Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana
Plasma membranes are heterogeneous and contain multiple functional nanodomains. Although several signaling proteins have been shown to function by moving into or out of nanodomains, little is known regarding the effects of environmental cues on nanodomain organization. In this study, we investigated...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-05-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.897594/full |
| _version_ | 1828345126293864448 |
|---|---|
| author | Changwen Xu Changwen Xu Sammar Abbas Sammar Abbas Hongping Qian Hongping Qian Meng Yu Xi Zhang Xi Zhang Xiaojuan Li Xiaojuan Li Yaning Cui Yaning Cui Jinxing Lin Jinxing Lin |
| author_facet | Changwen Xu Changwen Xu Sammar Abbas Sammar Abbas Hongping Qian Hongping Qian Meng Yu Xi Zhang Xi Zhang Xiaojuan Li Xiaojuan Li Yaning Cui Yaning Cui Jinxing Lin Jinxing Lin |
| author_sort | Changwen Xu |
| collection | DOAJ |
| description | Plasma membranes are heterogeneous and contain multiple functional nanodomains. Although several signaling proteins have been shown to function by moving into or out of nanodomains, little is known regarding the effects of environmental cues on nanodomain organization. In this study, we investigated the heterogeneity and organization of distinct nanodomains, including those containing Arabidopsis thaliana flotillin-1 (AtFlot1) and hypersensitive induced reaction-1 proteins (AtHIR1), in response to biotic and abiotic stress. Variable-angle total internal reflection fluorescence microscopy coupled with single-particle tracking (SPT) revealed that AtFlot1 and AtHIR1 exhibit different lateral dynamics and inhabit different types of nanodomains. Furthermore, via SPT and fluorescence correlation spectroscopy, we observed lower density and intensity of AtFlot1 fluorescence in the plasma membrane after biotic stress. In contrast, the density and intensity of signal indicating AtHIR1 markedly increased in response to biotic stress. In response to abiotic stress, the density and intensity of both AtFlot1 and AtHIR1 signals decreased significantly. Importantly, SPT coupled with fluorescence recovery after photobleaching revealed that biotic and abiotic stress can regulate the dynamics of AtFlot1; however, only the abiotic stress can regulate AtHIR1 dynamics. Taken together, these findings suggest that a plethora of highly distinct nanodomains coexist in the plasma membrane (PM) and that different nanodomains may perform distinct functions in response to biotic and abiotic stresses. These phenomena may be explained by the spatial clustering of plasma membrane proteins with their associated signaling components within dedicated PM nanodomains. |
| first_indexed | 2024-04-14T00:07:05Z |
| format | Article |
| id | doaj.art-bf22c41d6d11457a9aaf89d2fd80c208 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-14T00:07:05Z |
| publishDate | 2022-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-bf22c41d6d11457a9aaf89d2fd80c2082022-12-22T02:23:29ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-05-011310.3389/fpls.2022.897594897594Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thalianaChangwen Xu0Changwen Xu1Sammar Abbas2Sammar Abbas3Hongping Qian4Hongping Qian5Meng Yu6Xi Zhang7Xi Zhang8Xiaojuan Li9Xiaojuan Li10Yaning Cui11Yaning Cui12Jinxing Lin13Jinxing Lin14National Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaCollege of Life Sciences, Hebei Agricultural University, Baoding, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaNational Engineering Research Center of Tree Breeding and Ecological Restoration, Beijing Forestry University, Beijing, ChinaCollege of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, ChinaPlasma membranes are heterogeneous and contain multiple functional nanodomains. Although several signaling proteins have been shown to function by moving into or out of nanodomains, little is known regarding the effects of environmental cues on nanodomain organization. In this study, we investigated the heterogeneity and organization of distinct nanodomains, including those containing Arabidopsis thaliana flotillin-1 (AtFlot1) and hypersensitive induced reaction-1 proteins (AtHIR1), in response to biotic and abiotic stress. Variable-angle total internal reflection fluorescence microscopy coupled with single-particle tracking (SPT) revealed that AtFlot1 and AtHIR1 exhibit different lateral dynamics and inhabit different types of nanodomains. Furthermore, via SPT and fluorescence correlation spectroscopy, we observed lower density and intensity of AtFlot1 fluorescence in the plasma membrane after biotic stress. In contrast, the density and intensity of signal indicating AtHIR1 markedly increased in response to biotic stress. In response to abiotic stress, the density and intensity of both AtFlot1 and AtHIR1 signals decreased significantly. Importantly, SPT coupled with fluorescence recovery after photobleaching revealed that biotic and abiotic stress can regulate the dynamics of AtFlot1; however, only the abiotic stress can regulate AtHIR1 dynamics. Taken together, these findings suggest that a plethora of highly distinct nanodomains coexist in the plasma membrane (PM) and that different nanodomains may perform distinct functions in response to biotic and abiotic stresses. These phenomena may be explained by the spatial clustering of plasma membrane proteins with their associated signaling components within dedicated PM nanodomains.https://www.frontiersin.org/articles/10.3389/fpls.2022.897594/fullVA-TIRFMnanodomaindynamicsbiotic and abiotic stressesflotillin-1hypersensitive induced reaction-1 |
| spellingShingle | Changwen Xu Changwen Xu Sammar Abbas Sammar Abbas Hongping Qian Hongping Qian Meng Yu Xi Zhang Xi Zhang Xiaojuan Li Xiaojuan Li Yaning Cui Yaning Cui Jinxing Lin Jinxing Lin Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana Frontiers in Plant Science VA-TIRFM nanodomain dynamics biotic and abiotic stresses flotillin-1 hypersensitive induced reaction-1 |
| title | Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana |
| title_full | Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana |
| title_fullStr | Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana |
| title_full_unstemmed | Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana |
| title_short | Environmental Cues Contribute to Dynamic Plasma Membrane Organization of Nanodomains Containing Flotillin-1 and Hypersensitive Induced Reaction-1 Proteins in Arabidopsis thaliana |
| title_sort | environmental cues contribute to dynamic plasma membrane organization of nanodomains containing flotillin 1 and hypersensitive induced reaction 1 proteins in arabidopsis thaliana |
| topic | VA-TIRFM nanodomain dynamics biotic and abiotic stresses flotillin-1 hypersensitive induced reaction-1 |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.897594/full |
| work_keys_str_mv | AT changwenxu environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT changwenxu environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT sammarabbas environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT sammarabbas environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT hongpingqian environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT hongpingqian environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT mengyu environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT xizhang environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT xizhang environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT xiaojuanli environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT xiaojuanli environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT yaningcui environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT yaningcui environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT jinxinglin environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana AT jinxinglin environmentalcuescontributetodynamicplasmamembraneorganizationofnanodomainscontainingflotillin1andhypersensitiveinducedreaction1proteinsinarabidopsisthaliana |