Cell-type specific light-mediated transcript regulation in the multicellular alga Volvox carteri

BMC Genomics

Arash Kianianmomeni¹ 

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

关键词: Green algae;    Photoreceptors;    Gene expression;    Light quality;    Cell types;   

Others  :  1140808
DOI  :  10.1186/1471-2164-15-764

 received in 2014-03-06, accepted in 2014-09-03,  发布年份 2014

【 摘 要 】

Background

The multicellular green alga Volvox carteri makes use of none less than 13 photoreceptors, which are mostly expressed in a cell-type specific manner. This gives reason to believe that trasncriptome pattern of each cell type could change differentially in response to environmental light. Here, the cell-type specific changes of various transcripts from different pathways in response to blue, red and far-red light were analyzed.

Results

In response to different light qualities, distinct changes in transcript accumulation of genes encoding proteins involved in chlorophyll and carotenoid biosynthesis, light-harvesting complexes, circadian clock and cell cycle control were observed. Namely, blue light tends to be effective to accumulate transcripts in the somatic cells; while red light leads to accumulate transcripts predominantly in the reproductive cells. Blue light also induced marked accumulation of two components of circadian rhythms only in the somatic cells, indicating that these clock-relevant components are affected by blue light in a cell-type specific manner. Further, we show that photosynthetic associated genes are regulated distinctly among cell types by different light qualities.

Conclusion

Our results suggest that Volvox uses different sophisticated cell-type specific light signaling pathways to modulate expression of genes involved in various cellular and metabolic pathways including circadian rhythms and photosynthesis in response to environmental light.

