Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Photoperiodism and photocontrol of stem elongation in two photomorphogenic mutants of Pisum sativum L.

  • 87 Accesses

  • 20 Citations

Abstract

The photomorphogenic mutation lv in the garden pea (Pisum sativum L.), which appears to reduce the response to light-stable phytochrome, has been isolated on a tall, late photoperiodic genetic background and its effects further characterised. Plants possessing lv have a reduced flowering response to photoperiod relative to wild-type plants, indicating that light-stable phytochrome may have a flower-inhibitory role in the flowering response of long-day plants to photoperiod. In general, lv plants are longer and have reduced leaf development relative to Lv plants. These differences are maximised under continuous light from fluorescent lamps (containing negligible far-red (FR) light), and decrease with addition of FR to the incident light. Enrichment of white light from fluorescent lamps with FR promotes stem elongation in the wild type but causes a reduction in elongation in the lv mutant. This “negative” shade-avoidance response appears to be the consequence of a strong inhibitory effect of light rich in FR, revealed in lv plants in the absence of a normal response to red (R) light. These results indicate that the wild-type response to the R: FR ratio may be comprised of two distinct photoresponses, one in which FR supplementation promotes elongation by reducing the inhibitory effect of R, and the other in which light rich in FR actively inhibits elongation. This hypothesis is discussed in relation to functional differentiation of phytochrome types in the light-grown plant. Gene lw has been reported previously to reduce internode length and the response to gibberellin A1, and to delay flowering. The present study shows that the lw mutation confers an increased response to photoperiod. In all these responses the lw phenotype is superficially “opposite” to the lv phenotype. The possibility that the mutation might primarily affect light perception was therefore considered. The degree of dwarfing of lw plants was found to depend upon light quality and quantity. Dwarfing is more extreme in plants grown under continuous R light than in those grown in continuous FR or blue light or in darkness. Studies of the fluence-rate response show that the lw mutation imparts a lower fluence requirement for inhibition of elongation by white light from fluorescent lamps. Dark-grown lw plants are more strongly inhibited by a R pulse than are wild-type plants but, as in the wild type, this inhibition remains reversible by FR. Light-grown lw plants show an exaggerated elongation response to end-of-day FR light. Taken together, these findings indicate that the lw mutant may be hypersensitive to phytochrome action.

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

Abbreviations

B:

blue light

cv:

cultivar

EOD-FR:

end-of-day far-red light

FR:

far-red light

GA:

gibberellin

Pfr :

far-redlight-absorbing form of phytochrome

phyA, phyB:

phytochromes A, B

R:

red light

W:

white light

WT:

wild type

References

  1. Abe, H., Yamamoto, K.T., Nagatani, A., Furuya, M. (1985) Characterization of green tissue-specific phytochrome isolated immunochemically from pea seedlings. Plant Cell Physiol. 26, 1387–1399

  2. Adamse, P., Jaspers, P.A.P.M., Kendrick, R.E., Koornneef, M. (1987) Photomorphogenic responses of a long-hypocotyl mutant of Cucumis sativus L. J. Plant Physiol. 127, 481–491

  3. Adamse, P., Jaspers, P.A.P.M., Bakker, J.A., Kendrick, R.E., Koornneef, M. (1988a) Photophysiology and phytochrome content of long-hypocotyl mutant and wild-type cucumber seedlings. Plant Physiol. 87, 264–268

  4. Adamse, P., Jaspers, P.A.P.M., Bakker, J.A., Wesselius, J.C., Heeringa, G.H., Kendrick, R.E., Koornneef, M. (1988b) Photophysiology of a tomato mutant deficient in labile phytochrome. J. Plant Physiol. 133, 436–440

  5. Beggs, C.J., Holmes, M.G., Jabben, M., Schafer, E. (1980) Action spectra for the inhibition of hypocotyl growth by continuous irradiation in light and dark-grown Sinapis alba L. seedlings. Plant Physiol. 66, 615–618

  6. Boylan, M.T., Quail, P.H. (1989) Oat phytochrome is biologically active in transgenic tomatoes. Plant Cell. 1, 765–773

  7. Boylan, M.T., Quail, P.H. (1991) Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc. Natl. Acad. Sci. USA 88, 10806–10810

  8. Carr-Smith, H.D., Johnson, C.B., Thomas, B. (1989) Action spectrum for the effect of day-extensions on flowering and apex elongation in green, light-grown wheat (Triticum aestivum L.). Planta 179, 428–432

  9. Chory, J., Peto, C.A., Ashbaugh, M., Saganich, R., Pratt, L.H., Ausubel, F. (1989) Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants. Plant Cell. 1, 867–880

  10. Dehesh, K., Tepperman, J., Christensen, A.H., Quail, P.H. (1991) phyB is evolutionarily conserved and constitutively expressed in rice seedling shoots. Mol. Gen. Genet. 225, 305–313

