Advertisement

Planta

, Volume 231, Issue 3, pp 665–675 | Cite as

Light exaggerates apical hook curvature through phytochrome actions in tomato seedlings

  • Chizuko ShichijoEmail author
  • Hisako Ohuchi
  • Naoko Iwata
  • Yukari Nagatoshi
  • Miki Takahashi
  • Eri Nakatani
  • Kentaroh Inoue
  • Seiji Tsurumi
  • Osamu Tanaka
  • Tohru Hashimoto
Original Article

Abstract

Contrary to the established notion that the apical hook of dark-grown dicotyledonous seedlings opens in response to light, we found in tomato (Solanum lycopersicum L.) that the apical hook curvature is exaggerated by light. Experiments with several tomato cultivars and phytochrome mutants, irradiated with red and far-red light either as a brief pulse (Rp, FRp) or continuously (Rc, FRc), revealed: the hook-exaggeration response is maximal at the emergence of the hypocotyl from the seed; the effect of Rp is FRp-reversible; fluence–response curves to a single Rp or FRp show an involvement of low and very low fluence responses (LFR, VLFR); the effect of Rc is fluence-rate dependent, but that of FRc is not; the phyA mutant (phyA hp-1) failed to respond to an Rp of less than 10−2 μmol m−2 and to an FRp of all fluences tested as well as to FRc, thus indicating that the hook-exaggeration response involves phyA-mediated VLFR. The Rp fluence–response curve with the same mutant also confirmed the presence of an LFR mediated by phytochrome(s) other than phyA, although the phyB1 mutant (phyB1 hp-1) still showed full response probably due to other redundant phytochrome species (e.g., phyB2). Simulation experiments led to the possible significance of hook exaggeration in the field that the photoresponse may facilitate the release of seed coat when seeds germinate at some range of depth in soil. It was also observed that seed coat and/or endosperm are essential to the hook exaggeration.

Keywords

Apical hypocotyl hook High-pigment-1 Hook curvature Mutant Phytochrome Solanum lycopersicum L. 

Abbreviations

FR (FRp, FRc)

Far-red light (pulse of FR, continuous FR)

HIR

High-irradiance response

hp-1

High-pigment-1

LFR

Low fluence response

Pfr

FR-absorbing form of phytochrome

Pfr/P

Ratio of Pfr to total phytochrome

R (Rp, Rc)

Red light (pulse of R, continuous R)

VLFR

Very low fluence response

WL

White light

Notes

Acknowledgments

We thank Professor Richard E. Kendrick (Wageningen Agricultural University, Wageningen, The Netherlands) for supplying seeds of tomato mutants, and Professors Tetsuro Mimura and Taisaku Amakawa (Kobe University, Japan), and Mr. Nobuyuki Kawashima (President, Kyokko Trading Co, Tokyo, Japan) for their kind cooperation.

Supplementary material

Supplementary Movie S1: Time-lapse movie. Growth and hook curvature exaggeration in tomato seedlings under continuous WL, taken at 10-min intervals during 6 days (144 h). White fluorescent light, 17 μmol m−2 s−1. Cv. Ponte-Rosa Supplementary material 1 (MP4 4815 kb)

