Skip to main content
SpringerLink
Log in

Distinct leaf developmental and gene expression responses to light quantity depend on blue-photoreceptor or plastid-derived signals, and can occur in the absence of phototropins

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Leaf palisade cell development and the composition of chloroplasts respond to the fluence rate of light to maximise photosynthetic light capture while minimising photodamage. The underlying light sensory mechanisms are probably multiple and remain only partially understood. Phototropins (PHOT1 and PHOT2) are blue light receptors regulating responses which are light quantity-dependent and which include the control of leaf expansion. Here we show that genes for proteins in the reaction centres show long-term responses in wild type plants, and single blue photoreceptor mutants, to light fluence rate consistent with regulation by photosynthetic redox signals. Using contrasting intensities of white or broad-band red or blue light, we observe that increased fluence rate results in thicker leaves and greater number of palisade cells, but the anticlinal elongation of those cells is specifically responsive to the fluence rate of blue light. This palisade cell elongation response is still quantitatively normal in fully light-exposed regions of phot1 phot2 double mutants under increased fluence rate of white light. Plants grown at high light display elevated expression of RBCS (for the Rubisco small subunit) which, together with expected down-regulation of LHCB1 (for the photosynthetic antenna primarily of photosystem II), is also observed in phot double mutants. We conclude that an unknown blue light photoreceptor, or combination thereof, controls the development of a typical palisade cell morphology, but phototropins are not essential for either this response or acclimation-related gene expression changes. Together with previous evidence, our data further demonstrate that photosynthetic (chloroplast-derived) signals play a central role in the majority of acclimation responses.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

PHOT1, 2:

Phototropin 1, 2

Rubisco:

Ribulose bis-phosphate carboxylase-oxygenase

References

  • Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801

    Article  PubMed  CAS  Google Scholar 

  • Bailey S, Horton P, Walters RG (2004) Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 218:793–802

    Article  PubMed  CAS  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  PubMed  CAS  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee M, Sparvoli S, Edmunds C, Garosi P, Findlay K, Martin C (1996) DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 15:4194–4207

    PubMed  CAS  Google Scholar 

  • Chen YB, Durnford DG, Koblizek M, Falkowski PG (2004) Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol 136:3737–3750

    Article  PubMed  CAS  Google Scholar 

  • Escoubas JM, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92:10237–10241

    Article  PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Bräutigam K, Pfannschmidt T (2005a) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56:1491–1498

    Article  PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Bräutigam K, Wirtz M, Hell R, Dietzmann A, Dario Leister D, Oelmüller R Pfannschmidt T (2005b) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328

    Article  PubMed  CAS  Google Scholar 

  • Harada A, Sakai T, Okada K (2003) phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc Natl Acad Sci USA 100:8583–8588

    Article  PubMed  CAS  Google Scholar 

  • Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Im C-S, Eberhard S, Huang K, Beck CF, Grossman AR (2006) Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J 48:1–16

    Article  PubMed  CAS  Google Scholar 

  • Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954

    Article  PubMed  CAS  Google Scholar 

  • Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654–657

    Article  PubMed  CAS  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

    Article  PubMed  CAS  Google Scholar 

  • Keddie JS, Carroll B, Jones JD, Gruissem W (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J 15:4208–4217

    PubMed  CAS  Google Scholar 

  • Kim G-T, Yano S, Kozuka T, Tsukaya H (2005) Photomorphogenesis of leaves: shade-avoidance syndrome and differentiation of sun/shade leaves. Photochem Photobiol Sci 4:770–774

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol 77:226–233

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Kagawa T (2006) Phototropin and light-signaling in phototropism. Curr Opin Plant Biol 9:503–508

    Article  PubMed  CAS  Google Scholar 

  • Kozuka T, Horiguchi G, Kim GT, Ohgishi M, Sakai T, Tsukaya H (2005) The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar. Plant Cell Physiol 46:213–223

    Article  PubMed  CAS  Google Scholar 

  • Kruk J, Karpinski S (2006) An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone-pool and its redox state in thylakoids of Arabidopsis. Biochim Biophys Acta 1757:1669–1675

    Article  PubMed  CAS  Google Scholar 

  • Lin C (2002) Blue light receptors and signal transduction. Plant Cell 14:S207–S225

    PubMed  CAS  Google Scholar 

  • López-Juez E, Baynton CE, Page AM, Pyke KA, Robertson S, Vinti G (1999) Multiple light and plastid signals control chloroplast development in Arabidopsis. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer, Dordrecht, pp 2805–2808

    Google Scholar 

  • Mao J, Zhang Y-C, Sang Y, Li Q-H, Yang H-Q (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102:12270–12275

