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The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway.

ABSTRACT: The evolutionary histories of complex traits are complicated because such traits are comprised of multiple integrated and interacting components, which may have different individual histories. Phylogenetic studies of complex trait evolution often do not take this into account, instead focusing only on the history of whole, integrated traits; for example, mapping eyes as simply present or absent through history. Using the biochemistry of animal vision as a model, we demonstrate how investigating the individual components of complex systems can aid in elucidating both the origins and diversification of such systems. Opsin-based phototransduction underlies all visual phenotypes in animals, using complex protein cascades that translate light information into changes in cyclic nucleotide gated (CNG) or canonical transient receptor potential (TRPC) ion-channel activity. Here we show that CNG ion channels play a role in cnidarian phototransduction. Transcripts of a CNG ion channel co-localize with opsin in specific cell types of the eyeless cnidarian Hydra magnipapillata. Further, the CNG inhibitor cis-diltiazem ablates a stereotypical photoresponse in the hydra. Our findings in the Cnidaria, the only non-bilaterian lineage to possess functional opsins, allow us to trace the history of CNG-based photosensitivity to the very origin of animal phototransduction. Our general analytical approach, based on explicit phylogenetic analysis of individual components, contrasts the deep evolutionary history of CNG-based phototransduction, today used in vertebrate vision, with the more recent assembly of TRPC-based systems that are common to protostome (e.g. fly and mollusc) vision.

SUBMITTER: Plachetzki DC

PROVIDER: S-EPMC2880087 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway.

Plachetzki David C DC Fong Caitlin R CR Oakley Todd H TH

Proceedings. Biological sciences 20100310 1690

The evolutionary histories of complex traits are complicated because such traits are comprised of multiple integrated and interacting components, which may have different individual histories. Phylogenetic studies of complex trait evolution often do not take this into account, instead focusing only on the history of whole, integrated traits; for example, mapping eyes as simply present or absent through history. Using the biochemistry of animal vision as a model, we demonstrate how investigating ...[more]

PMID: 20219739

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Project description:Analysis of transcriptome in moss Physcomitrella patens CNGCb null mutant at 25 and 34 degrees C for 30 minutes. Results provide insight into role of CNGCb in acquired thermotolerance induced by non-lethal heat treatment. Typically at dawn of a hot summer day, land plants need precise molecular thermometers to sense harmless increments in the ambient temperature to timely develop a heat-shock response (HSR) and accumulate protective heat shock proteins (Hsps), in anticipation of upcoming harmful temperatures at mid-day. Here, we found that the CNGCb gene from Physcomitrella patens and its Arabidopsis ortholog CNGC2, encode for a component of cyclic nucleotide gated Ca2+ channels acting as the primary thermosensors of land plant cells. Disruption of CNGCb or CNGC2 produced a hyper-thermosensitive phenotype, giving rise to a HSR and acquired thermotolerance at significantly milder heat-priming treatments than in wild type plants. In an aequorin-expressing moss, CNGCb loss-of-function caused altered Ca2+ signaling and a sustained Ca2+ influx. Patch clamp recordings on moss protoplasts showed the presence of three distinct thermo-responsive Ca2+-channels in wild type cells. Deletion of CNGCb led to a total absence of one, and it increased the open probability of the remaining two thermo-responsive Ca2+ channels. Thus, both in Arabidopsis and moss, CNGC2 and CNGCb are expected to form with other related CNGCs, heteromeric Ca2+ channels in the plasma membrane that respond to mild increments in the ambient temperature by triggering an optimal HSR, leading to the onset of plant acquired thermotolerance. The WT moss tissues were heat-shocked for a half an hour at 34°C and 38°C and CNGCb at 25and 34°C followed by liquid nitrogen freezing. Total RNA was isolated using RNeasy Mini Kit (QIAGEN, Hilden, Germany) and two biological replicate samples for each treatment, were extracted. An Agilent-certified microarray service lab (MOgene, LC, St. Louis, MO, USA) was used to verify the integrity of the RNA and perform the microarray experiments. Two biological replicates were performed.

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The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway.

Publications

The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway.

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