Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii

Schmidt, J; Eckert, Roger

doi:10.1038/262713a0

Cited by 253 publications

(173 citation statements)

References 8 publications

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“…Among them is a Ca 21 -binding protein with an EF hand motif (ID 162748; Vs2) with a C-terminally located single phosphorylation site. In the behavioral responses of C. reinhardtii to light, extracellular Ca 21 and Ca 21 fluxes are intricately involved (Schmidt and Eckert, 1976;Morel-Laurens 1987;Pazour et al, 1995;for review, see Witman, 1993). Both photoreceptors ChR-1 and ChR-2 are directly lightgated ion channels, which are able to conduct Ca 21 under physiological conditions.…”

Section: Discussionmentioning

confidence: 99%

The Phosphoproteome of aChlamydomonas reinhardtiiEyespot Fraction Includes Key Proteins of the Light Signaling Pathway

et al. 2007

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Flagellate green algae have developed a visual system, the eyespot apparatus, which allows the cell to phototax. In a recent proteomic approach, we identified 202 proteins from a fraction enriched in eyespot apparatuses of Chlamydomonas reinhardtii. Among these proteins, five protein kinases and two protein phosphatases were present, indicating that reversible protein phosphorylation occurs in the eyespot. About 20 major phosphoprotein bands were detected in immunoblots of eyespot proteins with an anti-phosphothreonine antibody. Toward the profiling of the targets of protein kinases in the eyespot fraction, we analyzed its phosphoproteome. The solubilized proteins of the eyespot fraction were treated with the endopeptidases LysC and trypsin prior to enrichment of phosphopeptides with immobilized metal-ion affinity chromatography. Phosphopeptides were analyzed by nano-liquid chromatography-electrospray ionization-mass spectrometry (MS) with MS/MS as well as neutral-loss-triggered MS/MS/MS spectra. We were able to identify 68 different phosphopeptides along with 52 precise in vivo phosphorylation sites corresponding to 32 known proteins of the eyespot fraction. Among the identified phosphoproteins are enzymes of carotenoid and fatty acid metabolism, putative signaling components, such as a SOUL heme-binding protein, a Ca 21 -binding protein, and an unusual protein kinase, but also several proteins with unknown function. Notably, two unique photoreceptors, channelrhodopsin-1 and channelrhodopsin-2, contain three and one phosphorylation sites, respectively. Phosphorylation of both photoreceptors occurs in the cytoplasmatic loop next to their seven transmembrane regions in a similar distance to that observed in vertebrate rhodopsins, implying functional importance for regulation of these directly light-gated ion channels relevant for the photoresponses of C. reinhardtii.

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Section: Discussionmentioning

confidence: 99%

The Phosphoproteome of aChlamydomonas reinhardtiiEyespot Fraction Includes Key Proteins of the Light Signaling Pathway

et al. 2007

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“…Photoexcitation of the receptor molecules results in the generation of photoreceptor currents, membrane depolarization, and, above a certain threshold of the stimulus intensity, activation of voltage-gated Ca 2ϩ channels in the flagellar membrane (8,9). These rapid electrical events bring about asymmetric motile responses of the two flagella during phototaxis (10,11) and a brief alteration of the flagellar beating mode during the photophobic response (12).…”

mentioning

confidence: 99%

Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii

Sineshchekov

Jung

Spudich

2002

Proc. Natl. Acad. Sci. U.S.A.

