trafficking in the leaf (Tomczynska et al. 2020). In addition, PWL2 and BAS1 effectors secreted by the infection hyphae of the rice blast fungus first accumulate at the biotrophic interfacial complex, then symplastically move from one cell to another. The effectors may move ahead of the infection hyphae, depending on the size of the effector and the cell type (Khang et al. 2010).
In contrast, another effector, BAS4, uniformly expressed in the infection hyphae, does not translocate through the cytoplasm. The corn smut effector Cmu1, which disrupts the SA signaling pathway, moves symplastically (Djamei et al. 2011). Bacteria such as Pseudomonas syringae strain DC3000 deliver dozens of effectors using the type III secretion system, affecting multiple components and manipulating cellular processes and intercellular communication (Aung et al. 2020; Lewis et al. 2009). A recent study demonstrated that the movement of effectors such as other molecules across the PD largely depends on their molecular weight (Li et al. 2021). The cell-to-cell movement of effectors possibly primes host cells for further pathogen colonization (Toruño et al. 2016). The exact mechanism of the movement of effectors through the PD and whether this movement is regulated remain to be deciphered.
Fig. 1. Plant defense is executed through intercellular communication. A, Resting stage. Callose hemostasis is regulated by plasmodesmata (PD)-located proteins: PD-localized proteins (PDLPs), PD-associated β-1,3 glucanase (PDGB), PD-associated callose binding protein (PDCB), and callose synthase (CalS)/glucan synthase-like (GSL). B, Pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). Detection of PAMP using a pattern recognition receptor (PRR) activates early immune responses such as the production of reactive oxygen species (ROS), activation of mitogen-activated protein kinase (MAPK), Ca2+ signaling, defense gene expression, and PD closure through callose deposition, secretion of secondary metabolites, and the establishment of an ROS wave in the apoplast. C, Effector-triggered susceptibility (ETS). Effectors delivered by type III secretion system may negatively regulate MAPK and Ca2+ signaling, inhibiting defense gene expression. Effectors may assist in apoplastic colonization to suppress the immune response or may translocate through the PD to inhibit the systemic response. D, Effector-triggered immunity (ETI). Effector recognition by resistance protein triggers early and late immune responses such as the synthesis of pathogenesis-related (PR) proteins, and the restricted translocation of effectors by PDLPs helps in the hypersensitive response. E, Systemic acquired resistance (SAR). Execution of defense responses in distantly located cells mediates mobile signaling molecules translocated through the PD or apoplast. The master regulator of SAR, pipecolic acid, is regulated by MAPK signaling in the local cell.
ETI.
Resistant plants have evolved to recognize effectors via intracellular nucleotide binding site (NBS) and the leucine-rich (LRR) repeat domain or resistance proteins and counterattack by inducing ETI (Fig. 1D). The amplitude and acceleration of ETI are faster than PTI, usually causing localized cell death, called hypersensitive response (HR), at the infection site.
However, recent data indicate positive feedback regulation between PTI and ETI. The ETI boosts PTI responses, and PTI strengthens ETI-induced HR during P. syringae strain DC3000 infection (Ngou et al. 2020). In addition, HR is believed to work in concert with callose deposition (Rinne and van der Schoot 2003). One of the hallmarks of ETI is the synthesis of pathogenesis-related proteins, which are localized to PD in maize and restrict PD permeability (Murillo et al. 1997).
Recently, more evidence associates ETI with the PD function. For instance, upon recognizing an effector from P. syringae, HopW1-1 induces a resistance response such as the accumulation of the signal molecule SA, inducing the expression of several defense-related genes (Lee et al. 2008). One of the induced genes is HopW1-1, a member of the PDLP gene family, indicating the role of ETI in PD trafficking (Lee and Lu 2011; Thomas et al. 2008). In addition, PDLP5 and PDLP7 negatively regulate the symplastic movement of the P. syringae strain DC3000 effector HopAF1.
Another study demonstrated that two effectors, Avr2 and Six5, from the fungus Fusarium oxysporum are required for ETI in the tomato. Furthermore, Avr2 and Six5 interact at the PD, and Avr2 moves from cell to cell in the presence of Six5, causing disease in susceptible plants. However, HR is induced when the I-2 protein recognizes Avr2 in the xylem-adjacent cell of the resistant plant (Cao et al. 2018). The electrophysical study of HR induced by the effector avrRpt2 revealed the occurrence of a rapid, irreversible depolarization of the membrane that might propagate through the PD (Pike et al. 2005).
Systemic acquired resistance.
Activation of the abovementioned local defense signaling might lead to the induction of cell-to-cell communication and execution defense responses at the systemic level, known as systemic acquired resistance (SAR) (Fig. 1E). In addition, SAR can be described as the fourth level of defense response because it ensures enhanced resistance against the subsequent pathogenic challenge. Furthermore, SAR activation depends on two signaling pathways to generate signaling molecules, such as azelaic acid and glycerol-3-phosphate: (i) SA and the signaling protein NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) and (ii) ROS and nitric oxide (Singh et al. 2017). The SAR signaling molecule is transported from the site of infection to distantly located uninfected tissues.
Moreover, SA moves apoplastically, whereas azelaic acid and glycerol-3-phosphate both use the symplastic route to track the vasculature and eventually distribute to systemic tissues (Lim et al. 2016; Yu et al. 2013). Defective in induced resistance 1 (DIR1) is a lipid transfer protein involved in SAR, moving symplastically (Carella et al. 2015). When these signals arrive at systemic tissues, they initiate the de novo synthesis of defense-related molecules, which could lead to activating SAR (Lim et al. 2016; Singh et al. 2017; Yu et al. 2013).
The PDLPs interact and modulate the stability of SAR components. For instance, azelaic acid induced 1 (AZI1), a DIR1-interacting protein required for SAR, interacts with PDLP1 and PDLP5. In addition, PDLP1 and PDLP5 are required for AZI1 stability, and the loss of either PDLP1 or PDLP5 leads to the delocalization of AZI1 to chloroplasts (Carella et al. 2015; Lim et al. 2016). The systemic movement of DIR1 is also abolished in plants overexpressing PDLP1 and PDLP5, indicating that feedback regulation through PD is crucial for long-distance SAR signaling (Carella et al. 2015). It is suggested that PDLPs involved in SAR retain their localization to PD but PDLPs can relocalize to different cell compartments during defense (Caillaud et al. 2014).
Another mobile element contributing to SAR is pipecolic acid. Pipecolic acid functions upstream of nitric oxide or ROS, azelaic acid, and glycerol-3-phosphate pathways and is synthesized by aberrant growth and death 2 (AGD2)-like defense response protein 1. Wang et al. (2018) demonstrated that the accumulation of pipecolic acid and expression of AGD2-like defense response protein 1 are induced by the activation of the MAPK enzymes MPK3 and MPK6 and the phosphorylation of downstream WRKY33, suggesting the critical role of MAPK signaling in SAR establishment.
CELL-TO-CELL COMMUNICATION, HORMONES, AND DEFENSE
Plant hormones such as auxin, gibberellins (GA), abscisic acid (ABA), cytokinins (CK), SA, ethylene (ET), jasmonates
