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Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light-signaling pathways

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Abstract

Photosynthetic organisms, e.g., plants including green algae, use a sophisticated light-sensing system, composed of primary photoreceptors and additional downstream signaling components, to monitor changes in the ambient light environment towards adjust their growth and development. Although a variety of cellular processes, e.g., initiation of cleavage division and final cellular differentiation, have been shown to be light-regulated in the green alga Volvox carteri, little is known about the underlying light perception and signaling pathways. This multicellular alga possesses at least 12 photoreceptors, i.e., one phototropin (VcPhot), four cryptochromes (VcCRYa, VcCRYp, VcCRYd1, and VcCRYd2), and seven members of rhodopsin-like photoreceptors (VR1, VChR1, VChR2, VcHKR1, VcHKR2, VcHKR3, and VcHKR4), which display distinct light-dependent chemical processes based on their protein architectures and associated chromophores. Gene expression analyses could show that the transcript levels of some of the photoreceptor genes (e.g., VChR1 and VcHKR1) accumulate during division cleavages, while others (e.g., VcCRYa, VcCRYp, and VcPhot) accumulate during final cellular differentiation. However, the pattern of transcript accumulation changes when the alga switches to the sexual development. Eight photoreceptor genes, e.g., VcPhot, VcCRYp, and VcHKR1, are highly expressed in the somatic cells, while only the animal-type rhodopsin VR1 was found to be highly expressed in the reproductive cells/embryos during both asexual and sexual life cycles. Moreover, accumulation of VChR1 and VcCRYa transcripts is more sensitive to light and changes in response to more than one light quality. Obviously, different regulatory mechanisms underlying gene expression control transcript accumulation of photoreceptors not only during development, but also in a cell-type specific way and in response to various external signals such as light quality. The transcriptional patterns described in this study show that Volvox photoreceptors are mostly expressed in a cell-type specific manner. This gives reason to believe that cell-type specific light-signaling pathways allow differential regulation of cellular and developmental processes in response to the environmental light cues.

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Acknowledgments

We thank Halil Kavakli (College of Engineering Chemical and Biological Engineering, Koç University) and Alexey Desnitskiy (Department of Embryology, St. Petersburg State University) for reading the manuscript and Kordula Puls for technical assistance. We also would like to gratefully thank Georg Kreimer (Department of Biology, Friedrich-Alexander-Universität Erlangen-Nürnberg) for providing colored glass filters to perform light-dependent gene expression analysis. This study was funded by a grant (KI 1779/1-1) from the German Research Foundation (DFG) to AK. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

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  1. Department of Cellular and Developmental Biology of Plants, University of Bielefeld, Universitätsstr. 25, D-33615, Bielefeld, Germany

    Arash Kianianmomeni & Armin Hallmann

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Correspondence to Arash Kianianmomeni.

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Kianianmomeni, A., Hallmann, A. Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light-signaling pathways. Curr Genet 61, 3–18 (2015). https://doi.org/10.1007/s00294-014-0440-3

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