The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors
The jasmonic acid (JA) signaling pathway is one of the primary mechanisms that allow plants to respond to a variety of biotic and abiotic stressors. Within this pathway, the JAZ repressor proteins and the basic helix-loop-helix (bHLH) transcription factor MYC3 play a critical role. JA is a volatile...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2020.01139/full |
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| author | Samara Oña Chuquimarca Samara Oña Chuquimarca Sebastián Ayala-Ruano Sebastián Ayala-Ruano Jonas Goossens Jonas Goossens Laurens Pauwels Laurens Pauwels Alain Goossens Alain Goossens Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Miguel Ángel Méndez Miguel Ángel Méndez |
| author_facet | Samara Oña Chuquimarca Samara Oña Chuquimarca Sebastián Ayala-Ruano Sebastián Ayala-Ruano Jonas Goossens Jonas Goossens Laurens Pauwels Laurens Pauwels Alain Goossens Alain Goossens Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Miguel Ángel Méndez Miguel Ángel Méndez |
| author_sort | Samara Oña Chuquimarca |
| collection | DOAJ |
| description | The jasmonic acid (JA) signaling pathway is one of the primary mechanisms that allow plants to respond to a variety of biotic and abiotic stressors. Within this pathway, the JAZ repressor proteins and the basic helix-loop-helix (bHLH) transcription factor MYC3 play a critical role. JA is a volatile organic compound with an essential role in plant immunity. The increase in the concentration of JA leads to the decoupling of the JAZ repressor proteins and the bHLH transcription factor MYC3 causing the induction of genes of interest. The primary goal of this study was to identify the molecular basis of JAZ-MYC coupling. For this purpose, we modeled and validated 12 JAZ-MYC3 3D in silico structures and developed a molecular dynamics/machine learning pipeline to obtain two outcomes. First, we calculated the average free binding energy of JAZ-MYC3 complexes, which was predicted to be -10.94 +/-2.67 kJ/mol. Second, we predicted which ones should be the interface residues that make the predominant contribution to the free energy of binding (molecular hotspots). The predicted protein hotspots matched a conserved linear motif SL••FL•••R, which may have a crucial role during MYC3 recognition of JAZ proteins. As a proof of concept, we tested, both in silico and in vitro, the importance of this motif on PEAPOD (PPD) proteins, which also belong to the TIFY protein family, like the JAZ proteins, but cannot bind to MYC3. By mutating these proteins to match the SL••FL•••R motif, we could force PPDs to bind the MYC3 transcription factor. Taken together, modeling protein-protein interactions and using machine learning will help to find essential motifs and molecular mechanisms in the JA pathway. |
| first_indexed | 2024-12-12T08:51:11Z |
| format | Article |
| id | doaj.art-609e2c78711d48999ea134fee9a257dd |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-12T08:51:11Z |
| publishDate | 2020-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-609e2c78711d48999ea134fee9a257dd2022-12-22T00:30:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-08-011110.3389/fpls.2020.01139538511The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to StressorsSamara Oña Chuquimarca0Samara Oña Chuquimarca1Sebastián Ayala-Ruano2Sebastián Ayala-Ruano3Jonas Goossens4Jonas Goossens5Laurens Pauwels6Laurens Pauwels7Alain Goossens8Alain Goossens9Antonio Leon-Reyes10Antonio Leon-Reyes11Antonio Leon-Reyes12Antonio Leon-Reyes13Miguel Ángel Méndez14Miguel Ángel Méndez15Grupo de Química Computacional y Teórica, Departamento de Ingeniería Química, Universidad San Francisco de Quito USFQ, Campus Cumbayá, Quito, EcuadorInstituto de Simulación Computacional (ISC-USFQ), Universidad San Francisco de Quito USFQ, Quito, EcuadorGrupo de Química Computacional y Teórica, Departamento de Ingeniería Química, Universidad San Francisco de Quito USFQ, Campus Cumbayá, Quito, EcuadorInstituto de Simulación Computacional (ISC-USFQ), Universidad San Francisco de Quito USFQ, Quito, EcuadorDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumLaboratorio de Biotecnología Agrícola y de Alimentos, Ingeniería en Agronomía, Colegio de Ciencias e Ingenierías, Universidad San Francisco de Quito, Campus Cumbayá, Quito, EcuadorColegio de Ciencias Biológicas y Ambientales COCIBA, Instituto de Microbiología, Universidad San Francisco de Quito USFQ, Campus Cumbayá, Quito, EcuadorColegio de Ciencias Biológicas y Ambientales COCIBA, Instituto de Investigaciones Biológicas y Ambientales BIÓSFERA, Universidad San Francisco de Quito USFQ, Campus Cumbayá, Quito, EcuadorDepartment of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesGrupo de Química Computacional y Teórica, Departamento de Ingeniería Química, Universidad San Francisco de Quito USFQ, Campus Cumbayá, Quito, EcuadorInstituto de Simulación Computacional (ISC-USFQ), Universidad San Francisco de Quito USFQ, Quito, EcuadorThe jasmonic acid (JA) signaling pathway is one of the primary mechanisms that allow plants to respond to a variety of biotic and abiotic stressors. Within this pathway, the JAZ repressor proteins and the basic helix-loop-helix (bHLH) transcription factor MYC3 play a critical role. JA is a volatile organic compound with an essential role in plant immunity. The increase in the concentration of JA leads to the decoupling of the JAZ repressor proteins and the bHLH transcription factor MYC3 causing the induction of genes of interest. The primary goal of this study was to identify the molecular basis of JAZ-MYC coupling. For this purpose, we modeled and validated 12 JAZ-MYC3 3D in silico structures and developed a molecular dynamics/machine learning pipeline to obtain two outcomes. First, we calculated the average free binding energy of JAZ-MYC3 complexes, which was predicted to be -10.94 +/-2.67 kJ/mol. Second, we predicted which ones should be the interface residues that make the predominant contribution to the free energy of binding (molecular hotspots). The predicted protein hotspots matched a conserved linear motif SL••FL•••R, which may have a crucial role during MYC3 recognition of JAZ proteins. As a proof of concept, we tested, both in silico and in vitro, the importance of this motif on PEAPOD (PPD) proteins, which also belong to the TIFY protein family, like the JAZ proteins, but cannot bind to MYC3. By mutating these proteins to match the SL••FL•••R motif, we could force PPDs to bind the MYC3 transcription factor. Taken together, modeling protein-protein interactions and using machine learning will help to find essential motifs and molecular mechanisms in the JA pathway.https://www.frontiersin.org/article/10.3389/fpls.2020.01139/fullJAZMYCplant defensemachine learningmodelingcomputer |
| spellingShingle | Samara Oña Chuquimarca Samara Oña Chuquimarca Sebastián Ayala-Ruano Sebastián Ayala-Ruano Jonas Goossens Jonas Goossens Laurens Pauwels Laurens Pauwels Alain Goossens Alain Goossens Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Antonio Leon-Reyes Miguel Ángel Méndez Miguel Ángel Méndez The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors Frontiers in Plant Science JAZ MYC plant defense machine learning modeling computer |
| title | The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors |
| title_full | The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors |
| title_fullStr | The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors |
| title_full_unstemmed | The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors |
| title_short | The Molecular Basis of JAZ-MYC Coupling, a Protein-Protein Interface Essential for Plant Response to Stressors |
| title_sort | molecular basis of jaz myc coupling a protein protein interface essential for plant response to stressors |
| topic | JAZ MYC plant defense machine learning modeling computer |
| url | https://www.frontiersin.org/article/10.3389/fpls.2020.01139/full |
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