Skip to main content
SpringerLink
Log in

Evidence for some common signal transduction events for opposite regulation of nitrate reductase and phytochrome-I gene expression by light

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have explored the possible involvement of the phosphoinositide (PI) cycle and protein kinase C (PKC) in the phytochrome (Pfr)-mediated light signal transduction pathway using nitrate reductase (NR) and phytochrome-I (PhyI) genes as model systems. We have shown earlier that phorbol myristate acetate (PMA) completely replaces the red light effect in stimulating nitrate reductase activity and transcript levels in maize. In this paper, we present detailed evidence to show that PMA mimics the red light effect and follows similar kinetics to enhance NR steady-state transcript accumulation in a nitrate-dependent manner. We also show that PMA inhibits phyI steady-state transcript accumulation in a manner similar to red light, indicating that a PKC-type enzyme(s) may be involved in mediating the light effect in both cases. Serotonin or 5-hydroxytryptamine (5-HT), a stimulator of PI turnover, was also found to mimic the red light effect in enhancing NR transcript levels and inhibiting phyI transcript accumulation, indicating the role of the PI cycle in generating second messengers for regulating the two genes. These results indicate that phytochrome-mediated light regulation of NR and phyI gene expression may involve certain common steps in the signal transduction pathway such as the PI cycle and protein phosphorylation by a PKC-type enzyme.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. AlgarraP, LinderS, ThummlerF: Biochemical evidence that phytochrome of the moss Ceratodon purpureus is a light regulated protein kinase. FEBS Lett 315: 69–73 (1993).

    Article  PubMed  Google Scholar 

  2. BossenME, KendrickRE, VrendenbergWJ: The involvement of a G-protein in phytochrome-regulated Ca2+-dependent swelling of wheat protoplasts. Physiol Plant 80: 55–62 (1990).

    Article  Google Scholar 

  3. BowlerC, NeuhausG, YamagataH, ChuaN-H: Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77: 73–81 (1994).

    Article  PubMed  Google Scholar 

  4. ChandokMR, SoporySK: Phorbol myristate acetate replaces phytochrome-mediated stimulation of nitrate reductase in maize. Phytochememistry 31: 2255–2258 (1992).

    Article  Google Scholar 

  5. ChandokMR, SoporySK: 5-Hydroxytryptamine affects turnover of polyphosphoinositides in maize and stimulates nitrate reductase in the absence of light. FEBS Lett 36: 39–42 (1994).

    Article  Google Scholar 

  6. ChomczynskiP: Solubilization in formamide protects RNA from degradation. Nucl Acids Res 20: 3791–3792 (1992).

    PubMed  Google Scholar 

  7. ChristensenAH, QuailPH: Structure and expression of a maize phytochrome encoding gene. Gene 85: 381–390 (1989).

    PubMed  Google Scholar 

  8. ColbertJT, HersheyHP, QuailPH: Phytochrome regulation of phytochrome mRNA abundance. Plant Mol Biol 5: 91–101 (1985).

    Google Scholar 

  9. DasR, SoporySK: Evidence for regulation of calcium uptake by phytochrome in maize protoplasts. Biochem Biophys Res Commun 128: 1455–1460 (1985).

    PubMed  Google Scholar 

  10. DengX-W: Fresh view of light signal transduction in plants. Cell 76: 423–426 (1994).

    Article  PubMed  Google Scholar 

  11. DooshiA, Aneeta, SoporySK: Regulation of protein phosphorylation by phytochrome in Sorghum bicolor. Photochem Photobiol 55: 465–468 (1992).

    Google Scholar 

  12. EinsapaharKJ, ThompsonGA: Transmembrane signalling via phosphatidylinositol 4,5 biphosphate hydrolysis in plants. Plant Physiol 93: 361–366 (1990).

    Google Scholar 

  13. FuruyaM: Molecular properties and biogenesis of phytochrome I and II. Arch Biophys 25: 133–137 (1989).

    Google Scholar 

  14. FuruyaM: Phytochromes: their molecular species, gene families, and functions. Annu Rev Plant Physiol Plant Mol Biol 44: 617–645 (1993).

    Article  Google Scholar 

  15. GilmartinPM, SarokinL, MemelinkJ, ChuaN-H: Molecular light switches for plant genes. Plant Cell 2: 369–378 (1990).

    Article  PubMed  Google Scholar 

  16. GowriG, CampbellWH: cDNA clones for corn leaf NADH nitrate reductase and chlorplast NAD(P)+ glyceraldehyde-3-phosphate dehydrogenase. Plant Physiol 90: 792–798 (1989).