【 授权许可】

   
2014 Kianianmomeni; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Grossman AR, Lohr M, Im CS: Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 2004, 38:119-173.
• [2]Kirk MM, Kirk DL: Translational regulation of protein-synthesis, in response to light, at a critical stage of Volvox development. Cell 1985, 41(2):419-428.
• [3]Huang KY, Beck CF: 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 U S A 2003, 100(10):6269-6274.
• [4]Oldenhof H, Zachleder V, van den Ende H: Blue light delays commitment to cell division in Chlamydomonas reinhardtii. Plant Biol (Stuttg) 2004, 6(6):689-695.
• [5]Foster KW, Smyth RD: Light antennas in phototactic algae. Microbiol Rev 1980, 44(4):572-630.
• [6]Kianianmomeni A, Hallmann A: Algal photoreceptors: in vivo functions and potential applications. Planta 2014, 239(1):1-26.
• [7]Hegemann P: Algal sensory photoreceptors. Annu Rev Plant Biol 2008, 59:167-189.
• [8]Liu B, Zuo ZC, Liu HT, Liu XM, Lin CT: Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev 2011, 25(10):1029-1034.
• [9]Jiao Y, Yang H, Ma L, Sun N, Yu H, Liu T, Gao Y, Gu H, Chen Z, Wada M, Gerstein M, Zhao H, Qu LJ, Deng XW: A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiol 2003, 133(4):1480-1493.
• [10]Beel B, Prager K, Spexard M, Sasso S, Weiss D, Muller N, Heinnickel M, Dewez D, Ikoma D, Grossman AR, Kottke T, Mittag M: A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 2012, 24(7):2992-3008.
• [11]Im CS, Eberhard S, Huang K, Beck CF, Grossman AR: Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J 2006, 48(1):1-16.
• [12]Sineshchekov OA, Jung KH, Spudich JL: Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 2002, 99(13):8689-8694.
• [13]Deininger W, Kroger P, Hegemann U, Lottspeich F, Hegemann P: Chlamyrhodopsin represents a new type of sensory photoreceptor. EMBO J 1995, 14(23):5849-5858.
• [14]Trippens J, Greiner A, Schellwat J, Neukam M, Rottmann T, Lu Y, Kateriya S, Hegemann P, Kreimer G: Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell 2012, 24:4687-4702.
• [15]Kirk DL: A twelve-step program for evolving multicellularity and a division of labor. Bioessays 2005, 27(3):299-310.
• [16]Kianianmomeni A, Hallmann A: Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light signaling pathways. Curr Genet 2014. doi:10.1007/s00294-014-0440-3
• [17]Kirk D: Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Cambridge, UK: Cambridge University Press; 1998.
• [18]Hallmann A: Extracellular matrix and sex-inducing pheromone in Volvox. Int Rev Cytol 2003, 227:131-182.
• [19]Kianianmomeni A, Stehfest K, Nematollahi G, Hegemann P, Hallmann A: 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 2009, 151(1):347-366.
• [20]Ebnet E, Fischer M, Deininger W, Hegemann P: Volvoxrhodopsin, a light-regulated sensory photoreceptor of the spheroidal green alga Volvox carteri. Plant Cell 1999, 11(8):1473-1484.
• [21]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: Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 2010, 329(5988):223-226.
• [22]Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, et al.: The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318(5848):245-250.
• [23]Johanningmeier U, Howell SH: Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors. J Biol Chem 1984, 259(21):13541-13549.
• [24]Teramoto H, Itoh T, Ono TA: High-intensity-light-dependent and transient expression of new genes encoding distant relatives of light-harvesting chlorophyll-a/b proteins in Chlamydomonas reinhardtii. Plant Cell Physiol 2004, 45(9):1221-1232.
• [25]Teramoto H, Ishii A, Kimura Y, Hasegawa K, Nakazawa S, Nakamura T, Higashi S, Watanabe M, Ono TA: Action spectrum for expression of the high intensity light-inducible Lhc-like gene Lhl4 in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol 2006, 47(3):419-425.
• [26]Vasileuskaya Z, Oster U, Beck CF: Involvement of tetrapyrroles in inter-organellar signaling in plants and algae. Photosynth Res 2004, 82(3):289-299.
• [27]Matters GL, Beale SI: Structure and light-regulated expression of the gsa gene encoding the chlorophyll biosynthetic enzyme, glutamate 1-semialdehyde aminotransferase, in Chlamydomonas reinhardtii. Plant Mol Biol 1994, 24(4):617-629.
• [28]Matters GL, Beale SI: Blue-light-regulated expression of genes for two early steps of chlorophyll biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 1995, 109(2):471-479.
