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Current Genetics

, Volume 61, Issue 1, pp 3–18 | Cite as

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

  • Arash KianianmomeniEmail author
  • Armin Hallmann
Research Article

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.

Keywords

Green algae Photoreceptors Transcript level Cell types Development Light quality 

Notes

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.

Supplementary material

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References

  1. Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL (1990) Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 18:141–153PubMedCrossRefGoogle Scholar
  2. Beel B, Prager K, Spexard M, Sasso S, Weiss D, Muller N, Heinnickel M, Dewez D, Ikoma D, Grossman AR, Kottke T, Mittag M (2012) A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 24:2992–3008PubMedCrossRefPubMedCentralGoogle Scholar
  3. Berthold P, Tsunoda SP, Ernst OP, Mages W, Gradmann D, Hegemann P (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 20:1665–1677PubMedCrossRefPubMedCentralGoogle Scholar
  4. Boonyareth M, Saranak J, Pinthong D, Sanvarinda Y, Foster KW (2009) Roles of cyclic AMP in regulation of phototaxis in Chlamydomonas reinhardtii. Biologia 64:1058–1065CrossRefGoogle Scholar
  5. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kroger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van de Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244PubMedCrossRefGoogle Scholar
  6. Brudler R, Hitomi K, Daiyasu H, Toh H, Kucho K, Ishiura M, Kanehisa M, Roberts VA, Todo T, Tainer JA, Getzoff ED (2003) Identification of a new cryptochrome class. Structure, function, and evolution. Mol Cell 11:59–67PubMedCrossRefGoogle Scholar
  7. Cashmore AR, Jarillo JA, Wu YJ, Liu DM (1999) Cryptochromes: blue light receptors for plants and animals. Science 284:760–765PubMedCrossRefGoogle Scholar
  8. Catlett NL, Yoder OC, Turgeon BG (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2:1151–1161PubMedCrossRefPubMedCentralGoogle Scholar
  9. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364PubMedCrossRefGoogle Scholar
  10. Choi G, Przybylska M, Straus D (1996) Three abundant germ line-specific transcripts in Volvox carteri encode photosynthetic proteins. Curr Genet 30:347–355PubMedCrossRefGoogle Scholar
  11. Danon A, Coll NS, Apel K (2006) Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. Proc Natl Acad Sci 103:17036–17041PubMedCrossRefPubMedCentralGoogle Scholar
  12. Deininger W, Kroger P, Hegemann U, Lottspeich F, Hegemann P (1995) Chlamyrhodopsin represents a new type of sensory photoreceptor. EMBO J 14:5849–5858PubMedPubMedCentralGoogle Scholar
  13. Ebnet E, Fischer M, Deininger W, Hegemann P (1999) Volvoxrhodopsin, a light-regulated sensory photoreceptor of the spheroidal green alga Volvox carteri. Plant Cell 11:1473–1484PubMedCrossRefPubMedCentralGoogle Scholar
  14. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251PubMedCrossRefPubMedCentralGoogle Scholar
  15. Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J Cell Sci 114:3857–3863PubMedGoogle Scholar
  16. Goodenough UW (1989) Cyclic AMP enhances the sexual agglutinability of Chlamydomonas flagella. J Cell Biol 109:247–252PubMedCrossRefGoogle Scholar
  17. Grossman AR, Lohr M, Im CS (2004) Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 38:119–173PubMedCrossRefGoogle Scholar
  18. Heyl A, Brault M, Frugier F, Kuderova A, Lindner AC, Motyka V, Rashotte AM, Schwartzenberg KV, Vankova R, Schaller GE (2013) Nomenclature for members of the two-component signaling pathway of plants. Plant Physiol 161:1063–1065PubMedCrossRefPubMedCentralGoogle Scholar
  19. Hoops HJ (1997) Motility in the colonial and multicellular Volvocales: structure, function, and evolution. Protoplasma 199:99–112CrossRefGoogle Scholar
  20. Huang KY, Beck CF (2003) Photoropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci 100:6269–6274PubMedCrossRefPubMedCentralGoogle Scholar
  21. Im CS, Eberhard S, Huang K, Beck CF, Grossman AR (2006) Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J 48:1–16PubMedCrossRefGoogle Scholar
