Aphids curtail the impact of feeding damage by limiting oligogalacturonide release and suppressing cell wall associated immunity

Aphids are insect pests that use piercing-sucking mouthparts to navigate into leaf tissues and feed from phloem sap. During feeding and probing, aphids penetrate the rigid plant cell walls and deliver effector proteins mixed with saliva into the host plant cells. Cell wall damage usually leads to the release of damage-associated molecular patterns (DAMPs), including oligogalacturonides (OGs), which promote pattern recognition receptor (PRR)-triggered immunity (PTI) against pathogens. Whether OG-induced plant defence responses play a role in aphid-plant interactions is not fully understood. Here we show that OGs are released in aphid-exposed leaves but less so than in non-treated plants, indicating that these insects may suppress the accumulation of OGs during feeding. Prior exposure of plants to OGs induces plant defense responses that reduce the ability of M. persicae to colonize plants. This plant defense is suppressed by the aphid effector Mp10 (also known as chemosensory protein 4 or CSP4) that is delivered by aphids into the cytoplasm of plant cells. Mp10 suppresses PTI responses to OGs and a variety of other elicitors. In understanding it’s mode of action we have found a possible role for Mp10 in the regulation of PTI via the trafficking of cell surface PRRs. Therefore, aphids actively manage the impact of feeding damage by limiting OG release and suppressing cell wall associated immunity.Generation of schematics: The schematics in background panel ii, in Results panel 5, and in Conclusions panel, were created with BioRender.com. Acknowledgments: We thank Cyril Zipfel (The Sainsbury Laboratory, Norwich Research Park, Norwich, UK) for the bak1-5 bkk1-1 seeds and Jen Sheen (Department of Molecular Biology, Massachusetts General Hospital, Department of Genetics, Harvard Medical School, Boston, MA, USA) for cpk5 cpk6 cpk11 seeds. We are grateful to the John Innes Centre (JIC) Horticultural Services for growing plants, the JIC Entomology Facility for rearing aphid stocks, and the JIC Bioimaging Platform for helping with confocal experiments. This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) grants (Grant numbers: BB/R009481/1, BB/V008544/1, BBS/E/J/000PR9795, BBS/E/J/000PR9796 and BBS/E/J/000PR9797) and the John Innes Foundation. Additional support was received from Sapienza University "Progetti di Avvio alla Ricerca 2016" (Project number: AR21615506343970), EMBO Short-Term Fellowship (ASTF number: 477-2016) and PRIN 2017 (Grant number: 2017ZBBYNC)