References

  1. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P, Hellmann H (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J 47:591–603PubMedCrossRefGoogle Scholar
  2. Botto JF, Sánchez RA, Whitelam GC, Casal JJ (1996) Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiol 110:439–444PubMedGoogle Scholar
  3. Casal JJ, Sánchez RA, Vierstra RD (1994) Avena phytochrome A overexpressed in transgenic tobacco seedlings differentially affects red/far-red reversible and very-low-fluence responses (cotyledon unfolding) during de-etiolation. Planta 192:306–309CrossRefGoogle Scholar
  4. Casal JJ, Sánchez RA, Botto JF (1998) Modes of action of phytochromes. J Exp Bot 49:127–138CrossRefGoogle Scholar
  5. Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E, Zheng N, Deng XW (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18:1991–2004PubMedCrossRefGoogle Scholar
  6. Clough RC, Casal JJ, Jordan ET, Christou P, Vierstra RD (1995) Expression of functional oat phytochrome A in transgenic rice. Plant Physiol 109:1039–1045PubMedCrossRefGoogle Scholar
  7. Cone JW, Jaspers PAPM, Kendrick RE (1985) Biphasic fluence–response curves for light induced germination of Arabidopsis thaliana seeds. Plant Cell Environ 8:605–612CrossRefGoogle Scholar
  8. Franklin KA, Allen T, Whitelam GC (2007) Phytochrome A is an irradiance-dependent red light sensor. Plant J 50:108–117PubMedCrossRefGoogle Scholar
  9. Goeschl JD, Pratt HK, Bonner BA (1967) An effect of light on the production of ethylene and the growth of the plumular portion of etiolated pea seedlings. Plant Physiol 42:1077–1080PubMedCrossRefGoogle Scholar
  10. Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis. Plant Physiol 105:141–149PubMedCrossRefGoogle Scholar
  11. Kang BG, Ray PM (1969) Ethylene and carbon dioxide as mediators in the response of the bean hypocotyl hook to light and auxins. Planta 87:206–216CrossRefGoogle Scholar
  12. Kerckhoffs LHJ, van Tuinen A, Hauser BA, Cordonnier-Pratt M-M, Nagatani A, Koornneef M, Pratt LH, Kendrick RE (1996) Molecular analysis of tri-mutant alleles in tomato indicates the Tri locus is the gene encoding the apoprotein of phytochrome B1. Planta 199:152–157CrossRefGoogle Scholar
  13. Kerckhoffs LHJ, de Groot NAMA, van Tuinen A, Schreuder MEL, Nagatani A, Koornneef M, Kendrick RE (1997a) Physiological characterization of exaggerated-photoresponse mutants of tomato. J Plant Physiol 150:578–587Google Scholar
  14. Kerckhoffs LHJ, Schreuder MEL, van Tuinen A, Koornneef M, Kendrick RE (1997b) Phytochrome control of anthocyanin biosynthesis in tomato seedlings: analysis using photomorphogenic mutants. Photochem Photobiol 65:374–381CrossRefGoogle Scholar
  15. Lazarova GI, Kerckhoffs LHJ, Brandstädter J, Matsui M, Kendrick RE, Cordonnier-Pratt M-M, Pratt LH (1998) Molecular analysis of PHYA in wild-type and phytochrome A-deficient mutants of tomato. Plant J 14:653–662PubMedCrossRefGoogle Scholar
  16. Lieberman M, Segev O, Gilboa N, Lalazar A, Levin I (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor Appl Genet 108:1574–1581PubMedCrossRefGoogle Scholar
  17. Liscum E, Hangarter RP (1993a) Light-stimulated apical hook opening in wild-type Arabidopsis thaliana seedlings. Plant Physiol 101:567–572PubMedGoogle Scholar
  18. Liscum E, Hangarter RP (1993b) Photomorphogenic mutants of Arabidopsis thaliana reveal activities of multiple photosensory systems during light-stimulated apical-hook opening. Planta 191:214–221CrossRefGoogle Scholar
  19. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101:9897–9902PubMedCrossRefGoogle Scholar
  20. Mancinelli AL (1994) The physiology of phytochrome action. In: Kendrick RE, Kronengerg GHM (eds) Photomorphogenesis in plants, 2nd edn. Kluwer, Dordrecht, pp 211–269CrossRefGoogle Scholar
  21. Mandoli DF, Briggs WR (1981) Phytochrome control of two low-irradiance responses in etiolated oat seedlings. Plant Physiol 67:733–739PubMedCrossRefGoogle Scholar
