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. 1998 Jun;10(6):889–904. doi: 10.1105/tpc.10.6.889

An Arabidopsis mutant hypersensitive to red and far-red light signals.

T Genoud 1, A J Millar 1, N Nishizawa 1, S A Kay 1, E Schäfer 1, A Nagatani 1, N H Chua 1
PMCID: PMC144040  PMID: 9634578

Abstract

A new mutant called psi2 (for phytochrome signaling) was isolated by screening for elevated activity of a chlorophyll a/b binding protein-luciferase (CAB2-LUC) transgene in Arabidopsis. This mutant exhibited hypersensitive induction of CAB1, CAB2, and the small subunit of ribulose-1,5-bisphosphate carboxylase (RBCS) promoters in the very low fluence range of red light and a hypersensitive response in hypocotyl growth in continuous red light of higher fluences. In addition, at high- but not low-light fluence rates, the mutant showed light-dependent superinduction of the pathogen-related protein gene PR-1a and developed spontaneous necrotic lesions in the absence of any pathogen. Expression of genes responding to various hormone and environmental stress pathways in the mutant was not significantly different from that of the wild type. Analysis of double mutants demonstrated that the effects of the psi2 mutation are dependent on both phytochromes phyA and phyB. The mutation is recessive and maps to the bottom of chromosome 5. Together, our results suggest that PSI2 specifically and negatively regulates both phyA and phyB phototransduction pathways. The induction of cell death by deregulated signaling pathways observed in psi2 is reminiscent of retinal degenerative diseases in animals and humans.

