Plasmodesmata Localizing Proteins Regulate Transport and Signaling during Systemic Acquired Immunity in Plants

Abstract

Systemic acquired resistance (SAR) in plants is mediated by the signaling molecules azelaic acid (AzA), glycerol-3-phosphate (G3P), and salicylic acid (SA). Here, we show that AzA and G3P transport occurs via the symplastic route, which is regulated by channels known as plasmodesmata (PD). In contrast, SA moves via the extracytosolic apoplast compartment. We found that PD localizing proteins (PDLP) 1 and 5 were required for SAR even though PD permeability in pdlp1 and 5 mutants was comparable to or higher than wild-type plants, respectively. Furthermore, PDLP function was required in the recipient cell, suggesting regulatory function in SAR. Interestingly, overexpression of PDLP5 drastically reduced PD permeability, yet also impaired SAR. PDLP1 interacted with AZI1 (lipid transfer-like protein required for AzA- and G3P-induced SAR) and contributed to its intracellular partitioning. Together, these results reveal the transport routes of SAR chemical signals and highlight the regulatory role of PD-localizing proteins in SAR.

Role of plasmodesmata and plasmodesmata localizing proteins in systemic immunity

“…11,12 Likewise, only a small percentage of SA is transported to the distal tissues. 23 Together, these results suggest that the transport of SA, AzA, and G3P is unlikely to be via simple diffusion from the source (infected) to sink (distal) tissues. 24 A tight regulation of the transport of AzA, G3P, and SA to the distal tissues is likely advantageous because it would be expected to better regulate the untimely induction of defenses in the distal uninfected tissues and thereby prevent metabolic perturbations that could be detrimental to overall plant health and fitness.…”

“…We recently showed that the transport of AzA and G3P from local to distal tissues occurs via the symplastic route, 23 regulated by plasmodesmata (PD) channels. 25,26 In contrast, SA moves via the extracytosolic apoplastic compartment (Fig.…”

“…This is consistent with the fact that pathogen infection negatively regulates PD permeability. 23 Thus, the apoplastic transport route of SA would enable its transport in spite of reduced PD permeability in pathogen-infected plants. As expected, reduced PD permeability results in decreased transport of AzA and G3P, but not SA.…”

“…28 Consistent with their impaired transport, plants overexpressing PDLP5 were defective in SAR. 23 Moreover, localized application of AzA, G3P, or other SAR signals including NO, ROS and SA were unable to rescue the SAR defect of 35S-PDLP5 plants. Together, these results suggest that PD-mediated symplastic transport of AzA and G3P, and likely other molecules induced in response to pathogen infection or AzA/G3P application is critical for the normal induction of SAR.…”

“…The induced levels of cytosolic SA inhibits PD permeability, 27 and this in turn correlates with pathogen induced reduction in PD permeability. 23 The levels of PD localizing protein 5 regulates PD permeability and thereby transport of AzA and G3P via PD but has no affect on the transport of SA. Both PDLP1 and PDLP5 proteins are required for SAR and contribute to the partitioning of the lipid transfer protein AZI1 between the plastids (chl) and cytoplasm.…”