  22. Mazzella MA, Alconada Magliano TM, Casal JJ (1997) Dual effect of phytochrome A on hypocotyl growth under continuous red light. Plant Cell Environ 20:261–267CrossRefGoogle Scholar
  23. Mohr H, Noblé A (1960) Die Steuerung der Schliessung und Öffnung des Plumula-Hakens bei Keimlingen von Lactuca sativa durch sichtbare Strahlung. Planta 55:327–342CrossRefGoogle Scholar
  24. Peters JL, van Tuinen A, Adamse P, Kendrick RE, Koornneef M (1989) High pigment mutants of tomato exhibit high sensitivity for phytochrome action. J Plant Physiol 134:661–666Google Scholar
  25. Peters JL, Schreuder MEL, Verduin SJW, Kendrick RE (1992) Physiological characterization of a high-pigment mutant of tomato. Photochem Photobiol 56:75–82CrossRefGoogle Scholar
  26. Peters JL, Széll M, Kendrick RE (1998) The expression of light-regulated genes in the high-pigment-1 mutant of tomato. Plant Physiol 117:797–807PubMedCrossRefGoogle Scholar
  27. Shichijo C, Hashimoto T (1997) A red light signal distinct from the far-red-absorbing form of phytochrome in anthocyanin induction of Sorghum bicolor. J Photochem Photobiol B: Biol 38:70–75CrossRefGoogle Scholar
  28. Shichijo C, Hamada T, Hiraoka M, Johnson CB, Hashimoto T (1993) Enhancement of red-light-induced anthocyanin synthesis in sorghum first internodes by moderate low temperature given in the pre-irradiation culture period. Planta 191:238–245CrossRefGoogle Scholar
  29. Shichijo C, Onda S, Kawano R, Nishimura Y, Hashimoto T (1999) Phytochrome elicits the cryptic red-light signal which results in amplification of anthocyanin biosynthesis in sorghum. Planta 208:80–87CrossRefGoogle Scholar
  30. Shichijo C, Katada K, Tanaka O, Hashimoto T (2001) Phytochrome A-mediated inhibition of seed germination in tomato. Planta 213:764–769PubMedCrossRefGoogle Scholar
  31. Shinomura T, Nagatani A, Hanzawa H, Kubota M, Watanabe M, Furuya M (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:8129–8133PubMedCrossRefGoogle Scholar
  32. Staneloni RJ, Rodriguez-Batiller MJ, Legisa D, Scarpin MR, Agalou A, Cerdán PD, Meijer AH, Ouwerkerk PBF, Casal JJ (2009) Bell-like homeodomain selectively regulates the high-irradiance response of phytochrome A. Proc Natl Acad Sci USA 106:13624–13629PubMedCrossRefGoogle Scholar
  33. van Tuinen A, Kerckhoffs LHJ, Nagatani A, Kendrick RE, Koornneef M (1995a) Far-red light-insensitive, phytochrome A-deficient mutants of tomato. Mol Gen Genet 246:133–141PubMedCrossRefGoogle Scholar
  34. van Tuinen A, Kerckhoffs LHJ, Nagatani A, Kendrick RE, Koornneef M (1995b) A temporarily red light-insensitive mutant of tomato lacks a light-stable, B-like phytochrome. Plant Physiol 108:939–947PubMedGoogle Scholar
  35. Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55:89–103PubMedCrossRefGoogle Scholar
  36. Weller JL, Schreuder MEL, Smith H, Koornneef M, Kendrick RE (2000) Physiological interactions of phytochromes A, B1 and B2 in the control of development in tomato. Plant J 24:345–356PubMedCrossRefGoogle Scholar
  37. Weller JL, Perrotta G, Schreuder MEL, van Tuinen A, Koornneef M, Giuliano G, Kendrick RE (2001) Genetic dissection of blue-light sensing in tomato using mutants deficient in cryptochrome 1 and phytochromes A, B1 and B2. Plant J 25:427–440PubMedCrossRefGoogle Scholar
  38. Withrow RB, Klein WH, Elstad V (1957) Action spectra of photomorphogenic induction and its photoinactivation. Plant Physiol 32:453–462PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Chizuko Shichijo
    • 1
    Email author
  • Hisako Ohuchi
    • 2
  • Naoko Iwata
    • 2
  • Yukari Nagatoshi
    • 3
  • Miki Takahashi
    • 1
  • Eri Nakatani
    • 1
  • Kentaroh Inoue
    • 2
  • Seiji Tsurumi
    • 4
  • Osamu Tanaka
    • 2
  • Tohru Hashimoto
    • 5
  1. 1.Department of Biology, Graduate School of ScienceKobe UniversityKobeJapan
  2. 2.Faculty of Science and EngineeringKonan UniversityKobeJapan
  3. 3.Faculty of Human DevelopmentKobe UniversityKobeJapan
  4. 4.Center for Supports to Research and Education ActivitiesKobe UniversityKobeJapan
  5. 5.Uozaki Life Science LaboratoryKobeJapan

Personalised recommendations