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 endodermal cell fate and maintain the quiescent center function (Helariutta et al. 2000; Nakajima et al. 2001). Both WUS and SHR have been demonstrated to trafﬁc through the PD.

The passage of proteins through the PD is highly selective and is mediated by callose (β-1,3 glucan polymer) deposition at the PD oriﬁce, reducing the size exclusion limit. The PD-located proteins, including PD-localized proteins (PDLPs), PD-associated β-1,3 glucanase, PD-associated callose binding protein, callose synthase (CalS)/glucan synthase-like (GSL), and remorin-like proteins, regulate PD-callose homeostasis. A decreased PD permeability correlates with ROS accumulation (Cui and Lee 2016). The redox states of the cellular organelles such as mitochondria and chloroplast regulate PD permeability (Benitez-Alfonso et al. 2009; Stonebloom et al. 2012).

PLANT-PATHOGEN INTERACTION DURING CELL-TO-CELL COMMUNICATION

Preformed defense.

As the ﬁrst line of defense, plants use physical barriers to restrict the spread of pathogens from one cell to another. These barriers include the cuticle in leaves (cutin and waxes) and the cell wall (cellulose, hemicellulose, pectin, and proteins) (Somerville et al. 2004; Yeats and Rose 2013). In roots, cell-wall modiﬁcations include forming Casparian strips in the endodermis and depositing lignin, suberin (phenolic compound), lamellae, and secondary walls (Geldner 2013; Thomas et al. 2007). These act as apoplastic barriers for the entry and colonization of pathogens because mutants that are defective in cellulose or lignin synthesis are more susceptible to pathogens (Miedes et al. 2014).

The second level of defense includes a range of constitutive secondary metabolites such as antimicrobial proteins (defensin or defensin-like proteins) and chemicals (saponin and glucosinolates), generally called phytoanticipins (Osbourn 1996; Tierens et al. 2001). When a potential pathogen enters the host’s apoplast by releasing cell-wall-degrading enzymes (Bellaﬁore et al. 2008; Kämper et al. 2006), the “danger” cues (ROS and damage-associated molecular components) can be sensed by neighboring cells via intercellular signaling, priming the neighboring cells through the de novo synthesis of phytoalexins. Phytoalexins (e.g., camalexin) can interfere with the pathogen’s metabolism or maturation, leading to their inhibition. Plants also secrete proteases in the apoplast to suppress bacterial growth at a low pH (Wang et al. 2020), followed by intricate intra- and intercellular signaling, collectively known as apoplast immunity, an interface between preformed and induced defense.

Induced defense.

When potential phytopathogens breach the barriers mentioned above and reach the apoplasts, the plants activate the third level of inducible defense. This type of plant-pathogen interaction operates as a zig-zag model in three successive steps: pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI), effector-triggered susceptibility (ETS), and effector-triggered immunity (ETI) (Jones and Dangl 2006) (Fig. 1).

PTI.

Plants recognize PAMPs by speciﬁc membrane-localized pattern recognition receptors. The recognition of PAMPs (e.g., ﬂg22, a conserved ﬂagellar 22 amino acid long peptide) via pattern recognition receptors (FLS2 and BAK1) induces a complex network of signaling pathways such as mitogen-activated protein kinase (MAPK) signaling, Ca2+ signaling, ion ﬂux changes, defense hormones, and transcriptional reprogramming, collectively called PTI (Fig. 1B) (Jones and Dangl 2006; Zhou and Zhang 2020). Some defense responses are executed through the apoplast, including the accumulation of apoplastic ROS, a restricted efﬂux of nutrients from the cytosol to the apoplast, and the production and secretion of antimicrobial compounds such as camalexin (Ahuja et al. 2012; O’Brien et al. 2012).

Moreover, MPK3- and MPK6-mediated phosphorylation of transcription factor WRKY33 regulates the production of camalexin (Mao et al. 2011). One of the hallmarks of PTI is the increased regulation of symplastic trafﬁcking through callose deposition in the PD oriﬁce to limit cell-to-cell communication (Faulkner et al. 2013; Stahl and Faulkner 2016; B. Xu et al. 2017). A lower level of callose deposition is often correlated with higher infection and vice versa (Voigt and Somerville 2009). The PD-localized calcium-binding protein calmodulin-like protein 41 plays a crucial role in ﬂg22-induced PD closure to regulate plant immunity (B. Xu et al. 2017).

Chitin (a fungal PAMP), perceived by the PD PM-located lysin motif domain-containing glycosylphosphatidylinositol-anchored protein 2 (LYM2), triggers PD closure (Faulkner et al. 2013). The PD closure does not require the receptor chitin elicitor receptor kinase 1 located in the cellular PM. Cheval and Faulkner (2018) demonstrated that LYM2 induces phosphorylation and activation of NADPH oxidase respiratory burst oxidase homolog protein D and requires the calcium-dependent protein kinases (CPKs) CPK6 and CPL11 to mediate chitin-triggered PD closure through callose deposition.

These studies illustrated the speciﬁcity and signiﬁcance of PD in the PTI response that integrates calcium and ROS signaling. However, the degree and mode of action or inhibition cannot be generalized. For instance, the roots have a zone type-speciﬁc response. The ﬂg22-induced PTI response is spatially restricted in the root cap and the elongation zone, whereas elf18 induces little response overall. Moreover, chitin elicits a directional response in the differentiated zone (Kunze et al. 2004; Zhou et al. 2020). Laser-induced cell ablation in the epidermis strongly induces the PAMP response in the stele of the root but not in the neighboring epidermal cells (Zhou et al. 2020). This outcome could be due to less counter-mechanical stimulation or pressure from underlying cells or the perception of the collapse of PD integrity, which are of different degrees and quality in cortical and epidermal cells.

The application of ROS decreases the permeability of the PD, presumably via regulating callose synthesis and deposition (Cui and Lee 2016; Thomas et al. 2008). However, the mechanism and key players behind the ROS-mediated PD regulation during PTI in unknown. It is speculated that PDLP1 and PDLP5, which are associated with the immune response in Arabidopsis (Caillaud et al. 2014; Wang et al. 2013), could function with the domain of an unknown function protein (DUF26), which is proposed to be involved in ROS perception and signaling (Bourdais et al. 2015) and, thus, could mediate PAMP-triggered ROS signals (Cheval and Faulkner 2018).

ETS.

To overcome PTI, some pathogens deliver specialized virulence factors or effectors to the plant apoplast (apoplastic effectors) or directly inside cells (cytosolic effectors) which cause disease in susceptible plants, commonly called ETS (Fig. 1C). Pathogens’ diverse effectors may interfere with defense by various mechanisms in a spatially or temporally dependent manner, and the mode of invasion and action can vary from effector to effector (Toruño et al. 2016). Some effectors open up natural openings such as stomata for apoplastic colonization. Others move from cell to cell, exploiting the intercellular connection, and may target different cellular processes. For instance, effector protein RxLR3 from Phytophthora brassicae interacts with the PD-localized callose synthases CalS1, CalS2, and CalS3 and inhibits callose deposition to promote symplastic cell-to-cell Vol. 35, No. 2, 2022 / 99