Dataset Information

In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from Brachypodium distachyon.

ABSTRACT: 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 Ca²⁺. 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 Brachypodium distachyon (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 Ca²⁺ 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.

SUBMITTER: Kwiatkowski M

PROVIDER: S-EPMC8431786 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i>.

Kwiatkowski Mateusz M Wong Aloysius A Kozakiewicz-Piekarz Anna A Gehring Christoph C Jaworski Krzysztof K

International journal of molecular sciences 20210906 17

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 ...[more]

PMID: 34502563

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Project description:BackgroundThe local environment plays a major role in the spatial distribution of plant populations. Natural plant populations have an extremely poor displacing capacity, so their continued survival in a given environment depends on how well they adapt to local pedoclimatic conditions. Genomic tools can be used to identify adaptive traits at a DNA level and to further our understanding of evolutionary processes. Here we report the use of genotyping-by-sequencing on local groups of the sequenced monocot model species Brachypodium distachyon. Exploiting population genetics, landscape genomics and genome wide association studies, we evaluate B. distachyon role as a natural probe for identifying genomic loci involved in environmental adaptation.ResultsBrachypodium distachyon individuals were sampled in nine locations with different ecologies and characterized with 16,697 SNPs. Variations in sequencing depth showed consistent patterns at 8,072 genomic bins, which were significantly enriched in transposable elements. We investigated the structuration and diversity of this collection, and exploited climatic data to identify loci with adaptive significance through i) two different approaches for genome wide association analyses considering climatic variation, ii) an outlier loci approach, and iii) a canonical correlation analysis on differentially sequenced bins. A linkage disequilibrium-corrected Bonferroni method was applied to filter associations. The two association methods jointly identified a set of 15 genes significantly related to environmental adaptation. The outlier loci approach revealed that 5.7% of the loci analysed were under selection. The canonical correlation analysis showed that the distribution of some differentially sequenced regions was associated to environmental variation.ConclusionsWe show that the multi-faceted approach used here targeted different components of B. distachyon adaptive variation, and may lead to the discovery of genes related to environmental adaptation in natural populations. Its application to a model species with a fully sequenced genome is a modular strategy that enables the stratification of biological material and thus improves our knowledge of the functional loci determining adaptation in near-crop species. When coupled with population genetics and measures of genomic structuration, methods coming from genome wide association studies may lead to the exploitation of model species as natural probes to identify loci related to environmental adaptation.

Project description:BackgroundBrassinosteroids (BRs) are steroidal phytohormones that are involved in diverse physiological processes and affect many important traits, such as plant stature, stress tolerance, leaf angle, fertility, and grain filling. BR signaling and biosynthetic pathways have been studied in various plants, such as the model dicot Arabidopsis thaliana; however, relatively little is known about these pathways in monocots.ResultsTo characterize BR-related processes in the model grass Brachypodium distachyon, we studied the response of these plants to the specific BR biosynthesis inhibitor, propiconazole (Pcz). We found that treatments with Pcz produced a dwarf phenotype in B. distachyon seedlings, similar to that observed in Pcz-treated Arabidopsis plants and in characterized BR-deficient mutants. Through bioinformatics analysis, we identified a list of putative homologs of genes known to be involved in BR biosynthesis and signaling in Arabidopsis, such as DWF4, BR6OX2, CPD, BRI1, and BIN2. Evaluating the response of these genes to Pcz treatments revealed that candidates for BdDWF4, BR6OX2 and, CPD were under feedback regulation. In addition, Arabidopsis plants heterologously expressing BdDWF4 displayed tall statures and elongated petioles, as would be expected in plants with elevated levels of BRs. Moreover, heterologous expression of BdBIN2 in Arabidopsis resulted in dwarfism, suggesting that BdBIN2 functions as a negative regulator of BR signaling. However, the dwarf phenotypes of Arabidopsis bri1-5, a weak BRI1 mutant allele, were not complemented by overexpression of BdBRI1, indicating that BdBRI1 and BRI1 are not functionally equivalent.ConclusionWe identified components of the BR biosynthetic and signaling pathways in Brachypodium, and provided examples of both similarities and differences in the BR biology of these two plants. Our results suggest a framework for understanding BR biology in monocot crop plants such as Zea mays (maize) and Oryza sativa (rice).

Dataset Information

In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from Brachypodium distachyon.

Publications

In Search of Monocot Phosphodiesterases: Identification of a Calmodulin Stimulated Phosphodiesterase from <i>Brachypodium distachyon</i>.

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