Shapeshifting: how is plant ER architecture manipulated by pathogen effectors?

The world population is predicted to reach 9.7 billion by 2050, compared to today's 7.9 billion. More food needs to be produced from ever-dwindling natural resources with the additional challenges arising from climate change. The UK imports 45% of all its food and so future food security is both a global and a national issue that needs urgently addressing. One key approach is to reduce waste in the food chain. Between 17-30% of global crops are lost to pests and disease both pre- and post-harvest. The big challenge is therefore to breed crops with enhanced tolerance to plant pathogens (disease-causing microorganisms) but, crucially, without adversely compromising yield.

The endoplasmic reticulum (ER) is a major protein and lipid factory present in every plant cell. It forms a mesh-like network of membrane tubules and sheets, which extends throughout the cell and between nearby cells and is constantly reshaping and reorganising to meet the cells' changing demand for proteins.

We have recently discovered that when a harmful bacterial pathogen infects plant leaves, it causes a dramatic and rapid reorganisation of the plant ER, which seems to weaken the ER's capacity to participate in the cellular defence and therefore helps the pathogen invade. Our project will establish precisely how particular molecules produced by the pathogen, called 'effectors', remodel the ER architecture, and which specific effectors participate in this process. We aim to use this information, together with a toolkit of ER-shaping proteins that we have produced and studied over the last 10 years, in order to re-engineer the plant's ER into a bespoke form that is better suited to withstand pathogen attack. Success will represent a substantial impact on reducing crop losses and thus increasing our food security.

The plant endoplasmic reticulum (ER) is a highly pleomorphic organelle which rapidly remodels to meet the changing demands of the cell. It is extremely sensitive to perceived perturbations in environmental conditions such as temperature, mechanical stress and, as described here, pathogen infection. Our data show that the ER is an important and early target for pathogen effectors, but the underlying biology is not well understood.

We have recently discovered that when Arabidopsis leaves are infected by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000, the ER network undergoes dramatic and rapid reorganisation, which is necessary for pathogen proliferation. Crucially, these changes to the ER's shape and movement occur on a cell-autonomous basis, with some cells in the immediate vicinity of DC3000 showing striking ER alterations but other cells appearing completely unaffected. These alterations to the ER require the secretion of effector molecules into the plant cell. A few pathogen effectors are known to target the ER either directly or indirectly, but little is known about their modus operandi in promoting disease.

We have also discovered that Arabidopsis mutants with altered expression of key ER morphogenic proteins display very significant differences in their susceptibility to DC3000, further indicating that regulation of ER morphology is a key battleground during pathogen infection.

In this project we will build on these findings to:

- elucidate how ER architecture is remodelled by DC3000 and which specific effectors are involved in this process, with a view to better understanding the role of this relatively neglected, but essential, cellular component in plant disease resistance.

- use this information, together with our existing toolkit of ER-shaping proteins, to engineer 'smart' plants that are able to rapidly alter their ER architectural dynamics in response to biotic perturbations.