  11. Evans, L.T. (1976) Inflorescence initiation in Lolium temulentum L. XIV. The role of phytochrome in long day induction. Aust. J. Plant Physiol. 3, 207–217

  12. Furuya, M. (1989) Molecular properties and biogenesis of phytochrome I and II. Adv. Biophys. 25, 133–167

  13. Goto, N., Kumagai, T., Koornneef, M. (1991) Flowering responses to light-breaks in photomorphogenic mutants of Arabidopsis thaliana, a long-day plant. Physiol. Plant. 83, 209–215

  14. Holland, R.W.K., Vince, D. (1971) Floral initiation in Lolium temulentum L.: The role of phytochrome in the responses to red and far-red light. Planta 98, 232–243

  15. Jolly, C.J., Reid, J.B., Ross, J.J. (1987) Internode length in Pisum. Action of gene lw. Physiol. Plant. 69, 489–498

  16. Kay, S.A., Nagatani, A., Keith, B., Deak, M., Furuya, M., Chua, N.-H. (1989) Rice phytochrome is biologically active in transgenic tobacco. Plant Cell. 1, 775–782

  17. Keller, J.M., Shanklin, J., Vierstra, R.D., Hershey, H.P. (1989) Expression of a functional monocotyledonous phytochrome in transgenic tobacco. EMBO J. 8, 1005–1012

  18. Konomi, K., Abe, H., Furuya, M. (1987) Changes in content of phytochrome I and II apoproteins in embryonic axes of pea seeds during imbibition. Plant Cell Physiol. 28, 1443–1451

  19. Koornneef, M., Rolff, E., Spruit, C.J.P. (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z. Pflanzenphysiol. 100, 147–160

  20. Koornneef, M., Cone, J.W., Dekens, R.G., O'Herne-Roberts, E.G., Spruit, C.J.P., Kendrick, R.E. (1985) Photomorphogenic responses of long hypocotyl mutants of tomato. J. Plant Physiol. 120, 153–165

  21. Lopez-Juez, E., Buurmeijer, W.F., Heeringa, G.H., Kendrick, R.E., Wesselius, J.C. (1990a) Response of light-grown wild-type and long-hypocotyl mutant cucumber plants to end-of-day far-red light. Photochem. Photobiol. 52, 143–149

  22. Lopez-Juez, E., Nagatani, A., Buurmeijer, W.F., Peters, J.L., Furuya, M., Kendrick, R.E., Wesselius, J.C. (1990b) Response of light-grown wild-type and aurea mutant tomato plants to end-of-day far-red light. J. Photochem. Photobiol., B: Biology 4, 391–405

  23. Lopez-Juez, E., Nagatani, A., Tomizawa, K.-I., Deak, M., Kern, R., Kendrick, R.E., Furuya, M. (1992) The cucumber long-hypocotyl mutant lacks a light-stable PHYB-like phytochrome. Plant Cell. 4, 241–253

  24. Lumsden, P.J., Saji, H., Furuya, M. (1987) Action spectra confirm two separate actions of phytochrome in the induction of flowering in Lemna paucicostata 441. Plant Cell Physiol. 28, 1237–1242

  25. McCormac, A.C., Cherry, J.R., Hershey, H.P., Vierstra, R.D., Smith, H. (1991) Photoresponses of transgenic tobacco plants expressing an oat phytochrome gene. Planta 185, 162–170

  26. Murfet, I.C. (1985) Pisum sativum. In: Handbook of flowering, vol. 4, pp. 97–126, Halevy, A.H. ed. CRC Press, Boca Raton, Florida

  27. Nagatani, A., Reid, J.B., Ross, J.J., Dunnewijk, A., Furuya, M. (1990) Internode length in Pisum. The response to light quality, and phytochrome type I and II levels in lv plants. J. Plant Physiol. 135, 667–674

  28. Nagatani, A., Chory, J., Furuya, M. (1991a) Phytochrome B is not detectable in the hy3 mutant of Arabidopsis, which is deficient in responding to end-of-day far-red light treatments. Plant Cell Physiol. 32, 1119–1122

  29. Nagatani, A., Kay, S.A., Deak, M., Chua, N.-H., Furuya, M. (1991b) Rice type I phytochrome regulates hypocotyl elongation in transgenic tobacco seedlings. Proc. Natl. Acad. Sci. USA 88, 5207–5211

  30. Parks, B.M., Jones, A.M., Adamse, P., Koornneef, M., Kendrick, R.E., Quail, P.H. (1987) The aurea mutant of tomato is deficient is spectrophotometrically and immunochemically detectable phytochrome. Plant Mol. Biol. 9, 97–107

  31. Peters, J.L., van Tuinen, A., Adamse, P., Kendrick, R.E., Koornneef, M. (1989) High pigment mutants of tomato exhibit high sensitivity for phytochrome action. J. Plant Physiol. 134, 661–666

  32. Quail, P.H. (1991) Phytochrome: a light-activated molecular switch that regulates gene expression. Annu. Rev. Genet. 25, 389–409