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Selected References

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  1. Ahmad M., Cashmore A. R. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature. 1993 Nov 11;366(6451):162–166. doi: 10.1038/366162a0. [DOI] [PubMed] [Google Scholar]
  2. Ahmad M., Cashmore A. R. The blue-light receptor cryptochrome 1 shows functional dependence on phytochrome A or phytochrome B in Arabidopsis thaliana. Plant J. 1997 Mar;11(3):421–427. doi: 10.1046/j.1365-313x.1997.11030421.x. [DOI] [PubMed] [Google Scholar]
  3. Barnes S. A., McGrath R. B., Chua N. H. Light signal transduction in plants. Trends Cell Biol. 1997 Jan;7(1):21–26. doi: 10.1016/S0962-8924(97)10043-5. [DOI] [PubMed] [Google Scholar]
  4. Barnes S. A., Quaggio R. B., Whitelam G. C., Chua N. H. fhy1 defines a branch point in phytochrome A signal transduction pathways for gene expression. Plant J. 1996 Dec;10(6):1155–1161. doi: 10.1046/j.1365-313x.1996.10061155.x. [DOI] [PubMed] [Google Scholar]
  5. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  6. Bell E., Mullet J. E. Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 1993 Dec;103(4):1133–1137. doi: 10.1104/pp.103.4.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bowler C., Neuhaus G., Yamagata H., Chua N. H. Cyclic GMP and calcium mediate phytochrome phototransduction. Cell. 1994 Apr 8;77(1):73–81. doi: 10.1016/0092-8674(94)90236-4. [DOI] [PubMed] [Google Scholar]
  8. Bowler C., Yamagata H., Neuhaus G., Chua N. H. Phytochrome signal transduction pathways are regulated by reciprocal control mechanisms. Genes Dev. 1994 Sep 15;8(18):2188–2202. doi: 10.1101/gad.8.18.2188. [DOI] [PubMed] [Google Scholar]
  9. Casal J. J., Boccalandro H. Co-action between phytochrome B and HY4 in Arabidopsis thaliana. Planta. 1995;197(2):213–218. doi: 10.1007/BF00202639. [DOI] [PubMed] [Google Scholar]
  10. Castle L. A., Meinke D. W. A FUSCA gene of Arabidopsis encodes a novel protein essential for plant development. Plant Cell. 1994 Jan;6(1):25–41. doi: 10.1105/tpc.6.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chory J., Peto C., Feinbaum R., Pratt L., Ausubel F. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell. 1989 Sep 8;58(5):991–999. doi: 10.1016/0092-8674(89)90950-1. [DOI] [PubMed] [Google Scholar]
  12. Conceiço A. da S., Krebbers E. A cotyledon regulatory region is responsible for the different spatial expression patterns of Arabidopsis 2S albumin genes. Plant J. 1994 Apr;5(4):493–505. doi: 10.1046/j.1365-313x.1994.05040493.x. [DOI] [PubMed] [Google Scholar]
  13. Deng X. W., Matsui M., Wei N., Wagner D., Chu A. M., Feldmann K. A., Quail P. H. COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell. 1992 Nov 27;71(5):791–801. doi: 10.1016/0092-8674(92)90555-q. [DOI] [PubMed] [Google Scholar]
  14. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  15. Dietrich R. A., Richberg M. H., Schmidt R., Dean C., Dangl J. L. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell. 1997 Mar 7;88(5):685–694. doi: 10.1016/s0092-8674(00)81911-x. [DOI] [PubMed] [Google Scholar]
  16. Dolferus R., Jacobs M., Peacock W. J., Dennis E. S. Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol. 1994 Aug;105(4):1075–1087. doi: 10.1104/pp.105.4.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dolph P. J., Ranganathan R., Colley N. J., Hardy R. W., Socolich M., Zuker C. S. Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science. 1993 Jun 25;260(5116):1910–1916. doi: 10.1126/science.8316831. [DOI] [PubMed] [Google Scholar]
  18. Dryja T. P., Finn J. T., Peng Y. W., McGee T. L., Berson E. L., Yau K. W. Mutations in the gene encoding the alpha subunit of the rod cGMP-gated channel in autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10177–10181. doi: 10.1073/pnas.92.22.10177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Farrar G. J., Kenna P., Jordan S. A., Kumar-Singh R., Humphries M. M., Sharp E. M., Sheils D. M., Humphries P. A three-base-pair deletion in the peripherin-RDS gene in one form of retinitis pigmentosa. Nature. 1991 Dec 12;354(6353):478–480. doi: 10.1038/354478a0. [DOI] [PubMed] [Google Scholar]
  20. Feinbaum R. L., Ausubel F. M. Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol Cell Biol. 1988 May;8(5):1985–1992. doi: 10.1128/mcb.8.5.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gil P., Liu Y., Orbović V., Verkamp E., Poff K. L., Green P. J. Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol. 1994 Feb;104(2):777–784. doi: 10.1104/pp.104.2.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Goodman O. B., Jr, Krupnick J. G., Santini F., Gurevich V. V., Penn R. B., Gagnon A. W., Keen J. H., Benovic J. L. Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature. 1996 Oct 3;383(6599):447–450. doi: 10.1038/383447a0. [DOI] [PubMed] [Google Scholar]
  23. Green R., Fluhr R. UV-B-Induced PR-1 Accumulation Is Mediated by Active Oxygen Species. Plant Cell. 1995 Feb;7(2):203–212. doi: 10.1105/tpc.7.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Greenberg J. T., Ausubel F. M. Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 1993 Aug;4(2):327–341. doi: 10.1046/j.1365-313x.1993.04020327.x. [DOI] [PubMed] [Google Scholar]
  25. Greenberg J. T., Guo A., Klessig D. F., Ausubel F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. doi: 10.1016/0092-8674(94)90217-8. [DOI] [PubMed] [Google Scholar]
  26. Hoisington D. A., Neuffer M. G., Walbot V. Disease lesion mimics in maize. I. Effect of genetic background, temperature, developmental age, and wounding on necrotic spot formation with Les1. Dev Biol. 1982 Oct;93(2):381–388. doi: 10.1016/0012-1606(82)90125-7. [DOI] [PubMed] [Google Scholar]
  27. Jabs T., Dietrich R. A., Dangl J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996 Sep 27;273(5283):1853–1856. doi: 10.1126/science.273.5283.1853. [DOI] [PubMed] [Google Scholar]
  28. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  29. Kurkela S., Borg-Franck M. Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol. 1992 Jul;19(4):689–692. doi: 10.1007/BF00026794. [DOI] [PubMed] [Google Scholar]
