Table 1. Summary of phytohormone roles in defense and intercellular communication
| Hormone | Affecta | Transport mode | Defense roleb | Role against pathogen | References |
| Salicylic acid | Yes | Apoplast | ETI, SAR | Biotrophs, necrotrophs | Al-Daoude et al. 2019; Lim et al. 2016; Mittag and Strader 2020; Wang et al. 2013; Wildermuth et al. 2001 |
| Jasmonates | Yes | Symplast, apoplast | ETS | Necrotrophs, biotrophs, nematodes | Antico et al. 2012; Farmer et al. 2014; Li et al. 2017; Lim et al. 2016; Nakano and Mukaihara 2019; Yimer et al. 2018 |
| Auxin | Yes | Symplast, apoplast | PTI, ETI | Biotrophs, necrotrophs | Han et al. 2014; Kazan and Manners 2009; Qi et al. 2012; Robert and Friml 2009 |
| Abscisic acid | Yes | Symplast, apoplast | ETI | Necrotrophs | Benitez-Alfonso 2019; Mine et al. 2017; Tylewicz et al. 2018 |
| Ethylene | − | Free diffusion, apoplast | ETI | Biotrophs, necrotrophs | Guan et al. 2015; Yang et al. 2017 |
| Gibberellins | Yes | Symplast | − | Bacteria, necrotrophs | Kwiatkowska 1991; Navarro et al. 2008 |
| Cytokinins | Yes | Symplast | PTI, ETI | Biotrophs, necrotrophs | Bishopp et al. 2011; Naseem et al. 2015 |
| a | Whether or not it affects plasmodesmata permeability. |
| b | ETI = effector-triggered immunity, ETS = effector-triggered susceptibility, PTI = pathogen-associated molecular pattern-triggered immunity, and SAR = systemic acquired resistance. |
HOW PATHOGENS EXPLOIT HOSTS’ CELL-TO-CELL CONNECTION
Pathogens enter a host cell through a natural opening (e.g., stomata), wound, or tissue damage. The mode for infection varies from pathogen to pathogen (Fig. 2). For instance, nematodes and bacteria commonly use the apoplastic passage for colonization, whereas viruses and fungi exploit the symplastic passage for cell-to-cell spread (Kankanala et al. 2007).
Nematodes.
Sedentary endoparasite cyst nematodes and root-knot nematodes locate the host and penetrate through the roots in second-stage juveniles. The root-knot nematodes migrate through intercellular spaces in the cortex, reaching the xylem parenchyma and inducing the formation of the feeding structure of giant cells (Jones 1981; Wyss and Grundler 1992). Cyst nematodes with a more robust stylet migrate through penetrating the cortex and endodermis, reaching the vascular cylinder and establishing the syncytia (von Mende 1997). Giant cells are symplastically isolated and obtain nutrition through a transport-mediated process, whereas the syncytia are connected to the phloem by the PD (Hoth et al. 2008). Nematodes initiate the de novo formation of unloading the phloem and secondary PD biogenesis between the sieve elements that connect to syncytia to ensure macromolecular trafficking (Hofmann and Grundler 2006; Hoth et al. 2008). They also release effector repertoires that may suppress the host defense response, alter hormone signaling, and modify or degrade the cell wall to ensure a constant nutrient supply and further establish a systemic infection (Hewezi and Baum 2017).
Viruses.
Plant viruses are biotrophic obligate pathogens known to spread by hijacking trafficking through the PD. They encode the movement protein (MP) to transport their genomes across cells. Different MPs use different mechanisms for virus transport. Some viruses, such as the tobacco mosaic virus, require a single MP and not the coat protein (CP) for intercellular movement. Nontubule-forming viruses associate with PD via MP to facilitate movement by increasing the size exclusion limit of the PD (Schoelz et al. 2011). In contrast, the cucumber mosaic virus and Alfalfa mosaic virus require a single MP and CP for cell-to-cell movement (Kaplan et al. 1998). Some viruses such as the papaya mosaic virus and potato virus X have specialized open reading frames, known as triple gene blocks, which are required for movement through the PD and phloem (Morozov and Solovyev 2003).
Intercellular movement of members of genus Potyvirus, the largest group of RNA viruses, requires diverse host components and at least three viral proteins: CI, P3N-PIPO, and CP. Moreover, P3N-PIPO is the MP that targets CI to PD and forms a conical structure through which the virion or viral RNA/CP complex enters the adjacent cell (Wang 2021). Some viruses extensively modify the PD. For instance, MP in the cowpea mosaic virus forms growing tubules and replaces the appressed ER, leaving a PM-lined tunnel through which the virus can travel (van Lent et al. 1991).
Colocalization and interaction studies have demonstrated that the MP from the grapevine fanleaf virus (another tubule-forming virus) colocalizes and interacts with PDLPs. Furthermore, viral tubule and cell-to-cell spread were compromised in the PDLP triple mutant pdlp1/pdlp2/pdlp3. Viroids (small, single-stranded, circular RNAs) can also move through the PD and phloem and infect plants (Adkar-Purushothama and Perreault 2020). Some viruses (e.g., potato leafroll virus) are limited to the phloem. They may move as a virion with the CP, independent of the MP (Taliansky et al. 2003).
Filamentous pathogens (oomycetes and fungi).
Typically, biotrophs germinate on the host surface and attach through appressorium, followed by the apoplastic growth of hyphae, finally forming haustoria (the feeding structure) to obtain nutrients from the host. In contrast, necrotrophs derive nutrients by killing the host tissue and spreading from one cell to another. Hemibiotrophic fungi such as Magnaporthe oryzae breach the cuticle to form appressoria (infected cells) and rapidly colonize the host by forming invasive hyphae and secreting effectors, which can migrate from cell to cell and suppress host immunity (Giraldo et al. 2013). However, the signal or factor that drives the translocation is still debatable.
These pathogens use the PD as a suitable entry point to grow and invade the neighboring cells. In addition, invasive hyphae might constrict to pass through the PD (Kankanala et al. 2007). Inhibition of a single fungal MAPK, Pmk1, prevents the fungus from infecting neighboring cells (Sakulkoo et al. 2018). Due to their rapid colonization, the disease lesions appear within 4 to 5 days. Some oomycetes such as Hyaloperonospora arabidopsidis exploit stomata to reproduce through the emergence and spread of conidiosphore (Coates and Beynon 2010).
Bacteria.
Bacteria can enter plant tissues through natural openings or wounds and colonize the apoplast. However, unlike viruses and fungi, bacteria do not directly enter and spread through the
