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

Authors: Gravino Matteo; Pontiggia Daniela; Mugford Sam; Joyce Joshua; Drurey Claire; Prince David; Cervone Felice; +2 Authors

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

Abstract

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.

{"references": ["Bass\u00a0et al. (2014). The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Biochem Mol Biol 51: 41-51.", "Bos et al. (2010). A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genetics 6(11): e1001216.", "Mugford et al. (2016). An immuno-suppressive aphid saliva protein is delivered into the cytosol of plant mesophyll cells during feeding. Mol Plant Microbe Interact 29(11): 854-861.", "Silva-Sanzana\u00a0et al. (2019). Pectin methylesterases modulate plant homogalacturonan status in defenses against the aphid\u00a0Myzus persicae. Plant Cell 31(8): 1913-1929.", "Deshoux\u00a0et al. (2022). Role of acrostyle cuticular proteins in the retention of an aphid salivary effector. Int J Mol Sci 23(23):15337.", "Agrios (2005). Plant diseases caused by viruses. Plant Pathology (Fifth Edition), 723-824. DOI: 10.1016/B978-0-08-047378-9.50020-8.", "De Mori (2020). Molecular tools to investigate Sharka disease in Prunus species. Applied Plant Biotechnology for Improving Resistance to Biotic Stress, 203-223. DOI: 10.1016/B978-0-12-816030-5.00010-0.", "Zitter and Murphy (2009). Cucumber mosaic.\u00a0The Plant Health Instructor.\u00a0DOI: 10.1094/PHI-I-2009-0518-01."]}

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).

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Italy
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Keywords

Aphid effector protein Mp10, Arabidopsis thaliana, Calcium-Dependent Protein Kinases (CDPKs), Glycine-Rich Protein 3 (GRP3), Myzus persicae, Oligogalacturonides (OGs), PAMP-triggered immunity (PTI), Somatic Embryogenesis Receptor Kinases (SERKs)

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This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
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