  22. Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66PubMedCrossRefGoogle Scholar
  23. Kateriya S, Nagel G, Bamberg E, Hegemann P (2004) “Vision” in single-celled algae. News Physiol Sci 19:133–137PubMedGoogle Scholar
  24. Kianianmomeni A, Hallmann A (2013) Validation of reference genes for quantitative gene expression studies in Volvox carteri using real-time RT-PCR. Mol Biol Rep 40:6691–6699PubMedCrossRefGoogle Scholar
  25. Kianianmomeni A, Hallmann A (2014) Algal photoreceptors: in vivo functions and potential applications. Planta 239:1–26PubMedCrossRefGoogle Scholar
  26. Kianianmomeni A, Nematollahi G, Hallmann A (2008) A gender-specific retinoblastoma-related protein in Volvox carteri implies a role for the retinoblastoma protein family in sexual development. Plant Cell 20:2399–2419PubMedCrossRefPubMedCentralGoogle Scholar
  27. Kianianmomeni A, Stehfest K, Nematollahi G, Hegemann P, Hallmann A (2009) Channelrhodopsins of Volvox carteri are photochromic proteins that are specifically expressed in somatic cells under control of light, temperature, and the sex inducer. Plant Physiol 151:347–366PubMedCrossRefPubMedCentralGoogle Scholar
  28. Kirk D (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Cambridge University Press, Cambridge, UKGoogle Scholar
  29. Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. BioEssays News Rev Mol Cell Dev Biol 27:299–310CrossRefGoogle Scholar
  30. Kirk MM, Kirk DL (1985) Translational regulation of protein-synthesis, in response to light, at a critical stage of Volvox development. Cell 41:419–428PubMedCrossRefGoogle Scholar
  31. Kirk DL, Kirk MM (1986) Heat shock elicits production of sexual inducer in Volvox. Science 231:51–54PubMedCrossRefGoogle Scholar
  32. Kirk MM, Stark K, Miller SM, Muller W, Taillon BE, Gruber H, Schmitt R, Kirk DL (1999) regA, a Volvox gene that plays a central role in germ-soma differentiation, encodes a novel regulatory protein. Development 126:639–647PubMedGoogle Scholar
  33. Kochert G (1981) Sexual pheromones in Volvox development. In: O’Day DH, Horgen PA (eds) Sexual interactions in eukaryotic microbes. Academic Press, New York, pp 73–93CrossRefGoogle Scholar
  34. Kooijman R, Dewildt P, Vandenbriel W, Tan SH, Musgrave A, Vandenende H (1990) Cyclic AMP is one of the intracellular signals during the mating of Chlamydomonas eugametos. Planta 181:529–537PubMedCrossRefGoogle Scholar
  35. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98:193–205PubMedCrossRefGoogle Scholar
  36. Lopez L, Carbone F, Bianco L, Giuliano G, Facella P, Perrotta G (2012) Tomato plants overexpressing cryptochrome 2 reveal altered expression of energy and stress-related gene products in response to diurnal cues. Plant Cell Environ 35:994–1012PubMedCrossRefGoogle Scholar
  37. Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bogre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968PubMedCrossRefPubMedCentralGoogle Scholar
  38. Luck M, Mathes T, Bruun S, Fudim R, Hagedorn R, Nguyen TM, Kateriya S, Kennis JT, Hildebrandt P, Hegemann P (2012) A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by UV and blue light. J Biol Chem 287:40083–40090PubMedCrossRefPubMedCentralGoogle Scholar
  39. Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng XW (2005) Organ-specific expression of Arabidopsis genome during development. Plant Physiol 138:80–91PubMedCrossRefPubMedCentralGoogle Scholar
  40. Moran MA, Miller WL (2007) Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol 5:792–800PubMedCrossRefGoogle Scholar
  41. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, Bamberg E, Hegemann P (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398PubMedCrossRefGoogle Scholar
  42. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci 100:13940–13945PubMedCrossRefPubMedCentralGoogle Scholar
  43. Nedelcu AM, Michod RE (2003) Sex as a response to oxidative stress: the effect of antioxidants on sexual induction in a facultatively sexual lineage. Proc R Soc B 270(Suppl. 2):136–139CrossRefGoogle Scholar
  44. Nematollahi G, Kianianmomeni A, Hallmann A (2006) Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri. BMC Genom 7:321CrossRefGoogle Scholar