    Google Scholar 

  17. HerrinDL, SchmidtGW: Rapid, reversible staining of northern blots prior to hybridization. Biotechniques 6: 196–199 (1988).

    PubMed  Google Scholar 

  18. HoffT, TruongH-N, CabocheM: The use of mutants and transgenic plants to study nitrate assimilation. Plant Cell Environ 17: 489–506 (1994).

    Google Scholar 

  19. KaySA, NagataniA, KeithB, DeakM, ChuaNH: Rice phytochrome is biologically active in transgenic tobacco. Plant Cell 1: 775–782 (1989).

    Article  PubMed  Google Scholar 

  20. KatagiriF, ChuaN-H: Plant transcription factors, present knowledge and future challenges. Trends Genet 8: 22–27 (1992).

    Article  PubMed  Google Scholar 

  21. KomatsuS, HiranoH: Protein kinase activity and protein phosphorylation in rice (Oryza sativa L.) leaf. Plant Sci 94: 127–137 (1993).

    Article  Google Scholar 

  22. KuhlemeierC: Transcriptional and post-transcriptional regulation of gene expression in plants. Plant Mol Biol 19: 1–14 (1992).

    PubMed  Google Scholar 

  23. LiH, RouxSJ: Purification and characterization of a casein kinase 2-type protein kinase from pea nuclei. Plant Physiol 99: 686–692 (1992).

    PubMed  Google Scholar 

  24. LiscumE, HangarterRP: Genetic evidence that the red-absorbing form of phytochrome B modulates gravitropism in Arabidopsis thaliana. Plant Physiol 103: 15–19 (1993).

    PubMed  Google Scholar 

  25. LogemannJ, SchellJ, WillmitzerL: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).

    PubMed  Google Scholar 

  26. MorelloL, GianiS, CoraggioI, BreviarioD: Rice membranes contain a calcium-dependent protein kinase activity with biochemical features of animal protein kinase C. Biochem Biophys Res Commun 197: 55–61 (1993).

    Article  PubMed  Google Scholar 

  27. NanmoriT, TaguchiW, KinugasaM, OjiY, SaharaS, FukamiY and KikkawaU: Purification and characterization of protein kinase C from a higher plant, Brassica campestris L. Biochem Biophys Res Commun 203: 311–38 (1994).

    Article  PubMed  Google Scholar 

  28. NeuhausG, BowlerC, KernR, ChuaN-H: Calcium/calmodulin-dependent and independent phytochrome signalling pathways. Cell 73: 937–952 (1993).

    Article  PubMed  Google Scholar 

  29. OlahZ, KissZ: Occurence of lipid and phorbol ester activated protein kinase in wheat cells. FEBS Lett 195: 33–37 (1986).

    Article  Google Scholar 

  30. ParkMH, ChaeQ: Intracellular protein phosphorylation in oat (Avena sativa L.) protoplasts by phytochrome action: involvement of protein kinase C. Biochem Biophys Res Commun 169: 1185–1190 (1990).

    PubMed  Google Scholar 

  31. QuailPH: Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annu Rev Genet 25: 389–409 (1991).

    Article  PubMed  Google Scholar 

  32. Raghuram N: Signal transduction and nitrate reductase gene expression in maize. Ph.D. Thesis, Jawaharlal Nehru University, New Delhi, India (1994).

  33. Raghuram N, Sopory SK: Light regulation of NR gene expression: mechanism and signal-response coupling. Physiol Mol Biol Plants (1995) (in press).

  34. RanjevaR, BoudetAM: Phosphorylation of protein in plants: regulatory effects and potential involvement in stimulus-response coupling. Annu Rev Plant Physiol 38: 73–93 (1987).

    Google Scholar 

  35. RaoLVM, DattaN, SoporySK, Guha-MukherjeeS: Phytochrome mediated induction of nitrate reductase in etiolated maize leaves. Physiol Plant 50: 208–212 (1980).

    Google Scholar 

  36. RobertsDM, HarmonAC: Calcium modulated proteins: targets of intracellular calcium signals in higher plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375–414 (1992).

    Article  Google Scholar 

  37. RomeroLC, BiswalB, SongPS: Protein phosphorylation in isolated nuclei from etiolated Avena seedlings: effects of red/far-red light and cholera toxin. FEBS Lett 282: 347–350 (1991).

