In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i>
In plants, rapid and reversible biological responses to environmental cues may require complex cellular reprograming. This is enabled by signaling molecules such as the cyclic nucleotide monophosphates (cNMPs) cAMP and cGMP, as well as Ca<sup>2+</sup>. While the roles and synthesis of cA...
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MDPI AG
2021-09-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/17/9654 |
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| author | Mateusz Kwiatkowski Aloysius Wong Anna Kozakiewicz-Piekarz Christoph Gehring Krzysztof Jaworski |
| author_facet | Mateusz Kwiatkowski Aloysius Wong Anna Kozakiewicz-Piekarz Christoph Gehring Krzysztof Jaworski |
| author_sort | Mateusz Kwiatkowski |
| collection | DOAJ |
| description | In plants, rapid and reversible biological responses to environmental cues may require complex cellular reprograming. This is enabled by signaling molecules such as the cyclic nucleotide monophosphates (cNMPs) cAMP and cGMP, as well as Ca<sup>2+</sup>. While the roles and synthesis of cAMP and cGMP in plants are increasingly well-characterized, the “off signal” afforded by cNMP-degrading enzymes, the phosphodiesterases (PDEs), is, however, poorly understood, particularly so in monocots. Here, we identified a candidate PDE from the monocot <i>Brachypodium distachyon</i> (BDPDE1) and showed that it can hydrolyze cNMPs to 5′NMPs but with a preference for cAMP over cGMP in vitro. Notably, the PDE activity was significantly enhanced by Ca<sup>2+</sup> only in the presence of calmodulin (CaM), which interacts with BDPDE1, most likely at a predicted CaM-binding site. Finally, based on our biochemical, mutagenesis and structural analyses, we constructed a comprehensive amino acid consensus sequence extracted from the catalytic centers of annotated and/or experimentally validated PDEs across species to enable a broad application of this search motif for the identification of similar active sites in eukaryotes and prokaryotes. |
| first_indexed | 2024-03-10T08:10:11Z |
| format | Article |
| id | doaj.art-d80d35c7834a4574bf449b6506172a07 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T08:10:11Z |
| publishDate | 2021-09-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-d80d35c7834a4574bf449b6506172a072023-11-22T10:46:54ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-09-012217965410.3390/ijms22179654In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i>Mateusz Kwiatkowski0Aloysius Wong1Anna Kozakiewicz-Piekarz2Christoph Gehring3Krzysztof Jaworski4Department of Plant Physiology and Biotechnology, Nicolaus Copernicus University, Lwowska St. 1, 87-100 Torun, PolandDepartment of Biology, College of Science and Technology, Wenzhou-Kean University, 88 Daxue Road, Ouhai, Wenzhou 325060, ChinaDepartment of Biomedical and Polymer Chemistry, Faculty of Chemistry, Nicolaus Copernicus University, Gagarina St. 7, 87-100 Torun, PolandDepartment of Chemistry, Biology and Biotechnology, University of Perugia, Borgo XX giugno, 74, 06121 Perugia, ItalyDepartment of Plant Physiology and Biotechnology, Nicolaus Copernicus University, Lwowska St. 1, 87-100 Torun, PolandIn plants, rapid and reversible biological responses to environmental cues may require complex cellular reprograming. This is enabled by signaling molecules such as the cyclic nucleotide monophosphates (cNMPs) cAMP and cGMP, as well as Ca<sup>2+</sup>. While the roles and synthesis of cAMP and cGMP in plants are increasingly well-characterized, the “off signal” afforded by cNMP-degrading enzymes, the phosphodiesterases (PDEs), is, however, poorly understood, particularly so in monocots. Here, we identified a candidate PDE from the monocot <i>Brachypodium distachyon</i> (BDPDE1) and showed that it can hydrolyze cNMPs to 5′NMPs but with a preference for cAMP over cGMP in vitro. Notably, the PDE activity was significantly enhanced by Ca<sup>2+</sup> only in the presence of calmodulin (CaM), which interacts with BDPDE1, most likely at a predicted CaM-binding site. Finally, based on our biochemical, mutagenesis and structural analyses, we constructed a comprehensive amino acid consensus sequence extracted from the catalytic centers of annotated and/or experimentally validated PDEs across species to enable a broad application of this search motif for the identification of similar active sites in eukaryotes and prokaryotes.https://www.mdpi.com/1422-0067/22/17/9654phosphodiesterase (PDE)cAMPcGMPcalmodulin (CaM)calcium ionsprotein–protein interactions |
| spellingShingle | Mateusz Kwiatkowski Aloysius Wong Anna Kozakiewicz-Piekarz Christoph Gehring Krzysztof Jaworski In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> International Journal of Molecular Sciences phosphodiesterase (PDE) cAMP cGMP calmodulin (CaM) calcium ions protein–protein interactions |
| title | In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> |
| title_full | In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> |
| title_fullStr | In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> |
| title_full_unstemmed | In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> |
| title_short | In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i> |
| title_sort | in search of monocot phosphodiesterases identification of a calmodulin stimulated phosphodiesterase from i brachypodium distachyon i |
| topic | phosphodiesterase (PDE) cAMP cGMP calmodulin (CaM) calcium ions protein–protein interactions |
| url | https://www.mdpi.com/1422-0067/22/17/9654 |
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