Advertisement

UV-B response is modulated by cell-type specific signaling pathway in multicellular green algae Volvox carteri

  • Jafar RazeghiEmail author
  • Arash Kianianmomeni
Original Paper
  • 23 Downloads

Abstract

A fundamental question in biology is how multicellular organisms regulate cellular and physiological processes in response to environmental signals in a tissue/cell type-specific manner. Light is one such cue but little is known about its effect on molecular mechanisms underlying cell-type specific signaling. The Volvox genus presents a Germ-Soma differentiation that can be used to understand the genetic mechanisms of evolutionary transition from single-cell to multicellular organisms. Here we report the transcriptional analysis throughout both asexual and sexual life cycles of Volvox carteri in two different cell types under UV-B light irradiation. Our data show that VcUVR8-V1, the main splice variant of the VcUVR8 transcript, accumulates during initiation of cleavage division. Moreover, the transcript level of VcUVR8-V1 increases in response to the sex inducer. VcUVR8 expression seems to remain the same in both cell types, while VcCOP1, the interacting partner of VcUVR8, is expressed in a cell-type specific manner. Interestingly, illumination with low doses of UV-B leads to an increase of VcCOP1 transcript levels only in the somatic cells. Our results indicate that UV-B signaling pathway is differentially regulated between two cell types and environmental UV-B could be involved in cell-type specific regulation of developmental and physiological processes.

Keywords

UV-B photoreceptor UVR8 COP1 Gene expression Green algae Volvox carteri 

Notes

Acknowledgements

This work has been supported by the Center for International Scientific Studies & Collaboration [CISSC (2013)] to JR and DFG Grant KI 1779/1-1 to AK. We would like thank Magdalena Dombrowa and Saskia Wöllner for their great experimental support during this study. Also, we thank Stefania Viola, Wenteng Xu and Girish Beedessee for reading of the manuscript and helpful suggestions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2018_472_MOESM1_ESM.doc (66 kb)
Supplementary material 1 (DOC 65 KB)

