Abstract
The unicellular flagellate Euglena gracilis shows positive phototaxis at low-light intensities (<10 W/m2) and a negative one at higher irradiances (>10 W/m2). Phototaxis is based on blue light-activated adenylyl cyclases, which produce cAMP upon irradiation. In the absence of light the cells swim upward in the water column (negative gravitaxis). The results of sounding rocket campaigns and of a large number of ground experiments led to the following model of signal perception and transduction in gravitaxis of E. gracilis: The body of the cell is heavier than the surrounding medium, sediments and thereby exerts a force onto the lower membrane. Upon deviation from a vertical swimming path mechano-sensitive ion channels are activated. Calcium is gated inwards which leads to an increase in the intracellular calcium concentration and causes a change of the membrane potential. After influx, calcium activates one of several calmodulins found in Euglena, which in turn activates an adenylyl cyclase (different from the one involved in phototaxis) to produce cAMP from ATP. One further element in the sensory transduction chain of both phototaxis and gravitaxis is a specific protein kinase A. We found five different protein kinases A in E. gracilis. The blockage of only one of these (PK.4, accession No. EU935859) by means of RNAi inhibited both phototaxis and gravitaxis, while inhibition of the other four affected neither phototaxis nor gravitaxis. It is assumed that cAMP directly activates this protein kinase A which may in turn phosphorylate a protein involved in the flagellar beating mechanism.
Similar content being viewed by others
Abbreviations
- PAC:
-
Photoactivated adenylyl cyclase
- PK:
-
Protein kinase
- RACE:
-
Rapid amplification of cDNA ends
References
Boesger J, Wagner V, Weisheit W, Mittag M (2009) Analysis of flagellar phosphoproteins from Chlamydomonas reinhardtii. Eukaryot Cell 8:922–932
Chang SC, Kaufman PB (2000) Effects of staurosporine, okadaic acid and sodium fluoride on protein phosphorylation in graviresponding oat shoot pulvini. Plant Physiol Biochem 38:315–323
Checcucci A, Colombetti G, Ferrara R, Lenci F (1976) Further analysis of the mass photoresponses of Euglena gracilis Klebs (Flagellata euglenoidina). Monitore Zool Ital N S 10:271–277
Daiker V, Häder D-P, Lebert M (2010) Molecular characterization of a calmodulin involved in the signal transduction chain of gravitaxis in Euglena gracilis. Planta 231:1229–1236
Iseki M, Matsunaga S, Murakami A, Ohno K, Shiga K, Yoshida C, Sugai M, Takahashi T, Hori T, Watanabe M (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051
Lebert M, Häder D-P (1999) Image analysis: a versatile tool for numerous applications. G I T Imaging Microsc 1:5–6
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu L-H, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cherutti H, Chanfreau G, Chen C-L, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral J-P, Riaño-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen C-J, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martínez D, Ngau WCA, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250
Newton AC (2001) Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem Rev 101:2353–2364
Newton AC (2003) Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem J 370:361–371
Ngo H, Tschudi C, Gull K, Ullu E (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Nat Acad Sci USA 95:14687–14692
Ntefidou M, Häder D-P (2005) Photoactivated adenylyl cyclase (PAC) genes in the flagellate Euglena gracilis mutant strains. Photochem Photobiol Sci 4:732–739
Ntefidou M, Iseki M, Watanabe M, Lebert M, Häder D-P (2003) Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. Plant Physiol 133:1517–1521
Richter P, Häder D-P (2000) Calcium imaging in living cells. In: Häder D-P (ed) Image analysis: methods and applications. CRC Press, Boca Raton, pp 373–389
Richter P, Lebert M, Korn R, Häder D-P (2001a) Possible involvement of the membrane potential in the gravitactic orientation of Euglena gracilis. J Plant Physiol 158:35–39
Richter P, Lebert M, Tahedl H, Häder D-P (2001b) Calcium is involved in the gravitactic orientation in colorless flagellates. J Plant Physiol 158:689–697
Richter PR, Streb C, Ntefidou M, Lebert M, Häder D-P (2003) High light-induced sign change of gravitaxis in the flagellate Euglena gracilis is mediated by reactive oxygen species. Acta Protozool 42:197–204
Richter PR, Schuster M, Lebert M, Streb C, Häder D-P (2007) Gravitaxis of Euglena gracilis depends only partially on passive buoyancy. Adv Space Res 39:1218–1224
Sakato M, Sakakibara H, King SM (2007) Chlamydomonas outer arm dynein alters conformation in response to Ca2+. Mol Biol Cell 18:3620–3634
Schlösser UG (1994) SAG-Sammlung von Algenkulturen at the University of Göttingen. Catalogue of Strains 1994. Bot Acta 107:113–186
Schmidt M, Geßner G, Luff M, Heiland I, Wagner V, Kaminski M, Geimer S, Eitzinger N, Reißenweber T, Voytsekh O, Fiedler M, Mittag M, Kreimer G (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements. Plant Cell 18:1908–1930
Starr RC (1964) The culture collection of algae at Indiana University. Am J Bot 51:1013–1044
Streb C, Richter P, Ntefidou M, Lebert M, Häder D-P (2002) Sensory transduction of gravitaxis in Euglena gracilis. J Plant Physiol 159:855–862
Tahedl H, Richter P, Lebert M, Häder D-P (1998) cAMP is involved in gravitaxis signal transduction of Euglena gracilis. Microgravity Sci Technol 11:173–178
Vogel K, Häder D-P (1990) Simultaneous tracking of flagellates in real time by image analysis. In: Proc Fourth European Symposium on Life Science Research in Space (ESA SP-307), pp 541–545
Wagner V, Boesger J, Mittag M (2009) Sub-proteome analysis in the green flagellate alga Chlamydomonas reinhardtii. J Basic Microbiol 49:32–41
Wakabayashi K-I, Ide T, Kamiya R (2009) Calcium-dependent flagellar motility activation in Chlamydomonas reinhardtii in response to mechanical agitation. Cell Motil Cytoskel 66:736–742
Acknowledgments
The authors gratefully acknowledge the skillful technical assistance of Jennifer Tebart, Ulrike Trenz and Martin Schuster.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Daiker, V., Häder, DP., Richter, P.R. et al. The involvement of a protein kinase in phototaxis and gravitaxis of Euglena gracilis . Planta 233, 1055–1062 (2011). https://doi.org/10.1007/s00425-011-1364-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-011-1364-5