• [29]Li J, Timko MP: The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH:protochlorophyllide oxidoreductase. Plant Mol Biol 1996, 30(1):15-37.
• [30]Matters GL, Beale SI: Structure and expression of the Chlamydomonas reinhardtii alad gene encoding the chlorophyll biosynthetic enzyme, delta-aminolevulinic acid dehydratase (porphobilinogen synthase). Plant Mol Biol 1995, 27(3):607-617.
• [31]Mayfield SP, Schirmerrahire M, Frank G, Zuber H, Rochaix JD: Analysis of the genes of the OEE1 and OEE3 proteins of the photosystem II complex from Chlamydomonas reinhardtii. Plant Mol Biol 1989, 12(6):683-693.
• [32]Kim JM, Mayfield SP: Protein disulfide isomerase as a regulator of chloroplast translational activation. Science 1997, 278(5345):1954-1957.
• [33]Alizadeh D, Cohen A: Red light and calmodulin regulate the expression of the psbA binding protein genes in Chlamydomonas reinhardtii. Plant Cell Physiol 2010, 51(2):312-322.
• [34]Barnes D, Cohen A, Bruick RK, Kantardjieff K, Fowler S, Efuet E, Mayfield SP: Identification and characterization of a novel RNA binding protein that associates with the 5′-untranslated region of the chloroplast psbA mRNA. Biochemistry 2004, 43(26):8541-8550.
• [35]Bohne F, Linden H: Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta 2002, 1579(1):26-34.
• [36]Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, Todo T, Bowler C, Falciatore A: Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep 2009, 10(6):655-661.
• [37]Nematollahi G, Kianianmomeni A, Hallmann A: Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri. BMC Genomics 2006, 7:321.
• [38]Fukuzawa H, Fujiwara S, Tachiki A, Miyachi S: Nucleotide sequences of two genes CAH1 and CAH2 which encode carbonic anhydrase polypeptides in Chlamydomonas reinhardtii. Nucleic Acids Res 1990, 18(21):6441-6442.
• [39]Dionisio-Sese ML, Fukuzawa H, Miyachi S: Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 1990, 94(3):1103-1110.
• [40]Chen Q, Silflow CD: Isolation and characterization of glutamine synthetase genes in Chlamydomonas reinhardtii. Plant Physiol 1996, 112(3):987-996.
• [41]Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL: Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 1990, 18(2):141-153.
• [42]Provasoli L, Pintner IJ: Artificial Media for Fresh-Water Algae: Problems and Suggestions. In The Ecology of Algae, a Symposium Held at the Pymatuning Laboratory of Field Biology on June 18 and 19, 1959, (ed). Edited by Tryon CA, Hartman RT. Pittsburgh, PA: The Pymatuning Symposia in Ecology, Special Publication No 2, University of Pittsburgh; 1959:84-96.
• [43]Kianianmomeni A, Hallmann A: Validation of reference genes for quantitative gene expression studies in Volvox carteri using real-time RT-PCR. Mol Biol Rep 2013, 40:6691-6699.
• [44]Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW: Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 2001, 13(12):2589-2607.
• [45]Hamazato F, Shinomura T, Hanzawa H, Chory J, Furuya M: Fluence and wavelength requirements for Arabidopsis CAB gene induction by different phytochromes. Plant Physiol 1997, 115(4):1533-1540.
• [46]Iliev D, Voytsekh O, Schmidt EM, Fiedler M, Nykytenko A, Mittag M: A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock. Plant Physiol 2006, 142(2):797-806.
• [47]Cizkova M, Pichova A, Vitova M, Hlavova M, Hendrychova J, Umysova D, Galova E, Sevcovicova A, Zachleder V, Umen JG, Bisova K: CDKA and CDKB kinases from Chlamydomonas reinhardtii are able to complement cdc28 temperature-sensitive mutants of Saccharomyces cerevisiae. Protoplasma 2008, 232(3–4):183-191.
• [48]Bisova K, Krylov DM, Umen JG: Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol 2005, 137(2):475-491.
• [49]Schaap P: Guanylyl cyclases across the tree of life. Front Biosci 2005, 10:1485-1498.
• [50]Shenroy AR, Visweswariah SS: Class III nucleotide cyclases in bacteria and archaebacteria: lineage-specific expansion of adenylyl cyclases and a dearth of guanylyl cyclases. FEBS Lett 2004, 561(1–3):11-21.
• [51]Franklin KA, Whitelam GC: Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nature Genet 2007, 39(11):1410-1413.
• [52]Nagatani A: Light-regulated nuclear localization of phytochromes. Curr Opin Plant Biol 2004, 7(6):708-711.
