A PDLP-NHL3 complex integrates plasmodesmal immune signaling cascades

Abstract

The plant immune system relies on the perception of molecules that signal the presence of a microbe threat. This triggers signal transduction that mediates a range of cellular responses via a collection of molecular machinery including receptors, small molecules, and enzymes. One response to pathogen perception is the restriction of cell-to-cell communication by plasmodesmal closure. We previously found that while chitin and flg22 trigger specialized immune signaling cascades in the plasmodesmal plasma membrane, both execute plasmodesmal closure via callose synthesis at the plasmodesmata. This indicates the signaling pathways ultimately converge at or upstream of callose synthesis. To establish the hierarchy of signaling at plasmodesmata and characterize points of convergence in microbe elicitor-triggered signaling, we profiled the dependence of plasmodesmal responses triggered by different elicitors on a range of plasmodesmal signaling machinery. We identified that, like chitin, flg22 signals via RBOHD to induce plasmodesmal closure. Further, we found that PDLP1, PDLP5 and CALS1 are common to microbe- and SA-triggered responses, identifying PDLPs as a candidate signaling nexus. To understand how PDLPs relay a signal to CALS1, we screened for PDLP5 interactors and found NHL3, which is also required for chitin-, flg22- and SA-triggered plasmodesmal responses and PDLP-mediated activation of callose synthesis. We conclude that a PDLP-NHL3 complex acts as an integrating node of plasmodesmal signaling cascades, transmitting multiple immune signals to activate CALS1 and plasmodesmata closure.

Plasmodesmal closure elicits stress responses

“…Plasmodesmal closure is an early reaction, initiated within 30 minutes upon perceiving pathogen-derived molecules and stress-associated signals including SA and hydrogen peroxide (Xu et al 2017;Cheval et al 2020;Tee et al 2023b), and is critical for the execution of a full response. Thus, we reason that plasmodesmal closure regulates a range of downstream processes.…”

“…Thus, we reason that plasmodesmal closure regulates a range of downstream processes. However, considering the plethora of responses elicited during immunity, and the array of elicitors that trigger plasmodesmal closure via converging signaling pathways (Tee et al 2023b) Transcriptional profiling of responses to plasmodesmal closure identified transcriptional signatures of defense responses associated with SA production and signaling. It has long been known that constitutive over-production of the plasmodesmal protein PDLP5 closes plasmodesmata and leads to high levels of SA (Wang et al 2013).…”

“…The copyright holder for this preprint this version posted May 11, 2024. ; https://doi.org/10.1101/2024.05.08.593115 doi: bioRxiv preprint 3 PLASMODESMATA LOCATED PROTEIN 5 (PDLP5) integrates these responses, as well as plasmodesmal responses triggered by the defense hormone salicylic acid (SA; Wang et al 2013;Tee et al 2023b). The observation that lym2 mutants cannot close their plasmodesmata in response to chitin but execute normal chitin-triggered mitogenactivated protein kinase (MAPK) activation and apoplastic ROS production (Faulkner et al 2013) indicates that plasmodesmal signaling cascades can act independently of other responses.…”

The FW2.2/CNR protein regulates cell-to-cell communication in tomato by modulating callose deposition at plasmodesmata

“…The level of callose deposition is a highly regulated process involving two antagonistic enzymes, Callose Synthases and β-1,3-glucanases (Chen and Kim, 2009). Callose deposition is enhanced according to two main signalling pathways, one Reactive Oxygen Species (ROS)-dependent and the other one salicylic acid (SA)-dependent, which both induce the expression of receptor proteins such as PDLP5 that participate with Callose Synthase proteins in the regulation of PD permeability (Cui and Lee, 2016; Amsbury et al, 2018; Tee et al, 2022). The expected decrease in PD permeability under H 2 0 2 stress was not observed when FW2.2 is overexpressed, suggesting that FW2.2 play a role in the ROS-dependent pathway.…”

Plant plasmodesmata bridges form through ER-driven incomplete cytokinesis

“…1 A-H). These bridges are maintained post-cytokinesis and are the foundation for generating a multicellular communication network, indispensable for plant life (3,(10)(11)(12)(13)(14)(15)(16)(17)(18).…”