  30. Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  32. Li H. M., Altschmied L., Chory J. Arabidopsis mutants define downstream branches in the phototransduction pathway. Genes Dev. 1994 Feb 1;8(3):339–349. doi: 10.1101/gad.8.3.339. [DOI] [PubMed] [Google Scholar]
  33. Li Hm., Culligan K., Dixon R. A., Chory J. CUE1: A Mesophyll Cell-Specific Positive Regulator of Light-Controlled Gene Expression in Arabidopsis. Plant Cell. 1995 Oct;7(10):1599–1610. doi: 10.1105/tpc.7.10.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mayer R., Raventos D., Chua N. H. det1, cop1, and cop9 mutations cause inappropriate expression of several gene sets. Plant Cell. 1996 Nov;8(11):1951–1959. doi: 10.1105/tpc.8.11.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McLaughlin M. E., Sandberg M. A., Berson E. L., Dryja T. P. Recessive mutations in the gene encoding the beta-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat Genet. 1993 Jun;4(2):130–134. doi: 10.1038/ng0693-130. [DOI] [PubMed] [Google Scholar]
  36. Millar A. J., Carré I. A., Strayer C. A., Chua N. H., Kay S. A. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science. 1995 Feb 24;267(5201):1161–1163. doi: 10.1126/science.7855595. [DOI] [PubMed] [Google Scholar]
  37. Millar A. J., Kay S. A. Circadian Control of cab Gene Transcription and mRNA Accumulation in Arabidopsis. Plant Cell. 1991 May;3(5):541–550. doi: 10.1105/tpc.3.5.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Millar A. J., Short S. R., Chua N. H., Kay S. A. A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell. 1992 Sep;4(9):1075–1087. doi: 10.1105/tpc.4.9.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nagatani A., Kay S. A., Deak M., Chua N. H., Furuya M. Rice type I phytochrome regulates hypocotyl elongation in transgenic tobacco seedlings. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5207–5211. doi: 10.1073/pnas.88.12.5207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nagatani A., Reed J. W., Chory J. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A. Plant Physiol. 1993 May;102(1):269–277. doi: 10.1104/pp.102.1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Neuhaus G., Bowler C., Kern R., Chua N. H. Calcium/calmodulin-dependent and -independent phytochrome signal transduction pathways. Cell. 1993 Jun 4;73(5):937–952. doi: 10.1016/0092-8674(93)90272-r. [DOI] [PubMed] [Google Scholar]
  42. Pepper A., Delaney T., Washburn T., Poole D., Chory J. DET1, a negative regulator of light-mediated development and gene expression in arabidopsis, encodes a novel nuclear-localized protein. Cell. 1994 Jul 15;78(1):109–116. doi: 10.1016/0092-8674(94)90577-0. [DOI] [PubMed] [Google Scholar]
  43. Phillips A. L., Huttly A. K. Cloning of two gibberellin-regulated cDNAs from Arabidopsis thaliana by subtractive hybridization: expression of the tonoplast water channel, gamma-TIP, is increased by GA3. Plant Mol Biol. 1994 Feb;24(4):603–615. doi: 10.1007/BF00023557. [DOI] [PubMed] [Google Scholar]
  44. Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. Phytochromes: photosensory perception and signal transduction. Science. 1995 May 5;268(5211):675–680. doi: 10.1126/science.7732376. [DOI] [PubMed] [Google Scholar]
  45. Rabino I., Mancinelli A. L. Light, temperature, and anthocyanin production. Plant Physiol. 1986 Jul;81(3):922–924. doi: 10.1104/pp.81.3.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Somers D. E., Sharrock R. A., Tepperman J. M., Quail P. H. The hy3 Long Hypocotyl Mutant of Arabidopsis Is Deficient in Phytochrome B. Plant Cell. 1991 Dec;3(12):1263–1274. doi: 10.1105/tpc.3.12.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Takahashi T., Gasch A., Nishizawa N., Chua N. H. The DIMINUTO gene of Arabidopsis is involved in regulating cell elongation. Genes Dev. 1995 Jan 1;9(1):97–107. doi: 10.1101/gad.9.1.97. [DOI] [PubMed] [Google Scholar]
  48. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Vorst O., Kock P., Lever A., Weterings B., Weisbeek P., Smeekens S. The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J. 1993 Dec;4(6):933–945. doi: 10.1046/j.1365-313x.1993.04060933.x. [DOI] [PubMed] [Google Scholar]
  50. Wagner D., Hoecker U., Quail P. H. RED1 is necessary for phytochrome B-mediated red light-specific signal transduction in Arabidopsis. Plant Cell. 1997 May;9(5):731–743. doi: 10.1105/tpc.9.5.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wagner D., Tepperman J. M., Quail P. H. Overexpression of Phytochrome B Induces a Short Hypocotyl Phenotype in Transgenic Arabidopsis. Plant Cell. 1991 Dec;3(12):1275–1288. doi: 10.1105/tpc.3.12.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wang L. Y., Taverna F. A., Huang X. P., MacDonald J. F., Hampson D. R. Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science. 1993 Feb 19;259(5098):1173–1175. doi: 10.1126/science.8382377. [DOI] [PubMed] [Google Scholar]
  53. Wei N., Chamovitz D. A., Deng X. W. Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development. Cell. 1994 Jul 15;78(1):117–124. doi: 10.1016/0092-8674(94)90578-9. [DOI] [PubMed] [Google Scholar]
  54. Weymann K., Hunt M., Uknes S., Neuenschwander U., Lawton K., Steiner H. Y., Ryals J. Suppression and Restoration of Lesion Formation in Arabidopsis lsd Mutants. Plant Cell. 1995 Dec;7(12):2013–2022. doi: 10.1105/tpc.7.12.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Whitelam G. C., Johnson E., Peng J., Carol P., Anderson M. L., Cowl J. S., Harberd N. P. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell. 1993 Jul;5(7):757–768. doi: 10.1105/tpc.5.7.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Zhang L., Sports C. D., Osawa S., Weiss E. R. Rhodopsin phosphorylation sites and their role in arrestin binding. J Biol Chem. 1997 Jun 6;272(23):14762–14768. doi: 10.1074/jbc.272.23.14762. [DOI] [PubMed] [Google Scholar]

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