(JA), brassinosteroids, and strigolactones, play essential roles in integrating developmental and environmental cues. Although these are transported through the PD, many (e.g., SA, JA, GA, and auxin) regulate PD permeability under stress (Farmer et al. 2014; Han et al. 2014; Wang et al. 2013). In addition to the intercellular movement, phytohormones are detected in the phloem sap (e.g., SA), suggesting that plants may strategically use these micromolecules as signaling molecules at the local or systemic level (Lee and Frank 2018). Pathogens have evolved to manipulate the host defense system by producing hormones or their functional mimics or exploiting their antagonistic relationships and complex crosstalk. Selected hormones involved in defense and PD regulation are discussed below.
SA.
The accumulation of SA is required for both basal and induced immune responses (Fu and Dong 2013). A recent study found that intercellular communication during ETI is essential for cell survival (Zavaliev et al. 2020). Moreover, HR in distal tissue from the infection site promotes SA-inducing NPR1 condensation, in which NPR1 associates with an E3 ubiquitin ligase complex, and stress-related proteins are targeted to the proteasome. This phenomenon was not observed in the npr1 mutant, indicating that NPR1 is required for cell survival and inhibits ETI in secondary infections (Mittag and Strader 2020).
Although manipulating hormone signaling may confer resistance in plants, their constitutive induction also leads to pleiotropic effects on plant growth. This can, however, be avoided by the spatiotemporal regulation of gene expression. For example, a rice-blast-resistant plant was produced using controlled transcription and translation of NPR1 without affecting the growth and yield (G. Xu et al. 2017).
A molecular link between the regulation of immunity, hormonal signaling, and PD permeability has also been demonstrated. A PD-resident protein required for PD closure and basal immunity, PDLP5 is expressed at a low level in the absence of a pathogen attack. However, the expression is increased upon a pathogenic attack and the exogenous application of SA (Lee et al. 2011). Overexpression of PDLP5 reduced the PD permeability but both overexpression and loss of function result in a compromised SAR (Lim et al. 2016).
Another study found that the exogenous application of SA induces callose deposition and regulates PD closure (Wang et al. 2013). Callose synthase genes CALS1 and CALS8 are upregulated by an increased level of SA and ROS, respectively, both playing a role in PD closure (Cui and Lee 2016). A recent study demonstrated that SA triggers PD closure by reorganizing the PM lipid raft nanodomain (Huang et al. 2019). In addition, SA modulates the lipid raft-regulatory protein remorin (which is crucial for PM nanodomain assembly) and triggers the compartmentalization of the lipid raft nanodomain. This action results in the closure of the PD to restrict the spread of the virus (Huang et al. 2019). A remorin from Nicotiana (REM4) was recently found to interact with the effector HopZ1a, inducing ETI (Albers et al. 2019).
JA.
Plants produce JA, which can be apoplastically or symplastically transported from cell to cell as a defense hormone against various pathogens (Li et al. 2017; Mielke et al. 2011). Plants overexpressing PDLP5 have high JA in exudates and a reduced size exclusion limit, suggesting lower symplastic access of JA to the phloem (Lim et al. 2016). In addition, RipE1, an effector from Ralstonia solanacearum, is delivered in the host through the Hrp type III secretion system. Moreover, RipE1 is a protease that degrades the JAZ repressor and induces the expression of JA-responsive genes. The induction of JA signaling suppresses SA signaling and helps bacteria establish successful infection and bacterial wilt through ETS (Nakano and Mukaihara 2019).
Auxin.
Auxin regulates growth and development, which may be closely linked to defense signaling (Kazan and Manners 2009). Despite being a small and expectedly freely diffusible molecule, its tissue gradient is highly regulated across the PD through de novo callose deposition (Han et al. 2014). The auxin-PD-callose feedback loop regulates the symplastic transport of auxin in the hypocotyl and leaf for the phototropic response in the root for lateral root emergence (Gao et al. 2020; Sager et al. 2020). The reduction of enzyme activity such as GLS8/CalS10 (an enzyme involved in callose synthesis) indicates reduced apoplastic auxin transport and increased PD permeability (Han et al. 2014). The synthesis of callose suppresses cell death induced by a low calcium level. In addition, GSL10/CalS9 is required to alleviate defense response and cell-wall damage under low calcium conditions (Shikanai et al. 2020). Furthermore, GSL8 interacts with PDLP5 and GSL10 (Saatian et al. 2018). Symplastic transport of other signaling agents, including macromolecules, might be regulated by auxin or regulated with cross-talk in different pathways (Band 2021; Han et al. 2014). Overall, these data point to an intricate signaling network of defense (calcium signaling and callose synthesis) and hormone (auxin) transportation through
the PD.
ABA.
ABA is known to play a role in stomatal immunity (closure of the stomata after PAMP perception to restrict pathogen entry) against a broad spectrum of pathogens. However, ABA perception through the PYR1 receptor modulates the cross-talk between SA and ET signaling, redirecting the defense outcome (García-Andrade et al. 2020). Overexpression of ERF8, an ABA-inducible transcriptional repressor, negatively regulates ABA-mediated signaling and induces PCD in plants. In addition to accumulating apoplastic ROS, ABA signaling plays a role in bud dormancy and biotic stress such as the cell-to-cell spread of viruses and fungi by regulating the PD permeability through callose deposition, the number of PD, and the formation of a secondary PD (Alazem and Lin 2017; Kitagawa et al. 2019). The antiviral role of ABA is also achieved by the induced expression of RNA-silencing pathway genes (Alazem and Lin 2017).
CK.
A recent study found that CK induces systematic immunity in the tomato against fungi, dependent on SA and ET (Gupta et al. 2020). The exogenous application of CK also enhances the formation of a secondary PD in Sinapis alba (Ormenese et al. 2006). The PD callose regulates the long-distance movement of CK (Bishopp et al. 2011).
ET and GA.
The role of ET and GA in immunity has been extensively studied (De Bruyne et al. 2014; Guan et al. 2015). However, its dual function in regulating PD permeability and immunity is not yet reported. Moreover, P. syringae effector HopAF1, whose translocation is regulated by PDLPs during ETI, blocks ET induction to suppress immunity (Washington et al. 2016). In addition, GA regulates PD permeability, presumably through PD-associated β-1,3 glucanase, and the expression of PDBG mRNAs requires GA during development and stress (Rinne et al. 2001; Wu and Bradford 2003). Due to this evidence, it would be interesting to study how ET and GA (individually or through hormonal cross-talk) regulate cell-to-cell communication during plant-pathogen interaction (Table 1).