References

  1. Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321CrossRefGoogle 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 24:2992–3008CrossRefGoogle Scholar
  3. Beggs CJ, Wellmann E, Kronenberg GHM (1994) Photocontrol of flavonoid biosynthesis. In: Kendrick RE (ed) Photomorphogenesis in plants. Kluwer Academic Publishers, Dordrecht, pp 733–751CrossRefGoogle Scholar
  4. Brosché M, Strid Ȧ (2003) Molecular events following perception of ultraviolet-B radiation by plants. Physiol Plant 117:1–10CrossRefGoogle Scholar
  5. Brown BA, Cloix C, Jiang GH, Kaiserli E, Herzyk P, Kliebenstein DJ, Jenkins GI (2005) A UV-B-specific signaling component orchestrates plant UV protection. Proc Natl Acad Sci USA 102:18225–18230CrossRefGoogle Scholar
  6. Buchanan B, Gruissem W, Jones R (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Courier Companies. Inc, WaldorfGoogle Scholar
  7. Casati P, Walbot V (2004) Crosslinking of ribosomal proteins to RNA in maize ribosomes by UV-B and its effects on translation. Plant Physiol 136:3319–3332CrossRefGoogle Scholar
  8. Cen YP, Bornman JF (1990) The response of bean plants to UV-B radiation under different irradiances of background visible light. J Exp Bot 41:1489–1495CrossRefGoogle Scholar
  9. Christie JM, Arvai AS, Baxter KJ, Heilmann M, Pratt AJ, O’Hara A, Kelly SM, Hothorn M, Smith BO, Hitomi K, Jenkins GI, Getzoff ED (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–1496CrossRefGoogle Scholar
  10. Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, Todo T, Bowler C, Falciatore A (2009) Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep 10:655–661CrossRefGoogle Scholar
  11. Deng XW, Quail PH (1999) Signalling in light-controlled development. Semin Cell Dev Biol 10:121–129CrossRefGoogle Scholar
  12. Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71:791–801CrossRefGoogle 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 11:1473–1484CrossRefGoogle Scholar
  14. Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, Albert A, Cloix C, Jenkins GI, Oakeley EJ, Seidlitz HK, Nagy F, Ulm R (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28:591–601CrossRefGoogle Scholar
  15. Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5, 164–166Google Scholar
  16. Foster KW, Smyth RD (1980) Light antennas in phototactic algae. Microbiol Rev 44:572–630PubMedPubMedCentralGoogle Scholar
  17. Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420–1428CrossRefGoogle Scholar
  18. Gerszberg A, Hnatuszko-Konka K (2017) Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul 83:175–198CrossRefGoogle Scholar
  19. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98Google Scholar
  20. Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci 17:230–237CrossRefGoogle Scholar
  21. Heijde M, Zabulon G, Corellou F, Ishikawa T, Brazard J, Usman A, Sanchez F, Plaza P, Martin M, Falciatore A, Todo T, Bouget FY, Bowler C (2010) Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant Cell Environ 33:1614–1626CrossRefGoogle Scholar
  22. Hideg É, Barta C, Kálai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164CrossRefGoogle Scholar
  23. Izaguirre MM, Scopel AL, Baldwin IT, Ballare CL (2003) Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiol 132:1755–1767CrossRefGoogle Scholar
  24. Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135CrossRefGoogle Scholar
  25. Jiang SC, Mei C, Liang S, Yu YT, Lu K, Wu Z, Wang XF, Zhang DP (2015) Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses. Plant Mol Biol 88:369–385CrossRefGoogle Scholar
  26. Kianianmomeni A (2014a) Cell-type specific light-mediated transcript regulation in the multicellular alga Volvox carteri. BMC Genom 15:764–778CrossRefGoogle Scholar
  27. Kianianmomeni A (2014b) More light behind gene expression. Trends Plant Sci 19:488–490CrossRefGoogle Scholar
  28. Kianianmomeni A (2015a) Cell-type specific photoreceptors and light signaling pathways in the multicellular green alga Volvox carteri and their potential role in cellular differentiation. Plant Signal Behav 10: e1010935-1- e1010935-4Google Scholar
  29. Kianianmomeni A (2015b) Potential impact of gene regulatory mechanisms on the evolution of multicellularity in the volvocine algae. Commun Integr Biol 8: e1017175-1- e1017175-4Google Scholar
  30. 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 40:6691–6699CrossRefGoogle Scholar
  31. Kianianmomeni A, Hallmann A (2014a) Algal photoreceptors: in vivo functions and potential applications. Planta 239:1–26CrossRefGoogle Scholar
  32. Kianianmomeni A, Hallmann A (2014b) Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light-signaling pathways. Curr Genet 61:1–16Google Scholar
  33. Kianianmomeni A, Hallmann A (2015) Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light- signaling pathways. Curr Genet 61:3–18CrossRefGoogle Scholar
  34. 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 20:2399–2419CrossRefGoogle Scholar
  35. 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 151:347–366CrossRefGoogle Scholar
  36. Kinyó A, Kiss-László Z, Hambalkó S, Bebes A, Kiss M, Széll M, Bata-Csörgo Z, Nagy F, Kemény L (2010) COP1 contributes to UVB-induced signaling in human keratinocytes. J Invest Dermatol 130:541–545CrossRefGoogle Scholar
  37. Kirk DL (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Cambridge University Press, CambridgeGoogle Scholar
  38. Kirk DL, Kirk MM (1986) Heat shock elicits production of sexual inducer in Volvox. Science 231:51–54CrossRefGoogle Scholar