  45. O’Noil RM (1979) The light requirement for sexual induction of Volvox capensis Rich et Pocock. M. A. Thesis, Univ. of Texas, Austin: pp. 1–56Google Scholar
  46. Ozawa S, Nield J, Terao A, Stauber EJ, Hippler M, Koike H, Rochaix JD, Takahashi Y (2009) Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21:2424–2442PubMedCrossRefPubMedCentralGoogle Scholar
  47. Pasquale SM, Goodenough UW (1987) Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105:2279–2292PubMedCrossRefGoogle Scholar
  48. Piggot PJ, Hilbert DW (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7:579–586PubMedCrossRefGoogle Scholar
  49. Pokorny R, Klar T, Hennecke U, Carell T, Batschauer A, Essen LO (2008) Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc Natl Acad Sci 105:21023–21027PubMedCrossRefPubMedCentralGoogle Scholar
  50. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226PubMedCrossRefPubMedCentralGoogle Scholar
  51. Quarmby LM (1994) Signal transduction in the sexual life of Chlamydomonas. Plant Mol Biol 26:1271–1287PubMedCrossRefGoogle Scholar
  52. Quarmby LM, Hartzell HC (1994) Dissection of eukaryotic transmembrane signalling using Chlamydomonas. Trends Pharmacol Sci 15:343–349PubMedCrossRefGoogle Scholar
  53. Ragni M, D’Alcala MR (2004) Light as an information carrier underwater. J Plankton Res 26:433–443CrossRefGoogle Scholar
  54. Reisdorph NA, Small GD (2004) The CPH1 gene of Chlamydomonas reinhardtii encodes two forms of cryptochrome whose levels are controlled by light-induced proteolysis. Plant Physiol 134:1546–1554PubMedCrossRefPubMedCentralGoogle Scholar
  55. Sakaguchi H, Iwasa K (1979) Two photophobic responses in Volvox carteri. Plant Cell Physiol 20:909–916Google Scholar
  56. Schaller GE, Shiu SH, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21:R320–R330PubMedCrossRefGoogle Scholar
  57. Sineshchekov OA, Jung KH, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci 99:8689–8694PubMedCrossRefPubMedCentralGoogle Scholar
  58. Somers DE, Devlin PF, Kay SA (1998) Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282:1488–1490PubMedCrossRefGoogle Scholar
  59. Sommer U, Gliwicz ZM (1986) Long-range vertical migration of Volvox in tropical lake Cahora Bassa (Mozambique). Limnol Oceanogr 31:650–653CrossRefGoogle Scholar
  60. Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681–692PubMedCrossRefGoogle Scholar
  61. Starr RC, O’Neil RM, Miller CE (1980) l-Glutamic acid as a mediator of sexual morphogenesis in Volvox capensis. Proc Natl Acad Sci 77:1025–1028PubMedCrossRefPubMedCentralGoogle Scholar
  62. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215PubMedCrossRefGoogle Scholar
  63. Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, Yoshida K, Watanabe M, Daiyasu H, Toh H, Asamizu E, Tabata S, Miura K, Fukuzawa H, Nakamura S, Takahashi T (2003) Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun 301:711–717PubMedCrossRefGoogle Scholar
  64. Taminato A, Bagattini R, Gorjao R, Chen G, Kuspa A, Souza GM (2002) Role for YakA, cAMP, and protein kinase A in regulation of stress responses of Dictyostelium discoideum cells. Mol Biol Cell 13:2266–2275PubMedCrossRefPubMedCentralGoogle Scholar
  65. Trippens J, Greiner A, Schellwat J, Neukam M, Rottmann T, Lu Y, Kateriya S, Hegemann P, Kreimer G (2012) Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell 24:4687–4702PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ueki N, Matsunaga S, Inouye I, Hallmann A (2010) How 5,000 independent rowers coordinate their strokes in order to row into the sunlight: phototaxis in the multicellular green alga Volvox. BMC Biol 8:103PubMedCrossRefPubMedCentralGoogle Scholar
  67. Wang L, Renault G, Garreau H, Jacquet M (2004) Stress induces depletion of Cdc25p and decreases the cAMP producing capability in Saccharomyces cerevisiae. Microbiol 150:3383–3391CrossRefGoogle Scholar
  68. Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol 6:e4PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Cellular and Developmental Biology of PlantsUniversity of BielefeldBielefeldGermany

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