabro, 2022). Some microbial effectors have their genetic locations on dispensable chromosomes which may be missing from certain microbial strains together with regions of the chromosome that contain repetitions and lack high gene density (Peng et al., 2019). A study analyzed the location of virulence-related genes in fungus Pseudocercospora fijiensis which revealed most genes existed in “dispensable” genomic regions while transcriptome analysis showed these genes become active when P. fijiensis infects banana (Musa acuminata) (Noar and Daub, 2016), the P. fijiensis effectors were predicted through EffHunter software application using effector characteristics (Carreon-Anguiano et al., 2020), The analysis discovered 136 effectors which reside within dispensable genomic regions as well as genomic areas common to all strains designated the “core” genome (Todd et al., 2023). The evolution of effector protein genes encounters high selection pressure because of which their mutation rates surpass other gene families (Todd et al., 2023). Shared effectors between strains of the same species commonly develop polymorphisms because of host adaptation together with virulence expression (Kanja and Hammond-Kosack, 2020). Research shows that effectors exist in both closely related microbial populations as well as only in distantly related microbial groups (Todd et al., 2023). Orthologous proteins show minimal sequence similarity because they share functional identities with other proteins throughout different animal groups although their sequences have numerous variations which originated from their common ancestral origins (Todd et al., 2023). Avr4 from P.fijiensis shares only 50.5% sequence similarity with its corresponding ortholog in Cladosporium fulvum while these species both belong to the Dothidiomycetes fungal class (Todd et al., 2023). Latest omics studies detect effector protein domains and motifs even though most effectors display minimal sequence identity between family members (Todd et al., 2023). Different recognized domains exist with LysM and ceratoplatanin and RNAase while necrosis-inducing protein domains (NPP1 or NEP) and CFEM also belong to this classification (Carreon-Anguiano et al., 2022; Outram et al., 2021; Zhou and Zhang, 2020). Modern research demonstrates how microorganisms carry hundreds of effectors (Carreon-Anguiano et al., 2020; Noar and Daub, 2016; Sperschneider et al., 2018), which work at different times (Noar and Daub, 2016; Toruno et al., 2016). Plant effectors function to interrupt essential signalling procedures and phytoregulator production as well as plant defensive systems (Fabro, 2022; Han and Kahmann, 2019; Plett et al., 2020).

All plant-microbe interactions depend on effectors since these molecules help phytopathogens cause damage while promoting beneficial relationships with helpful microorganisms including mycorrhizae (Plett et al., 2020; Todd et al., 2023), and new studies investigate their function during microbe-microbe interactions (Snelders et al., 2021, 2020). The infection approach of phytopathogens determines the functioning of their effectors because biotrophic pathogens need living hosts to succeed but necrotrophic pathogens obtain nutrients by utilizing dead tissue. The infection pattern of hemibiotrophic phytopathogens spans two nutrient acquisition phases starting with survival in live tissue then continuing in deceased tissue cells (Todd et al., 2023). Biotrophic organism effectors block the host immune response while necrotrophic effectors generate excessive non-localized defenses that eventually destroy their host cells (Todd et al., 2023). The effectors of hemibiotrophic phytopathogens work to delay cellular demise at first but they launch effectors in the necrotrophic stage that advance host mortality (Castillo-Sanmiguel et al., 2022; Jones and Dangl, 2006; Thordal-Christensen, 2020; Todd et al., 2022b). For example, the effector BcNEP1 exhibits high levels of expression during the initial stages of Botrytis cinerea infection but the effectors BcSSP2 and BcNEP2 become active only after the early phase (Zhu et al., 2022). In the case of Colletotrichum spp. hemibiotrophic fungi effectors have specific functions during the biotrophic stage but induce death of host cells to move into necrotrophic development (Ono et al., 2020; Tsushima et al., 2021). Until the last decade researchers understood all effectors to be extracellular which led to their inclusion in the definition of effectors but the most extensively studied ones are apoplastic (extracellular) (Carreon-Anguiano et al., 2020). The field of effectoromics now recognizes intracellular effectors which function either inside the cytoplasm or the organelles as prominent new discoveries (Sperschneider and Dodds, 2022; Tariqjaveed et al., 2021; Todd et al., 2022a). Apoplastic effectors include small protein molecules that work through enzymatic degradation of cell walls combined with exploits that loosen these structures and additional activities such as protease inhibitory functions and inability for plant recognition of pathogenic organisms (Fabro, 2022; He et al., 2020; Langin et al., 2020). The biological functions together with the cellular locations of intracellular effectors within host cells demonstrate variability because most targets are essential defense proteins in plant immunity (Thordal-Christensen, 2020). Several targets encompass proteases and components from the ubiquitin and proteasome systems with addition to transcription-related proteins and receptors and biosynthetic machineries and phytoregulator-regulated signaling pathways that control defense responses in plants (Fabro, 2022; Han and Kahmann, 2019).

Microorganisms use their effector proteins to manipulate jasmonate (JA) and salicylate (SA) and ethylene (ET) phytoregulator production processes for their own benefit (Alhoraibi et al., 2019; Chini et al., 2018; Langin et al., 2020). For example, the fungal effector Cmu from Erysiphe quercicola functions as a chorismate mutase to deteriorate host salicylic acid synthesis (He et al., 2021). The VdIsc1 effector produced by Verticillium dahliae displays isochorismatase activity to block salicylic acid synthesis just like the fungus (Zhu et al., 2017). Through its function as RipAB Ralstonia solanacearum blocks the signaling mechanisms controlled by salicylic acid (Qi et al., 2022). Effectors produced by microorganisms serve two functions by maximizing phytoregulator synthesis or synthesizing close analogues of phytoregulators (Todd et al., 2023). For example, Lasiodiplodia mediterranea produces lasiojasmonate A (LasA) which acts as an analogue of jasmonic acid during necrotrophic infection of host plants. The pathogen uses LasA to produce the strong jasmonic acid regulator jasmonyl-isoleucine (JA-Ile) which boosts signaling mechanisms leading to cell death during necrotrophic development (Chini et al., 2018).

Forest ecosystems rely on fungal pathogens because these organisms facilitate natural decomposition yet pose an important threat as they cause plant ecosystem damage and biodiversity decline through invasions. Multiple effector systems of pathogens operate to alter plant defensive mechanisms during infection so they can spread infection more effectively while supplementing nutrient requirements. The microbial effectors launch attacks on plant protective defenses to initiate an extended evolutionary conflict between pathogen agents and plant organisms.

Fungal groups establish different life paths that assign them to biotrophic, necrotrophic and hemibiotrophic pathways in their interactions with host organisms. The living conditions of biotrophic fungi enable them to occupy plant cells yet necrotrophic fungi survive through cellular death of their hosts. Pathogens employ multiple strategies for activating plant defense mechanisms which proves that plant-pathogen systems function as well-adapted complex systems.

The virulence of pathogens increases because effectors both alter plant metabolic operations and signaling pathways and immune response functions and directly regulate phytohormones to block defense mechanisms. Host-specific behavior together with pathogen survival develops through effectors that adapt because of high mutation rates and evolutionary pressures. Studies of genetics show that effector genes find shelter within mobile genomic zones because these mobile areas produce specialized and varied features. Sustainable plant disease control methods need extensive identification of molecular plant-pathogen interactions to protect forest ecosystems. Research efforts need advancement regarding fungal effectors and plant immune responses and cytoplast and apoplast microbial communities because this information supports sustainable forest management and plant pathology research.