Cell-to-cell communication is fundamental to all multicellular organisms. In plants, the cytoplasm of adjacent cells is connected via intercellular ‘tunnels’ that cross the cell wall called plasmodesmata. These establish direct connections between cells and allow for the exchange of molecular resources and information to enable the co-ordination of responses to environmental and developmental signals. Plasmodesmata function as molecular ‘sluice gates’ to regulate the flux of soluble molecules between cells. We observed that whether plasmodesmata are open or closed underpins whether tissues can execute a full immune response, but it is not understood how independent immune-competent cells communicate and co-ordinate their responses which are both critical for organism-level responses.
This led us to ask how the connectivity of cells regulates multicellular immunity and, in this project, to address the specific questions: what immune responses are dependent upon plasmodesmal connectivity between cells? and what do host plants gain from regulation of their plasmodesmata during pathogen infection?
We have performed a series of high resolution experiments that firstly addressed how plasmodesmata underpin immune responses. We have shown that whether cells are symplastically connected to their neighbours affects the spatiotemporal profile of the response. We find that if plasmodesmata are closed independently of a pathogen, this alone triggers stress and induces the production of defence hormones to enhance plant resistance to biotrophic pathogens. Calcium responses are a key element of immunity and when we examine how calcium waves spread through a plant we found that unexpectedly, they do not travel through plasmodesmata. This changed common perception about these dramatic and critical response and will force the research community to explore new hypotheses for how signals spread through plants.
We have also found that pathogens target and manipulate plasmodesmata, and that many of their effector proteins that are secreted into host cells can move between cells through plasmodesmata. These effectors can interfere with the host immune response, suggesting that effectors advance ahead of the infection front to disable immunity before the pathogen gets to specific cells. We also found that pathogens can open the plasmodesmata up to facilitate this, raising intriguing questions of how a protein from an organism that does not have plasmodesmata can specifically manipulate these plant-specific structures.
Cell to cell connectivity is critical to both the host and the invading microbe, presenting a key battleground in infection. Our data identifies that for the host, whether plasmodesmata are open or closed regulates immune execution and carbon distribution and this must be balanced to optimise the outcomes of both growth and immunity. Pathogens can subvert these host processes and access resources to enable through own growth. Thus, all these factors are under complex spatiotemporal regulation to determine whether host or microbe controls the cellular network.
