Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants
Plasmodiophora brassicae is a devastating obligate, intracellular, biotrophic pathogen that causes clubroot disease in crucifer plants. Disease progression is regulated by effector proteins secreted by P. brassicae. Twelve P. brassicae putative effectors (PbPEs), expressed at various stages of disea...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.651279/full |
| _version_ | 1819009050084376576 |
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| author | Md Musharaf Hossain Edel Pérez-López Christopher D. Todd Yangdou Wei Peta C. Bonham-Smith |
| author_facet | Md Musharaf Hossain Edel Pérez-López Christopher D. Todd Yangdou Wei Peta C. Bonham-Smith |
| author_sort | Md Musharaf Hossain |
| collection | DOAJ |
| description | Plasmodiophora brassicae is a devastating obligate, intracellular, biotrophic pathogen that causes clubroot disease in crucifer plants. Disease progression is regulated by effector proteins secreted by P. brassicae. Twelve P. brassicae putative effectors (PbPEs), expressed at various stages of disease development [0, 2, 5, 7, 14, 21, and 28 days post inoculation (DPI)] in Arabidopsis and localizing to the plant endomembrane system, were studied for their roles in pathogenesis. Of the 12 PbPEs, seven showed an inhibitory effect on programmed cell death (PCD) as triggered by the PCD inducers, PiINF1 (Phytophthora infestans Infestin 1) and PiNPP1 (P. infestans necrosis causing protein). Showing the strongest level of PCD suppression, PbPE15, a member of the 2-oxoglutarate (2OG) and Fe (II)-dependent oxygenase superfamily and with gene expression during later stages of infection, appears to have a role in tumorigenesis as well as defense signaling in plants. PbPE13 produced an enhanced PiINF1-induced PCD response. Transient expression, in Nicotiana benthamiana leaves of these PbPEs minus the signal peptide (SP) (ΔspPbPEGFPs), showed localization to the endomembrane system, targeting the endoplasmic reticulum (ER), Golgi bodies and nucleo-cytoplasm, suggesting roles in manipulating plant cell secretion and vesicle trafficking. ΔspPbPE13GFP localized to plasma membrane (PM) lipid rafts with an association to plasmodesmata, suggesting a role at the cell-to-cell communication junction. Membrane relocalization of ΔspPbPE13GFP, triggered by flagellin N-terminus of Pseudomonas aeruginosa (flg22 – known to elicit a PAMP triggered immune response in plants), supports its involvement in raft-mediated immune signaling. This study is an important step in deciphering P. brassicae effector roles in the disruption of plant immunity to clubroot disease. |
| first_indexed | 2024-12-21T00:50:12Z |
| format | Article |
| id | doaj.art-86b3b6cd18c741b0b909f9f39d794e52 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-21T00:50:12Z |
| publishDate | 2021-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-86b3b6cd18c741b0b909f9f39d794e522022-12-21T19:21:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.651279651279Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in PlantsMd Musharaf Hossain0Edel Pérez-López1Christopher D. Todd2Yangdou Wei3Peta C. Bonham-Smith4Department of Biology, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Plant Sciences, Laval University, CRIV, Quebec City, QC, CanadaDepartment of Biology, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Biology, University of Saskatchewan, Saskatoon, SK, CanadaDepartment of Biology, University of Saskatchewan, Saskatoon, SK, CanadaPlasmodiophora brassicae is a devastating obligate, intracellular, biotrophic pathogen that causes clubroot disease in crucifer plants. Disease progression is regulated by effector proteins secreted by P. brassicae. Twelve P. brassicae putative effectors (PbPEs), expressed at various stages of disease development [0, 2, 5, 7, 14, 21, and 28 days post inoculation (DPI)] in Arabidopsis and localizing to the plant endomembrane system, were studied for their roles in pathogenesis. Of the 12 PbPEs, seven showed an inhibitory effect on programmed cell death (PCD) as triggered by the PCD inducers, PiINF1 (Phytophthora infestans Infestin 1) and PiNPP1 (P. infestans necrosis causing protein). Showing the strongest level of PCD suppression, PbPE15, a member of the 2-oxoglutarate (2OG) and Fe (II)-dependent oxygenase superfamily and with gene expression during later stages of infection, appears to have a role in tumorigenesis as well as defense signaling in plants. PbPE13 produced an enhanced PiINF1-induced PCD response. Transient expression, in Nicotiana benthamiana leaves of these PbPEs minus the signal peptide (SP) (ΔspPbPEGFPs), showed localization to the endomembrane system, targeting the endoplasmic reticulum (ER), Golgi bodies and nucleo-cytoplasm, suggesting roles in manipulating plant cell secretion and vesicle trafficking. ΔspPbPE13GFP localized to plasma membrane (PM) lipid rafts with an association to plasmodesmata, suggesting a role at the cell-to-cell communication junction. Membrane relocalization of ΔspPbPE13GFP, triggered by flagellin N-terminus of Pseudomonas aeruginosa (flg22 – known to elicit a PAMP triggered immune response in plants), supports its involvement in raft-mediated immune signaling. This study is an important step in deciphering P. brassicae effector roles in the disruption of plant immunity to clubroot disease.https://www.frontiersin.org/articles/10.3389/fmicb.2021.651279/fullPlasmodiophora brassicaeeffectorsendomembraneprogrammed cell deathpathogen-associated molecular pattern |
| spellingShingle | Md Musharaf Hossain Edel Pérez-López Christopher D. Todd Yangdou Wei Peta C. Bonham-Smith Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants Frontiers in Microbiology Plasmodiophora brassicae effectors endomembrane programmed cell death pathogen-associated molecular pattern |
| title | Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants |
| title_full | Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants |
| title_fullStr | Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants |
| title_full_unstemmed | Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants |
| title_short | Endomembrane-Targeting Plasmodiophora brassicae Effectors Modulate PAMP Triggered Immune Responses in Plants |
| title_sort | endomembrane targeting plasmodiophora brassicae effectors modulate pamp triggered immune responses in plants |
| topic | Plasmodiophora brassicae effectors endomembrane programmed cell death pathogen-associated molecular pattern |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.651279/full |
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