Phytophthora infestans: An interactome exposes a master manipulator
Phytophthora infestans is a mold-like oomycete pathogen, notoriously known for triggering the Irish potato famine in 1845. Almost two centuries later, scientists are still trying to unravel how exactly this organism makes plants sick. A comprehensive understanding of effector biology is key to answering this question. Effectors are proteins secreted by pathogens to suppress the plant’s immune system or manipulate certain cell functions for their own benefit. Until recently, most studies have focused on the targeted actions of individual effectors that expose only certain threads of how these pathogens cause disease. However, as sequencing technology and bioinformatics have become more advanced, scientists are now able to expand their view of how processes throughout the plant cell are impacted by pathogen effectors.
Through the use of co-immunoprecipitation and tandem mass spectrometry, it is now possible to identify which effectors interact with which plant proteins. Following this pipeline, researchers at The Sainsbury Laboratory were able to construct an expansive network of interactions connecting 59 P. infestans RXLR effectors with 586 plant proteins from Nicotiana benthamiana. Further investigation into the functions of these plant proteins using gene ontology analysis allowed scientists to derive which plant processes these pathogen effectors were targeting. One such family of effectors, PexRD12/31, was identified as targeting the behaviour and proliferation of host vesicles. Vesicles cargo organic compounds to different parts of plant cells and it is likely that the manipulation of these by the pathogen increases the extractability of nutrients from the host plant cells. This manipulation was subsequently observed directly using advanced microscopy, supporting this hypothesis.
Not only has this study provided fascinating insights into how P. infestans causes disease in plants, it has also validated how the use of interactomes constructed out of proteomics data are powerful resources in pinpointing the relationship between families of effectors and host processes. This study was merely a first step into exploring the nature of interactions presented in the interactome, and the authors believe there are still many relationships to identify. By making these data openly available to the community, they invite other researchers to leverage the interactome in their own investigations. As more and more information is becoming available with advanced technologies, open-sourcing data and facilitating global collaborations are key in answering fundamental plant pathology questions.
Mauricio Contreras, co-first author and doctoral candidate, said “While it is clear that P. infestans is able to massively reprogram its host, knowing what plant proteins and processes are being targeted is just the beginning of the story! We hope this host interactome is useful to the community and inspires scientists to come up with new avenues of scientific exploration.”
The senior postdoctoral scientist and co-lead of the study, Dr Joe Win, said “It is mind boggling to think how a microbe like Phytophthora infestans can breach layers of sophisticated defense systems present in plants and cause disease. The interaction network of the effectors and plant proteins we reported here has opened the door to study the infection process more holistically and identify areas where we could help protect plants. We have made all data openly available so that anyone who is interested can use them freely. We hope this research will form the basis of many more exciting research projects that will help protect our food sources.”
This research was funded primarily from the Gatsby Charitable Foundation, Biotechnology and Biological Sciences Research Council (BBSRC, UK), and European Research Council (ERC; NGRB and BLASTOFF projects). Ben Petre, co-first author and an TSL alumnus, was supported by a grant overseen by the French National Research Agency (ANR) as part of the ‘Investissements d’Avenir’ program (ANR-11-LABX-0002-01, Lab of Excellence ARBRE).
Benjamin Petre, Mauricio P Contreras, Tolga O Bozkurt, Martin H Schattat, Jan Sklenar, Sebastian Schornack, Ahmed Abd-El-Haliem, Roger Castells-Graells, Rosa Lozano-Duran, Yasin F Dagdas, Frank L H Menke, Alexandra M E Jones, Jack H Vossen, Silke Robatzek, Sophien Kamoun, Joe Win. Host-interactor screens of Phytophthora infestans RXLR proteins reveal vesicle trafficking as a major effector-targeted process, The Plant Cell, 2021;, koab069, https://doi.org/10.1093/plcell/koab069
For further information or to arrange an interview with Mauricio Contreras or Joe Win, contact:
About the Sainsbury Laboratory
The Sainsbury Laboratory is a world-leading independent research institute that specialises in plant-microbe interactions, funded by The Gatsby Charitable Foundation, The University of East Anglia and UKRI-BBSRC. Its work is focused on leading global efforts to reduce crop losses to disease.