The endoplasmic reticulum is a key battleground between phytoplasma aggression and host plant defense

Authors: Inaba, Junichi; KIM, BO MIN - Orise Fellow; Zhao, Yan; Jansen, Michael - Andrew; Wei, Wei

Submitted to: Cells
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/19/2023
Publication Date: 8/21/2023
Citation: Inaba, J., Kim, B., Zhao, Y., Jansen, M.A., Wei, W. 2023. The endoplasmic reticulum is a key battleground between phytoplasma aggression and host plant defense. Cells. https://doi.org/10.3390/cells12162110.
DOI: https://doi.org/10.3390/cells12162110

Interpretive Summary: Phytoplasmas are small bacteria that reside within hosts and rely on the host's nutrients for survival and replication. The endoplasmic reticulum (ER) is a key player in multiple cellular processes and a prime target for infection and proliferation of numerous intracellular pathogens. In this study, ARS scientists in Beltsville, Maryland investigated the impacts of potato purple top (PPT) phytoplasma infection on the ER of tomato plants, revealing that phytoplasma infection disrupts the equilibrium of the ER in tomato plants, leading to an abnormal accumulation of ER-resident proteins and morphological changes in the ER network. This discovery establishes a potential association between ER stress, induction of the unfolded protein response (UPR), and phytoplasma infection and colonization. The ER acts like a battleground where phytoplasmas attempt to exploit the plant's resources, while the plant counters by activating defense mechanisms. Gaining a deeper understanding of these cellular interactions, especially within the ER, can aid researchers in developing novel approaches to manage phytoplasma diseases in plants. The insights from this study hold significance for researchers and scientists engaged in plant pathology, molecular biology, and crop protection. Specifically, experts investigating phytoplasma diseases in plants and exploring plant-pathogen interactions will find this research highly valuable.

Technical Abstract: Phytoplasmas are intracellular plant pathogens that heavily rely on host cell nutrients for survival and propagation due to their limited ability to synthesize essential substrates. The endoplasmic reticulum (ER), which plays a vital role in various cellular processes, including lipid and protein biosynthesis, is an attractive target for numerous intracellular pathogens to exploit. This study investigated the impact of potato purple top (PPT) phytoplasma infection on the ER in tomato plants. Abnormal accumulation of ER-resident proteins, disrupted ER network structures and formation of protein aggregates in the phloem were observed using confocal microscopy and transmission electron microscopy, indicating a phytoplasma infection-induced disturbance in ER homeostasis. The co-localization of phytoplasmas with the accumulated ER-resident proteins suggests an association between ER stress, unfolded protein response (UPR) induction, and phytoplasma infection and colonization, with the ER stress response likely contributing to the host plant's defense mechanisms. Quantitative real-time PCR revealed a negative correlation between ER stress/UPR activation and PPT phytoplasma titer, implying the involvement of UPR in curbing phytoplasma proliferation. Inducing ER stress and activating the UPR pathway effectively decreased phytoplasma titer while suppressing the ER-resident protein, binding immunoglobulin protein (BiP) increased phytoplasma titer. These results highlight the ER as an intra-cellular battleground where phytoplasmas exploit host components for survival and multiplication, while host plants deploy defense mechanisms to counteract the invasion. Understanding the intricate interactions between phytoplasmas and plant hosts at the subcellular level, particularly within the ER, provides valuable insights for developing new strategies to control phytoplasma diseases.