    Article  PubMed  Google Scholar 

  38. RomeroLC, LamE: Guanine nucleotide binding protein involvement in early steps of phytochrome-regulated gene expression. Proc Natl Acad Sci USA 90: 1465–1469 (1993).

    PubMed  Google Scholar 

  39. RomeroLC, SommerD, GotorC, SongPS: G-proteins in etiolated Avena seedlings: possible phytochrome regulation. FEBS Lett 282: 341–346 (1991).

    Article  PubMed  Google Scholar 

  40. SambrookJ, FritschEF, ManiatisT: Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  41. SatoN: Nucleotide sequence and expression of the phytochrome gene in pisum sativum: differential regulation by light of multiple transcripts. Plant Mol Biol 11: 697–710 (1988).

    Google Scholar 

  42. SchindlerU, CashmoreAR: Photoregulated gene expression may involve ubiquitous DNA binding proteins. EMBO J 9: 3415–3427 (1990).

    PubMed  Google Scholar 

  43. Schneider-PoestchHAW: Signal transduction by phytochrome: phytochromes have a module related to the transmitter modules of bacterial sensor proteins. Photochem Photobiol 56: 839–846 (1992).

    PubMed  Google Scholar 

  44. SharmaAK, RaghuramN, ChandokMR, DasR, SoporySK: Investigations on the nature of the phytochrome-induced transmitter for the regulation of nitrate reductase in etiolated leaves of maize. J Exp Bot 45: 485–490 (1994).

    Google Scholar 

  45. SharmaAK, SoporySK: Independent effects of phytochrome and nitrate on nitrate reductase and nitrite reductase activities in maize. Photochem Photobiol 39: 491–493 (1984).

    Google Scholar 

  46. SharrockRA, QuailPH: Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution and differential expression of a plant regulatory photoreceptor family. Genes Devel 3: 1745–1757 (1989).

    PubMed  Google Scholar 

  47. SheenJ: Protein phosphatase activity is required for light inducible gene expression in maize. EMBO J 12: 3497–3505 (1993).

    PubMed  Google Scholar 

  48. SimpsonGG, ClarkG, BrownJWS: Isolation of a maize cDNA encoding a protein with extensive similarity to an inhibitor of protein kinase C and a cyanobacterial open reading frame. Biochim Biophys Acta 1222: 306–308 (1994).

    Article  PubMed  Google Scholar 

  49. SinghBR, SongPS: Phytochrome and protein phosphorylation. Photochem Photobiol 52: 249–254 (1990).

    PubMed  Google Scholar 

  50. SolomonsonLP, BarberMJ: Assimilatory nitrate reductase: functional properties and regulation. Annu Rev plant Physiol Plant Mol Biol 41: 225–253 (1990).

    Article  Google Scholar 

  51. TecottLH, JuliusD: A new wave of serotonin receptors. Curr Opin Neurobiol 3: 310–315 (1993).

    Article  PubMed  Google Scholar 

  52. ThompsonWF, WhiteMJ: Physiological and molecular studies of light regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42: 423–466 (1991).

    Article  Google Scholar 

  53. TirimanneTS, ColbertJT: Transient down-regulation of phytochrome mRNA abundance in etiolated cucumber cotyledons in response to continuous white light. Plant Physiol 97: 1581–1584 (1991).

    Google Scholar 

  54. TomizawaK, SatoN, FuruyaM: Phytochrome control of multiple transcripts of the phytochrome gene in Pisum sativum. Plant Mol Biol 12: 295–299 (1989).

    Google Scholar 

  55. TretynA, KendrickRE, WagnerG: The role(s) of calcium ions in phytochrome action. Photochem Photobiol 53: 1135–1156 (1991).

    Google Scholar 

  56. VierstraRD: Illuminating phytochrome functions: there is light at the end of the tunnel. Plant Physiol 103: 679–684 (1993).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Plant Physiology Laboratory, School of Life Sciences, Jawaharlal Nehru University, 110 067, New Delhi, India

    Nandula Raghuram & Sudhir K. Sopory

Authors
  1. Nandula Raghuram
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sudhir K. Sopory
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raghuram, N., Sopory, S.K. Evidence for some common signal transduction events for opposite regulation of nitrate reductase and phytochrome-I gene expression by light. Plant Mol Biol 29, 25–35 (1995). https://doi.org/10.1007/BF00019116

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00019116

Key words

Search

Navigation