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Neuronal calmodulin levels are controlled by CAMTA transcription factors.

ABSTRACT: The ubiquitous Ca2+ sensor calmodulin (CaM) binds and regulates many proteins, including ion channels, CaM kinases, and calcineurin, according to Ca2+-CaM levels. What regulates neuronal CaM levels, is, however, unclear. CaM-binding transcription activators (CAMTAs) are ancient proteins expressed broadly in nervous systems and whose loss confers pleiotropic behavioral defects in flies, mice, and humans. Using Caenorhabditis elegans and Drosophila, we show that CAMTAs control neuronal CaM levels. The behavioral and neuronal Ca2+ signaling defects in mutants lacking camt-1, the sole C. elegans CAMTA, can be rescued by supplementing neuronal CaM. CAMT-1 binds multiple sites in the CaM promoter and deleting these sites phenocopies camt-1. Our data suggest CAMTAs mediate a conserved and general mechanism that controls neuronal CaM levels, thereby regulating Ca2+ signaling, physiology, and behavior.

SUBMITTER: Vuong-Brender TT

PROVIDER: S-EPMC8428840 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Neuronal calmodulin levels are controlled by CAMTA transcription factors.

Vuong-Brender Thanh Thi TT Flynn Sean S Vallis Yvonne Y Sönmez Saliha E SE de Bono Mario M

eLife 20210909

The ubiquitous Ca2+ sensor calmodulin (CaM) binds and regulates many proteins, including ion channels, CaM kinases, and calcineurin, according to Ca2+-CaM levels. What regulates neuronal CaM levels, is, however, unclear. CaM-binding transcription activators (CAMTAs) are ancient proteins expressed broadly in nervous systems and whose loss confers pleiotropic behavioral defects in flies, mice, and humans. Using Caenorhabditis elegans and Drosophila, we show that ...[more]

PMID: 34499028

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Project description:BackgroundFruit ripening is an intricate developmental process driven by a highly coordinated action of complex hormonal networks. Ethylene is considered as the main phytohormone that regulates the ripening of climacteric fruits. Concomitantly, several ethylene-responsive transcription factors (TFs) are pivotal components of the regulatory network underlying fruit ripening. Calmodulin-binding transcription activator (CAMTA) is one such ethylene-induced TF implicated in various stress and plant developmental processes.ResultsOur comprehensive analysis of the CAMTA gene family in Durio zibethinus (durian, Dz) identified 10 CAMTAs with conserved domains. Phylogenetic analysis of DzCAMTAs, positioned DzCAMTA3 with its tomato ortholog that has already been validated for its role in the fruit ripening process through ethylene-mediated signaling. Furthermore, the transcriptome-wide analysis revealed DzCAMTA3 and DzCAMTA8 as the highest expressing durian CAMTA genes. These two DzCAMTAs possessed a distinct ripening-associated expression pattern during post-harvest ripening in Monthong, a durian cultivar native to Thailand. The expression profiling of DzCAMTA3 and DzCAMTA8 under natural ripening conditions and ethylene-induced/delayed ripening conditions substantiated their roles as ethylene-induced transcriptional activators of ripening. Similarly, auxin-suppressed expression of DzCAMTA3 and DzCAMTA8 confirmed their responsiveness to exogenous auxin treatment in a time-dependent manner. Accordingly, we propose that DzCAMTA3 and DzCAMTA8 synergistically crosstalk with ethylene during durian fruit ripening. In contrast, DzCAMTA3 and DzCAMTA8 antagonistically with auxin could affect the post-harvest ripening process in durian. Furthermore, DzCAMTA3 and DzCAMTA8 interacting genes contain significant CAMTA recognition motifs and regulated several pivotal fruit-ripening-associated pathways.ConclusionTaken together, the present study contributes to an in-depth understanding of the structure and probable function of CAMTA genes in the post-harvest ripening of durian.

Project description:Screening of cDNA expression libraries with labelled calmodulin (CaM) as a probe resulted in the isolation of cDNA encoding proteins designated CAMTA (for calmodulin-binding transcription activators). The Arabidopsis genome contains 6 members of this protein family (AtCAMTA1-6) all containing in addition to a defined CaM-binding domain a DNA-binding domain and ankyrin-repeat motifs. RT-PCR analysis revealed that all 6 genes are expressed in all organ throughout plant development. Therefore functional regulation of AtCAMTA proteins is likely mediated by second messengers (e.g. calcium/calmodulin signalling) and protein levels rather than by or in addition to gene expression levels. Based on domain organisation and sequence homologies we identified putative members of this protein family in C. elegans and in human. A yeast system was used to express chimeric fusion proteins comprised of the DNA-binding domain of the bacterial LexA protein with various segments of AtCAMTA1. This analysis revealed a distinct domain of AtCAMTA1 capable of activating transcription. Similar results were obtained with two human CAMTA homologues. To identify the gene targets of CAMTA proteins in Arabidopsiswe plan to analyse the transcriptome in loss_of_function and gain_of_function AtCAMTA mutants. For this we have already isolated a T-DNA insertion mutant of AtCAMTA1 (two alleles) and have requested two other insertion mutants of AtCAMTA2 and AtCAMTA3 identified in other labs. Screening for insertion mutants in the three remaining genes is underway. In addition we have initiated a gain_of_function approach in which DL10 proteins are expressed under the control of the dexamethasone-inducible promoter. Genes whose expression will be found modulated in the mutant plants will be considered candidate targets of AtCAMTA proteins. This analysis will complement an in vitro study of DNA-protein interactions to identify target-binding sites (part of the BBSRC funded project). As a first step in the project proposed to GARNet we suggest to compare the transcriptome in WT whole plants (2 weeks old) with that of three T-DNA insertion AtCAMTA mutants and one line expressing AtCAMTA1 under the control of an inducible promoter. Keywords: strain_or_line_design

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Neuronal calmodulin levels are controlled by CAMTA transcription factors.

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Neuronal calmodulin levels are controlled by CAMTA transcription factors.

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