  39. Kochert G, Crump WJ (1979) Reversal of sexual induction in Volvox carteri by ultraviolet irradiation and removal of sexual pheromone. Gamete Res 2:259–264CrossRefGoogle Scholar
  40. Kucera B, Leubner-metzger G, Wellmann E (2003) Distinct ultraviolet-signaling pathways in bean leaves. DNA damage is associated with β-1, 3-glucanase gene induction, but not with flavonoid formation. Plant Physiol 133:1445–1452CrossRefGoogle Scholar
  41. Laluk K, AbuQamar S, Mengiste T (2011) The arabidopsis mitochondria-localized pentatricopeptide repeat protein PGN functions in defense against necrotrophic fungi and abiotic stress tolerance. Plant Physiol 156:2053–2068CrossRefGoogle Scholar
  42. Lumsden P (1997) Plants and UV-B: responses to environmental change. Cambridge University Press, CambridgeGoogle Scholar
  43. McKenzie RL, Björn LO, Bais A, Ilyasd M (2003) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem Photobiol Sci 2:5–15CrossRefGoogle Scholar
  44. 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 296:2395–2398CrossRefGoogle Scholar
  45. 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 100:13940–13945CrossRefGoogle Scholar
  46. Nawaz G, Sai TZT, Lee K, Kim YO, Kang H (2018) Rice DEAD-box RNA helicase OsRH53 has negative impact on Arabidopsis response to abiotic stresses. Plant Growth Regul 85:153–163CrossRefGoogle Scholar
  47. Nedelcu AM, Marcu O, Michod RE (2004) Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc R Soc B 271:1591–1596CrossRefGoogle Scholar
  48. Nematollahi G, Kianianmomeni A, Hallmann A (2006) Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri. BMC Genom 7:321–340CrossRefGoogle Scholar
  49. Oravecz A, Baumann A, Máté Z, Brzezinska A, Molinier J, Oakeley EJ, Ádám É, Schäfer E, Nagy F, Ulm R (2006) CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18:1975–1990CrossRefGoogle Scholar
  50. Owens DK, Crosby KC, Runac J, Howard BA, Winkel BS (2008) Biochemical and genetic characterization of Arabidopsis flavanone 3beta-hydroxylase. Plant Physiol Biochem 46:833–843CrossRefGoogle Scholar
  51. Page RD (1996) TreeView: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  52. Park YJ, Lee HJ, Kwak KJ, Lee K, Hong SW, Kang H (2014) MicroRNA400-guided cleavage of pentatricopeptide repeat protein mRNAs renders Arabidopsis thaliana more susceptible to pathogenic bacteria and fungi. Plant Cell Physiol 55:1660–1668CrossRefGoogle Scholar
  53. 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 329:223–226CrossRefGoogle Scholar
  54. Provasoli L, Pintner IJ (1959) Artificial media for fresh-water algae: problems and suggestions. In Tryon CA, Hartman RT (eds) The ecology of algae, a symposium held at the pymatuning laboratory of field biology on June 18 and 19. The Pymatuning Symposia in Ecology, Special Publication No 2, University of Pittsburgh, Pittsburgh 84–96Google Scholar
  55. Rizzini L, Favory JJ, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schafer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106CrossRefGoogle Scholar
  56. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  57. Schaller GE, Shiu SH, Armitage JP (2011) Two-component systems and their co-option for eukaryotic signal transduction. Curr Biol 21:320–330CrossRefGoogle Scholar
  58. Stapleton A (1992) Ultraviolet radiation and plants: burning questions. Plant Cell 4:1353–1358CrossRefGoogle Scholar
  59. Starr RC (1969) Structure, reproduction and differentiation in Volvox carteri f. nagariensis Lyengre strains HK9 and 10. Arch Protistenkd Bd 111:204–222Google Scholar
  60. Starr RC, Jaenicke L (1974) Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc Natl Acad Sci USA 71:1050–1054CrossRefGoogle Scholar
  61. Starr RC, O’Neil RM, Miller CE (1980) L-Glutamic acid as a mediator of sexual differentiation in Volvox capensis. Proc Natl Acad Sci USA 77:1025–1028CrossRefGoogle Scholar
  62. Sturm S, Engelken J, Gruber A, Vugrinec S, Kroth PG, Adamska I, Lavaud J (2013) A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids. BMC Evol Biol 13:2148–2159CrossRefGoogle Scholar
  63. Tevini M, Teramura AH (1989) UV-B effects on terrestrial plants. Photochem Photobiol 50:479–487CrossRefGoogle Scholar
  64. Tilbrook KK, Dubois M, Crocco CD, Yin R, Chappuis R, Allorent G, Schmid-Siegert E, Goldschmidt-Clermont M, Ulma R (2016) UV-B perception and acclimation in Chlamydomonas reinhardtii. Plant Cell 28:966–983PubMedPubMedCentralGoogle Scholar
  65. Ulm R, Baumann A, Oravecz A (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. PNAS 101:1397–1402CrossRefGoogle Scholar
  66. 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
  67. Wu D, Hu Q, Yan Z, Chen W, Yan C, Huang X, Zhang J, Yang P, Deng H, Wang J, Deng X, Shi Y (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–219CrossRefGoogle Scholar
  68. Yi C, Deng XW (2005) COP1—from plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol 15:618–625CrossRefGoogle Scholar
  69. Yi C, Li S, Chen X, Wiemer EA, Wang J, Wei N, Deng XW (2005) Major vault protein, in concert with constitutively photomorphogenic 1, negatively regulates c-Jun-mediated activator protein 1 transcription in mammalian cells. Cancer Res 65:5835–5840CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Plant Biology, Faculty of Natural SciencesUniversity of TabrizTabrizIran
  2. 2.Department of Cellular and Developmental Biology of PlantsUniversity of BielefeldBielefeldGermany
  3. 3.CNSAC MedShop GmbHSt. PöltenAustria

Personalised recommendations