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Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells

View ORCID ProfileCesar L Cuevas-Velazquez, View ORCID ProfileTamara Vellosillo, View ORCID ProfileKarina Guadalupe, View ORCID ProfileH Broder Schmidt, View ORCID ProfileFeng Yu, View ORCID ProfileDavid Moses, View ORCID ProfileJennifer AN Brophy, View ORCID ProfileDante Cosio-Acosta, View ORCID ProfileAlakananda Das, Lingxin Wang, View ORCID ProfileAlexander M Jones, View ORCID ProfileAlejandra A Covarrubias, View ORCID ProfileShahar Sukenik, View ORCID ProfileJosé R Dinneny
doi: https://doi.org/10.1101/2021.02.17.431712
Cesar L Cuevas-Velazquez
1Department of Biology, Stanford University, Stanford, CA, 94305, USA
2Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA
3Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mor., 62210 Mexico
4Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, Ciudad de México, 04510, Mexico
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  • ORCID record for Cesar L Cuevas-Velazquez
  • For correspondence: cuevas@quimica.unam.mx alejandra.covarrubias@mail.ibt.unam.mx ssukenik@ucmerced.edu dinneny@stanford.edu
Tamara Vellosillo
1Department of Biology, Stanford University, Stanford, CA, 94305, USA
2Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA
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Karina Guadalupe
5Center for Cellular and Biomolecular Machines (CCBM), University of California, Merced, CA, 95343, USA
6Chemistry and Chemical Biology Program, University of California, Merced, CA, 95343, USA
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H Broder Schmidt
7Department of Biochemistry, Stanford University School of Medicine, Stanford, CA, 94305, USA
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Feng Yu
5Center for Cellular and Biomolecular Machines (CCBM), University of California, Merced, CA, 95343, USA
8Quantitative Systems Biology Program, University of California, Merced, CA, 95343, USA
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David Moses
5Center for Cellular and Biomolecular Machines (CCBM), University of California, Merced, CA, 95343, USA
6Chemistry and Chemical Biology Program, University of California, Merced, CA, 95343, USA
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Jennifer AN Brophy
1Department of Biology, Stanford University, Stanford, CA, 94305, USA
2Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA
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Dante Cosio-Acosta
3Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mor., 62210 Mexico
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Alakananda Das
9Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA, 94305, USA
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Lingxin Wang
9Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA, 94305, USA
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Alexander M Jones
10Sainsbury Laboratory, Cambridge University, Cambridge, CB2 1LR, UK
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Alejandra A Covarrubias
3Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mor., 62210 Mexico
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  • For correspondence: cuevas@quimica.unam.mx alejandra.covarrubias@mail.ibt.unam.mx ssukenik@ucmerced.edu dinneny@stanford.edu
Shahar Sukenik
5Center for Cellular and Biomolecular Machines (CCBM), University of California, Merced, CA, 95343, USA
6Chemistry and Chemical Biology Program, University of California, Merced, CA, 95343, USA
8Quantitative Systems Biology Program, University of California, Merced, CA, 95343, USA
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  • For correspondence: cuevas@quimica.unam.mx alejandra.covarrubias@mail.ibt.unam.mx ssukenik@ucmerced.edu dinneny@stanford.edu
José R Dinneny
1Department of Biology, Stanford University, Stanford, CA, 94305, USA
2Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, 94305, USA
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  • For correspondence: cuevas@quimica.unam.mx alejandra.covarrubias@mail.ibt.unam.mx ssukenik@ucmerced.edu dinneny@stanford.edu
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SUMMARY

Cell homeostasis is perturbed when dramatic shifts in the external environment cause the physical-chemical properties inside the cell to change. Methods that dynamically monitor these intracellular effects are currently lacking. Here, we leveraged the environmental sensitivity and structural plasticity of intrinsically disordered regions (IDRs) to develop a FRET biosensor capable of monitoring rapid intracellular changes caused by osmotic stress. The biosensor, named SED1, utilizes the Arabidopsis intrinsically disordered AtLEA4-5 protein expressed in plants under water deficit. Computational modeling and in vitro studies reveal that SED1 is highly sensitive to macromolecular crowding. SED1 exhibits large and near-linear osmolarity-dependent changes in FRET inside living bacteria, yeast, plant, and human cells, demonstrating the broad utility of this tool for studying water-associated stress. This study demonstrates the remarkable ability of IDRs to sense the cellular environment across the tree of life and provides a blueprint for their use in environmentally-responsive molecular tools.

Competing Interest Statement

The authors have declared no competing interest.

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Posted February 18, 2021.
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Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells
Cesar L Cuevas-Velazquez, Tamara Vellosillo, Karina Guadalupe, H Broder Schmidt, Feng Yu, David Moses, Jennifer AN Brophy, Dante Cosio-Acosta, Alakananda Das, Lingxin Wang, Alexander M Jones, Alejandra A Covarrubias, Shahar Sukenik, José R Dinneny
bioRxiv 2021.02.17.431712; doi: https://doi.org/10.1101/2021.02.17.431712
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Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells
Cesar L Cuevas-Velazquez, Tamara Vellosillo, Karina Guadalupe, H Broder Schmidt, Feng Yu, David Moses, Jennifer AN Brophy, Dante Cosio-Acosta, Alakananda Das, Lingxin Wang, Alexander M Jones, Alejandra A Covarrubias, Shahar Sukenik, José R Dinneny
bioRxiv 2021.02.17.431712; doi: https://doi.org/10.1101/2021.02.17.431712

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