The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense
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 bi...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-08-01
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| Series: | Cells |
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| Online Access: | https://www.mdpi.com/2073-4409/12/16/2110 |
| _version_ | 1827730127221424128 |
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| author | Junichi Inaba Bo Min Kim Yan Zhao Andrew M. Jansen Wei Wei |
| author_facet | Junichi Inaba Bo Min Kim Yan Zhao Andrew M. Jansen Wei Wei |
| author_sort | Junichi Inaba |
| collection | DOAJ |
| description | 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 colocalization 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 intracellular 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. |
| first_indexed | 2024-03-11T00:02:45Z |
| format | Article |
| id | doaj.art-c90441aec4dd4e9cb5da66358102c425 |
| institution | Directory Open Access Journal |
| issn | 2073-4409 |
| language | English |
| last_indexed | 2024-03-11T00:02:45Z |
| publishDate | 2023-08-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cells |
| spelling | doaj.art-c90441aec4dd4e9cb5da66358102c4252023-11-19T00:37:41ZengMDPI AGCells2073-44092023-08-011216211010.3390/cells12162110The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant DefenseJunichi Inaba0Bo Min Kim1Yan Zhao2Andrew M. Jansen3Wei Wei4Molecular Plant Pathology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USAMolecular Plant Pathology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USAMolecular Plant Pathology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USAElectron and Confocal Microscopy Unit, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USAMolecular Plant Pathology Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USAPhytoplasmas 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 colocalization 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 intracellular 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.https://www.mdpi.com/2073-4409/12/16/2110endoplasmic reticulum (ER)ER stressunfolded protein response (UPR)phytoplasmaER-resident proteins |
| spellingShingle | Junichi Inaba Bo Min Kim Yan Zhao Andrew M. Jansen Wei Wei The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense Cells endoplasmic reticulum (ER) ER stress unfolded protein response (UPR) phytoplasma ER-resident proteins |
| title | The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense |
| title_full | The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense |
| title_fullStr | The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense |
| title_full_unstemmed | The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense |
| title_short | The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense |
| title_sort | endoplasmic reticulum is a key battleground between phytoplasma aggression and host plant defense |
| topic | endoplasmic reticulum (ER) ER stress unfolded protein response (UPR) phytoplasma ER-resident proteins |
| url | https://www.mdpi.com/2073-4409/12/16/2110 |
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