Pseudomonas syringae type III secretion protein HrpP manipulates plant immunity to promote infection

Authors: LI, JUN-ZHOU - Chinese Society Of Agricultural Engineering; JIN, YA - Chinese Society Of Agricultural Engineering; ZHANG, WEI - Cornell University; CONG, SHEN - Chinese Academy Of Agricultural Sciences; ZHUANG, QIQUO - Sichuan University; GU, YI-LIN - Chinese Society Of Agricultural Engineering; Filiatrault, Melanie; WEI, HAI-LEI - Chinese Academy Of Agricultural Sciences

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/22/2023
Publication Date: 4/17/2023
Citation: Li, J., Jin, Y., Zhang, W., Cong, S., Zhuang, Q., Gu, Y., Filiatrault, M.J., Wei, H. 2023. Pseudomonas syringae type III secretion protein HrpP manipulates plant immunity to promote infection. Nature Communications. 11(3):e05148-22. https://doi.org/10.1128/spectrum.05148-22.
DOI: https://doi.org/10.1128/spectrum.05148-22

Interpretive Summary: For many bacteria, proteins that cause disease are transported from the bacteria into host cells during infection using a structure called the type III secretion system (T3SS). The proteins secreted are usually toxins or molecules that function to disrupt host cell functions and allow the bacteria to avoid the host defense response, grow, and promote disease. The system is composed of more than 20 proteins, some of which the functions are not currently known. HrpP is a bacterial protein previously shown to be secreted through the type III secretion delivery system into host cells however the role this protein plays in once inside the plant cell is unclear. This work shows that purified HrpP protein can induce plant cell death. Once inside the plant host cell HrpP interacts with a host plant protein to trigger a cascade of events that can suppress plant immunity, including alternating production of the plant hormones salicylic acid and jasmonate to promote bacterial infection. These findings describe activities for the bacterial T3SS substrate HrpP and provide a better understanding of the interactions of T3SS substrates with plant cells.

Technical Abstract: The bacterial plant pathogen Pseudomonas syringae deploys a type III secretion system (T3SS) to deliver effector proteins into plant cells to facilitate infection. However, few T3SS substrates have been studied for their direct interactions with plants. Here, for the first time, we show that P. syringae pv. tomato DC3000 (Pst DC3000) substrate HrpP protein induces host cell death, suppresses pattern-triggered immunity (PTI), and restores effector translocation ability of the hrpP mutant. The hrpP-transgenic Arabidopsis lines exhibited decreased PTI responses to flg22 and elf18, and enhanced disease susceptibility to Pst DC3000. Transcriptome analysis reveals that HrpP perception activates salicylic acid (SA) signaling while suppressing jasmonic acid (JA) signaling, which correlates with increased SA accumulation and decreased JA biosynthesis. Both yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BIFC) assays show that HrpP interacts with the Mitogen-activated protein kinase kinase 2 (MKK2) on the plant membrane and in the nucleus. HrpP1-119, rather than HrpP1-101, retains the ability to interact with MKK2 and suppress PTI in plants. In contrast, HrpP1-101 continues to cause cell death and electrolyte leakage. MKK2 silencing implies that MKK2 is not essential for HrpP-triggered cell death. Overall, our work highlights that rather than constituting the T3SS complex as a supramolecular component, the HrpP protein facilitates effector translocation and infection by manipulating plant immunity.