• [53]Winands A, Wagner G: Phytochrome of the green alga Mougeotia: cDNA sequence, autoregulation and phylogenetic position. Plant Mol Biol 1996, 32(4):589-597.
• [54]Kidd DG, Lagarias JC: Phytochrome from the green alga Mesotaenium caldariorum. J Biol Chem 1990, 265(12):7029-7035.
• [55]Casal JJ, Yanovsky MJ: Regulation of gene expression by light. Int J Dev Biol 2005, 49(5–6):501-511.
• [56]Wu HP, Su YS, Chen HC, Chen YR, Wu CC, Lin WD, Tu SL: Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens. Genome Biol 2014, 15(1):R10.
• [57]Jiao Y, Lau OS, Deng XW: Light-regulated transcriptional networks in higher plants. Nat Rev Genet 2007, 8(3):217-230.
• [58]Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bogre L, Shanahan H: Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 2008, 20(4):947-968.
• [59]Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng XW: Organ-specific expression of Arabidopsis genome during development. Plant Physiol 2005, 138(1):80-91.
• [60]Kami C, Lorrain S, Hornitschek P, Fankhauser C: Light-regulated plant growth and development. Curr Top Dev Biol 2010, 91:29-66.
• [61]Molas ML, Kiss JZ, Correll MJ: Gene profiling of the red light signalling pathways in roots. J Exp Bot 2006, 57(12):3217-3229.
• [62]Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH: Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci U S A 2001, 98(16):9437-9442.
• [63]Meyerowitz EM: Plants compared to animals: the broadest comparative study of development. Science 2002, 295(5559):1482-1485.
• [64]Tam LW, Kirk DL: Identification of cell-type-specific genes of Volvox carteri and characterization of their expression during the asexual life cycle. Dev Biol 1991, 145(1):51-66.
• [65]Meissner M, Stark K, Cresnar B, Kirk DL, Schmitt R: Volvox germline-specific genes that are putative targets of RegA repression encode chloroplast proteins. Curr Genet 1999, 36(6):363-370.
• [66]Deng XW, Quail PH: Signalling in light-controlled development. Semin Cell Dev Biol 1999, 10(2):121-129.
• [67]Neff MM, Fankhauser C, Chory J: Light: an indicator of time and place. Genes Dev 2000, 14(3):257-271.
• [68]Suetsugu N, Wada M: Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 2007, 388(9):927-935.
• [69]Franklin KA: Shade avoidance. New Phytologist 2008, 179(4):930-944.
• [70]Hudson ME, Lisch DR, Quail PH: The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 2003, 34(4):453-471.
• [71]Quail PH: Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 2002, 3(2):85-93.
• [72]Duncan L, Nishii I, Howard A, Kirk D, Miller SM: Orthologs and paralogs of regA, a master cell-type regulatory gene in Volvox carteri. Curr Genet 2006, 50(1):61-72.
• [73]Kirk MM, Stark K, Miller SM, Muller W, Taillon BE, Gruber H, Schmitt R, Kirk DL: regA, a Volvox gene that plays a central role in germ-soma differentiation, encodes a novel regulatory protein. Development 1999, 126(4):639-647.
• [74]Mittag M: Conserved circadian elements in phylogenetically diverse algae. Proc Natl Acad Sci U S A 1996, 93(25):14401-14404.
• [75]Zhao B, Schneid C, Iliev D, Schmidt EM, Wagner V, Wollnik F, Mittag M: The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology domain-containing subunits. Eukaryot Cell 2004, 3(3):815-825.
• [76]Yakir E, Hassidim M, Melamed-Book N, Hilman D, Kron I, Green RM: Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J 2011, 68(3):520-531.
• [77]Sommer U, Gliwicz ZM: Long-range vertical migration of Volvox in tropical lake Cahora Bassa (Mozambique). Limnol Oceanogr 1986, 31(3):650-653.
• [78]Moran MA, Miller WL: Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol 2007, 5(10):792-800.
• [79]Ragni M, D’Alcala MR: Light as an information carrier underwater. J Plankton Res 2004, 26(4):433-443.
• [80]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: Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun 2003, 301(3):711-717.
• [81]Luck M, Mathes T, Bruun S, Fudim R, Hagedorn R, Nguyen TM, Kateriya S, Kennis JT, Hildebrandt P, Hegemann P: A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by UV and blue light. J Biol Chem 2012, 287:40083-40090.
• [82]Roenneberg T, Foster RG: Twilight times: light and the circadian system. Photochem Photobiol 1997, 66(5):549-561.
• [83]Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B: The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 2011, 109(1–3):133-149.