    Article  PubMed  CAS  Google Scholar 

  • Maxwell DP, Laudenbach DE, Huner NPA (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109:787–795

    PubMed  CAS  Google Scholar 

  • Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. J Exp Bot 556:449–460

    Google Scholar 

  • Ohgishi M, Saji K, Okada K, Sakai T (2004) Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc Natl Acad Sci USA 101:2223–2228

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397:625–628

    Article  CAS  Google Scholar 

  • Pfannschmidt T, Schütze K, Brost M, Oelmüller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276:36125–36130

    Article  PubMed  CAS  Google Scholar 

  • Pursiheimo S, Mulo P, Rintamäki E, Aro E-M (2001) Coregulation of light-harvesting complex II phosphorylation and lhcb mRNA accumulation in winter rye. Plant J 26:317–327

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735

    Article  PubMed  CAS  Google Scholar 

  • Sawbridge TI, López-Juez E, Knight MR, Jenkins GI (1994) A blue-light photoreceptor mediates the fluence-rate-dependent control of rbcS gene expression in light-grown Phaseolus vulgaris primary leaves. Planta 192:1–8

    CAS  Google Scholar 

  • Schuerger AC, Brown CS, Stryjewski EC (1997) Anatomical features of pepper plants (Capsicum annuum L.) grown under red light-emitting diodes supplemented with blue or far-red light. Ann Bot 79:273–282

    Article  PubMed  CAS  Google Scholar 

  • Takemiya A, Inoue S, Doi M, Kinoshita T, Shimazaki K (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120–1127

    Article  PubMed  CAS  Google Scholar 

  • Tan W, Bögre L, López-Juez E (2007) Light fluence-rate and chloroplasts are sources of signals controlling mesophyll cell morphogenesis and division. Cell Biol Int (in press)

  • Trojan A, Gabryś H (1996) Chloroplast distribution in Arabidopsis thaliana (L.) depends on light conditions during growth. Plant Physiol 111:419–425

    PubMed  CAS  Google Scholar 

  • Vener AV, Van Kan PJ, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94:1585–1590

    Article  PubMed  CAS  Google Scholar 

  • Vinti G, Fourrier N, Bowyer JR, López-Juez E (2005) Arabidopsis cue mutants with defective plastids are impaired primarily in the photocontrol of expression of photosynthesis-associated nuclear genes. Plant Mol Biol 57:343–357

    Article  PubMed  CAS  Google Scholar 

  • Vogelmann TC (2002) Photosynthesis: physiological and ecological considerations. In: Taiz L, Zeiger E (eds) Plant physiology. Sinauer, Sunderland, pp 171–192

    Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  PubMed  CAS  Google Scholar 

  • Walters RG, Rogers JJM, Shephard F, Horton P (1999) Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209:517–527

    Article  PubMed  CAS  Google Scholar 

  • Weston E, Thorogood K, Vinti G, López-Juez E (2000) Light quantity controls leaf-cell and chloroplast development in Arabidopsis thaliana wild type and blue light-perception mutants. Planta 211:807–815

    Article  PubMed  CAS  Google Scholar 

  • Wilson KE, Sieger SM, Huner NPA (2003) The temperature-dependent accumulation of Mg-protoporphyrin IX and reactive oxygen species in Chlorella vulgaris. Physiol Plant 119:126–136

    Article  CAS  Google Scholar 

  • Yang DH, Andersson B, Aro EM, Ohad I (2001) The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation: cytochrome b 6 f deficient Lemna perpusilla plants are locked in a state of high-light acclimation. Photosynth Res 68:163–174

    Article  PubMed  CAS  Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b 6 f complexes controls the activation of the LHCII kinase. EMBO J 11:2961–2969

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Astrid Wingler (University College London, UK) for assistance with chlorophyll fluorescence measurements, and to three anonymous reviewers for their suggestions and constructive criticisms. This work was supported by grants from the UK BBSRC, and by a travel bursary from the British Council. This manuscript is dedicated to the memory of Prof. John R. Bowyer (1955–2006), a photosynthesis pioneer and a source of continuous insights and inspiration.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    Enrique López-Juez & John R. Bowyer

  2. Laboratory for Genetic Regulatory Systems, Genomic Function Research Group, RIKEN Plant Science Centre, 1-7-22 Suechiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Tatsuya Sakai

Authors
  1. Enrique López-Juez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John R. Bowyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuya Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enrique López-Juez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

López-Juez, E., Bowyer, J.R. & Sakai, T. Distinct leaf developmental and gene expression responses to light quantity depend on blue-photoreceptor or plastid-derived signals, and can occur in the absence of phototropins. Planta 227, 113–123 (2007). https://doi.org/10.1007/s00425-007-0599-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0599-7

Keywords

Search

Navigation