Plasmodesmata-Dependent Intercellular Movement of Bacterial Effectors

Abstract

Pathogenic microorganisms deliver protein effectors into host cells to suppress host immune responses. Recent findings reveal that phytopathogens manipulate the function of plant cell-to-cell communication channels known as plasmodesmata (PD) to promote diseases. Several bacterial and filamentous pathogen effectors have been shown to regulate PD in their host cells. A few effectors of filamentous pathogens have been reported to move from the infected cells to neighboring plant cells through PD; however, it is unclear whether bacterial effectors can traffic through PD in plants. In this study, we determined the intercellular movement of Pseudomonas syringae pv. tomato (Pst) DC3000 effectors between adjoining plant cells in Nicotiana benthamiana. We observed that at least 16 Pst DC3000 effectors have the capacity to move from transformed cells to the surrounding plant cells. The movement of the effectors is largely dependent on their molecular weights. The expression of PD regulators, Arabidopsis PD-located protein PDLP5 and PDLP7, leads to PD closure and inhibits the PD-dependent movement of a bacterial effector in N. benthamiana. Similarly, a 22-amino acid peptide of bacterial flagellin (flg22) treatment induces PD closure and suppresses the movement of a bacterial effector in N. benthamiana. Among the mobile effectors, HopAF1 and HopA1 are localized to the plasma membrane (PM) in plant cells. Interestingly, the PM association of HopAF1 does not negatively affect the PD-dependent movement. Together, our findings demonstrate that bacterial effectors are able to move intercellularly through PD in plants.

Plasmodesmata-Involved Battle Against Pathogens and Potential Strategies for Strengthening Hosts

“…Usually, bacterial pathogens do not cross the cell wall, probably because their suitable habitat is mostly limited to the apoplastic spaces between plant cells, unlike viruses and fungi which spread intercellularly during local and systemic infections (reviewed by Lee and Lu, 2011 ). Still, bacteria can release specific effector molecules into plant cells not unlike fungi do, which then move through the PD to spread intercellularly in the host (Li et al, 2020 ; Figure 1 ). Only a few effectors have been studied to date.…”

“…Once there, HopO1-1 enhances the PD-dependent intercellular molecular flux by destabilizing the PDLP7 and PLDP5 proteins of hosts without affecting their transcript levels (Aung et al, 2020 ). Further, Li et al ( 2020 ) recently proved that the movement of 16 Hop effectors of Pst DC3000 move from transformed cells into neighboring cells through PD depends on their molecular weights. Among them, HopAF1 was characterized by the highest PD-dependent movement, which can nonetheless be inhibited by callose overproduction (Li et al, 2020 ).…”

“…Further, Li et al ( 2020 ) recently proved that the movement of 16 Hop effectors of Pst DC3000 move from transformed cells into neighboring cells through PD depends on their molecular weights. Among them, HopAF1 was characterized by the highest PD-dependent movement, which can nonetheless be inhibited by callose overproduction (Li et al, 2020 ). This study provided robust evidence that the effectors of bacteria, like fungi, may possess an intercellular mobile ability.…”

Genome Editing for Plasmodesmal Biology

“…Furthermore, the mechanism of HopO1-1-enhanced PD permeability seems to be PDLP5/PDLP7-regulated callose accumulation-dependent. In addition to HopO1-1, recent studies reported that several effectors from P. syringae not only localized at PD, but they also moved symplastically between the cells through these channels ( Kang et al, 2021 ; Li et al, 2021 ). It was also suggested that the intercellular movement of effectors is PD permeability dependent manner ( Li et al, 2021 ).…”

“…In addition to HopO1-1, recent studies reported that several effectors from P. syringae not only localized at PD, but they also moved symplastically between the cells through these channels ( Kang et al, 2021 ; Li et al, 2021 ). It was also suggested that the intercellular movement of effectors is PD permeability dependent manner ( Li et al, 2021 ). However, the molecular linkage between the intercellular movement of effectors and PD regulation is still poorly understood.…”