  33. Reid, J.B. (1989) Genotype Le lv: an extremely long internode length type. Pisum Newslett. 21, 48–51

  34. Reid, J.B., Murfet, I.C. (1977) Flowering in Pisum: the effect of light quality on the genotype lf e Sn Hr. J. Exp. Bot. 28, 1357–1364

  35. Reid, J.B., Potts, W.C. (1986) Internode length in Pisum. Two further mutants, lh and ls, with reduced gibberellin synthesis, and a gibberellin insensitive mutant, lk. Physiol. Plant. 66, 417–426

  36. Reid, J.B., Ross, J.J. (1988) A new gene, lv, conferring an enhanced response to gibberellin A1. Physiol. Plant. 72, 595–604

  37. Reid, J.B., Ross, J.J. (1989) Internode length in Pisum. Two further gibberellin insensitivity genes, lka and lkb. Physiol. Plant. 75, 81–88

  38. Reid, J.B., Murfet, I.C., Potts, W.C. (1983) Internode length in Pisum. II. Additional information on the relationship and action of loci Le, La, Cry, Na and Lm. J. Exp. Bot. 34, 349–364

  39. Reid, J.B., Ross, J.J., Hasan, O. (1991) Internode length in Pisum: gene lkc. J. Plant Growth Regul. 10, 11–16

  40. Reid, J.B., Ross, J.J., Swain, S.M. (1992) Internode length in Pisum. A new, slender mutant with elevated levels of C19 gibberellins. Planta 188, 462–467

  41. Schneider, M.J., Borthwick, H.A., Hendricks, S.B. (1967) Effects of radiation on flowering of Hyoscyamus niger. Am. J. Bot. 54, 1241–1249

  42. Sharrock, R.A., Quail, P.H. (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution and differential expression of a plant regulatory photoreceptor family. Genes Dev. 3, 1745–1757

  43. Smith, H. (1982) Light quality, photoperception, and plant strategy. Annu Rev. Plant Physiol. 33, 481–518

  44. Smith, H., Whitelam, G.C. (1990) Phytochrome, a family of photoreceptors with multiple physiological roles. Plant Cell Environ. 13, 695–707

  45. Smith, H., Whitelam, G.C., McCormac, A.C. (1991) Do the members of the phytochrome family have different roles? Physiological evidence from wild-type, mutant and transgenic plants. In: Phytochrome properties and biological action, Thomas, B., Johnson, C.B. eds. Springer, Heidelberg

  46. Somers, D.E., Sharrock, R.A., Tepperman, J.M., Quail, P.H. (1991) The hy3 long hypocotyl mutant of Arabidopsis is deficient in phytochrome B. Plant Cell. 3, 1263–1274

  47. Takimoto, A., Saji, H. (1984) A role of phytochrome in photoperiodic induction: two-phytochrome-pool theory. Physiol. Plant. 61, 675–682

  48. Tomizawa, K.-L, Nagatani, A., Furuya, M. (1990) Phytochrome genes: Studies using the tools of molecular biology and photomorphogenic mutants. Photochem. Photobiol. 52, 265–275

  49. Vince-Prue, D. (1986) The duration of light and photoperiodic responses. In: Photomorphogenesis in plants, pp. 269–305, Kendrick, R.E., Kronenberg, G.H.M., eds. Martinus Nijhoff, Dordrecht

  50. Wagner, D., Tepperman, J.M., Quail, P.H. (1991) Overexpression of phytochrome B induces a short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell. 3, 1275–1288

  51. Wang, Y.-C., Stewart, S.J., Cordonnier, M.-M., Pratt, L.H. (1991) vena sativa L. contains three phytochromes, only one of which is abundant in etiolated tissue. Planta 184, 96–104

  52. Whitelam, G.C., Smith, H. (1991) Retention of phytochrome-mediated shade avoidance responses in phytochrome-deficient mutants of Arabidopsis, cucumber and tomato. J. Plant Physiol. 139, 119–125

Download references

Author information

Additional information

We thank Dr. T.A. La Rue and Dr. K.K. Sidorova for provision of seed, Katherine McPherson, Peter Bobbi, Leigh Johnson, Heidi Dungey and Douglas Madden for technical assistance, Dr. J.J. Ross for helpful discussion and critical reading of the manuscript, and the Australian Research Council for financial assistance. J.L.W. is in receipt of an Australian Postgraduate Research scholarship.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Weller, J.L., Reid, J.B. Photoperiodism and photocontrol of stem elongation in two photomorphogenic mutants of Pisum sativum L.. Planta 189, 15–23 (1993). https://doi.org/10.1007/BF00201338

Download citation

Key words

  • Elongation (stem)
  • Light (red: far-red ratio, end-of-day far-red)
  • Mutant (photomorphogenic)
  • Photoperiodism (flowering)
  • Phytochrome (response)
  • Pisum (mutant, photoperiodism)