513

437

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We demonstrate that two rhodopsins, identified from cDNA sequences, function as low-and high-light-intensity phototaxis receptors in the eukaryotic alga Chlamydomonas reinhardtii. Each of the receptors consists of an Ϸ300-residue seven-transmembrane helix domain with a retinal-binding pocket homologous to that of archaeal rhodopsins, followed by Ϸ400 residues of additional membraneassociated portion. The function of the two rhodopsins, Chlamydomonas sensory rhodopsins A and B (CSRA and CSRB), as phototaxis receptors is demonstrated by in vivo analysis of photoreceptor electrical currents and motility responses in transformants with RNA interference (RNAi) directed against each of the rhodopsin genes. The kinetics, fluence dependencies, and action spectra of the photoreceptor currents differ greatly in transformants in accord with the relative amounts of photoreceptor pigments expressed. The data show that CSRA has an absorption maximum near 510 nm and mediates a fast photoreceptor current that saturates at high light intensity. In contrast, CSRB absorbs maximally at 470 nm and generates a slow photoreceptor current saturating at low light intensity. The relative wavelength dependence of CSRA and CSRB activity in producing phototaxis responses matches precisely the wavelength dependence of the CSRA-and CSRB-generated currents, demonstrating that each receptor mediates phototaxis. The saturation of the two photoreceptor currents at different light fluence levels extends the range of light intensity to which the organism can respond. Further, at intensities where both operate, their light signals are integrated at the level of membrane depolarization caused by the two photoreceptor currents.retinal protein ͉ photoreceptor ͉ receptor currents ͉ signal transduction U nicellular flagellate algae optimize their light environment by motility responses. Phototaxis (or oriented movement) guides them toward or away from a light source, whereas photophobic responses prevent their crossing a light͞dark border (1). In Chlamydomonas reinhardtii these photomotility responses are mediated by retinal-containing receptor(s), as shown by retinal reconstitution studies in blind mutants (2-5). Moreover, it has been established that the native chromophore of the photoreceptor protein(s) is 6-s-trans all-trans-retinal, as in archaeal rhodopsins, and its alltrans͞13-cis isomerization is required for triggering behavioral responses (3,4,6).A complex photoreceptor apparatus is used to track the light source. The photoreceptor molecules appear to be localized in a small portion of the plasma membrane overlying the eyespot. Light absorption͞reflection by the eyespot modulates the photoreceptor illumination during helical swimming if the helix axis does not coincide with the light direction (7). This modulated illumination serves as a signal for the correction of the swimming path.A cascade of electrical phenomena plays a key role in the signal transduction. Photoexcitation of the receptor molecules results in the generation of photoreceptor...

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“…the studies by Ishijima et al (1999) on marine snail (Turritella communis) sperm and by Schmidt and Eckert (1976) on Chlamydomonas.…”

Section: Sperm Flagellamentioning

confidence: 99%

Stretch‐activated calcium channels relay fast calcium waves propagated by calcium‐induced calcium influx

Jaffe

2007

Biology of the Cell

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For nearly 30 years, fast calcium waves have been attributed to a regenerative process propagated by CICR (calcium-induced calcium release) from the endoplasmic reticulum. Here, I propose a model containing a new subclass of fast calcium waves which is propagated by CICI (calcium-induced calcium influx) through the plasma membrane. They are called fast CICI waves. These move at the order of 100 to 1000 µm/s (at 20 • C), rather than the order of 3 to 30 µm/s found for CICR. Moreover, in this proposed subclass, the calcium influx which drives calcium waves is relayed by stretch-activated calcium channels. This model is based upon reports from approx. 60 various systems. In seven of these reports, calcium waves were imaged, and, in five of these, evidence was presented that these waves were regenerated by CICI. Much of this model involves waves that move along functioning flagella and cilia. In these systems, waves of local calcium influx are thought to cause waves of local contraction by inducing the sliding of dynein or of kinesin past tubulin microtubules. Other cells which are reported to exhibit waves, which move at speeds in the fast CICI range, include ones from a dozen protozoa, three polychaete worms, three molluscs, a bryozoan, two sea urchins, one arthropod, four insects, Amphioxus, frogs, two fish and a vascular plant (Equisetum), together with numerous healthy, as well as cancerous, mammalian cells, including ones from human. In two of these systems, very gentle local mechanical stimulation is reported to initiate waves. In these non-flagellar systems, the calcium influxes are thought to speed the sliding of actinomyosin filaments past each other. Finally, I propose that this mechanochemical model could be tested by seeing if gentle mechanical stimulation induces waves in more of these systems and, more importantly, by imaging the predicted calcium waves in more of them.

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Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii

Cited by 253 publications

References 8 publications

The Phosphoproteome of aChlamydomonas reinhardtiiEyespot Fraction Includes Key Proteins of the Light Signaling Pathway

The Phosphoproteome of aChlamydomonas reinhardtiiEyespot Fraction Includes Key Proteins of the Light Signaling Pathway

Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii

Stretch‐activated calcium channels relay fast calcium waves propagated by calcium‐induced calcium influx

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