Skip to main content

Light environment within a leaf. II. Progress in the past one-third century

Journal of Plant Research volume 129, pages 353–363 (2016)Cite this article

Abstract

Studies directly related to light environments within a leaf, conduced mainly in the past one-third century, are reviewed. In particular, studies that revealed the profiles of light absorption and photosynthetic capacity are highlighted. Progress in this research field has been accelerated by devising innovative techniques. Roles of the main photosynthetic tissues, the palisade and spongy tissues, as the light guide and diffuser, respectively, are discussed. When the leaf is illuminated with diffuse light, light is absorbed more by the chloroplasts located near the illuminated surface. The meanings of the occupation of the mesophyll surfaces facing the intercellular spaces by chloroplasts and chloroplast movement are also discussed. The discrepancy between the light absorption profile and that of photosynthetic capacity is examined most intensively.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allen WA, Richardson AJ (1968) Interaction of light with a plant canopy. J Opt Soc Am 58:1023–1031

    Article  Google Scholar 

  • Anderson JM (1986) Photoregulation of the compositeon, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136

    CAS  Article  Google Scholar 

  • Biel KY, Fomina IR, Nazarova GN, Soukhovolsky VG, Khleboporos RG, Nishio JN (2010) Untangling metabolic spatial interactions of stress tolerance in plants. 1. Patterns of carbon metabolism within leaves. Protoplasma 245:49–73. doi:10.1007/s00709-010-0135-7

    CAS  Article  PubMed  Google Scholar 

  • Bornmann JF, Vogelmann TC, Martin G (1991) Measurements of chlorophyll fluorescence within leaves using a fiber optic microprobe. Plant Cell Environ 14:719–725

    Article  Google Scholar 

  • Brodersen CR, Vogelmann TC (2010) Do changes in light direction affect absorption profiles in leaves? Funct Plant Biol 37:403–412

    Article  Google Scholar 

  • Brodersen CR, Vogelmann TC, Williams WE, Gorton HL (2008) A new paradigm in leaf-level photosynthesis: direct and diffuse lights are not equal. Plant Cell Environ 31:159–164. doi:10.1111/j.1365-3040.2007.01751.x

    CAS  PubMed  Google Scholar 

  • Brugnoli E, Björkman O (1992) Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth Res 32:23–35

    CAS  Article  PubMed  Google Scholar 

  • Clayton RK (1970) Light and living matter, vol 1. The physical part, McGraw-Hill, New York, p 148

  • Cui M, Vogelmann TC, Smith WK (1991) Chlorophyll and light gradients in sun and shade leaves of Spinacia oleracea. Plant Cell Environ 14:493–500

    Article  Google Scholar 

  • Evans JR, Vogelmann TC (2003) Profiles of 14C fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant Cell Enviro 26:547–560

    CAS  Article  Google Scholar 

  • Evans JR, Vogelmann TC (2006) Photosynthesis within isobilateral Eucalyptus pauciflora leaves. New Phytol 171:771–782

    CAS  Article  PubMed  Google Scholar 

  • Evans JR, Jakobsen I, Ögren E (1993) Photosynthetic light-response curves. 2. Gradients of light absorption and photosynthetic capacity. Planta 189:191–200

    CAS  Article  Google Scholar 

  • Farquhar GD (1989) Models of integrated photosynthesis of cells and leaves. Phil Trans R Soc London B 323:357–367

    CAS  Article  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: Leaf age as a control on the allocation program. Oecologia 56:41–347. doi:10.1007/BF00379710

    Article  Google Scholar 

  • Gal A, Brumfeld V, Weiner S, Addadi L, Oron D (2012) Certain biomenerals in leaves function as light scatterers. Adv Opt Mater 24:OP77–OP83. doi:10.1002/adma.201104548

    CAS  Google Scholar 

  • Gates DM (1980) Biophysical ecology. Springer Verlag, New York, p 611

    Book  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Article  Google Scholar 

  • Gorton HL, Williams WE, Vogelmann TC (1999) Chloroplast movement in Alocassia macrorrhiza. Physiol Plant 106:421–428

    CAS  Article  Google Scholar 

  • He J, Yang W, Qin L, Fan D-Y, Chow WS (2015) Photoinactivation of photosystem II in wild-type and chlorophyll b-less barley leaves: which mechanism dominates depends on experimental circumstances. Photosynth Res 126:399–407. doi:10.1007/s11120-015-0164-0

    CAS  Article  PubMed  Google Scholar 

  • Higa T, Wada M (2016) Chloroplast avoidance movement is not functional in plants grown under strong sunlight. Plant Cell Environ. doi:10.1111/pce.12681

    PubMed  Google Scholar 

  • Hirose T, Werger MJA (1987) Maimizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72:520–526

    Article  Google Scholar 

  • Inoue Y, Shibata K (1973) Light-induced chloroplast rearrangents and their action spectra as measured by absorption spectrophotometry. Planta 114:341–358

    CAS  Article  PubMed  Google Scholar 

  • Inoue Y, Shibata K (1974) Comparative examination of terrestrial plant leaves in terms of light-induced absorption changes due to chloroplast rearrangements. Plant Cell Physiol 15:717–721

    Google Scholar 

  • Johnson DM, Smith SK, Vogelmann TC, Brodersen CR (2005) Leaf architecture and direction of incident light influence mesophyll fluorescence profiles. Amer J Bot 92:1425–1431

    Article  Google Scholar 

  • Karabourniotis G, Bornman JF, Nikolopoulos D (2000) A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Qeurcus coccifera. Plant Cell Environ 23:423–430

    Article  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. doi:10.1038/nature01213

    CAS  Article  PubMed  Google Scholar 

  • Koizumi M, Takahashi K, Mineuchi K, Nakamura T, Kano H (1998) Light gradients and the transverse distribution of chlorophyll fluorescence in mangrove and Camellia leaves. Ann Bot 81:527–533

    CAS  Article  Google Scholar 

  • Kubelka VP, Munk F (1931) Ein Beitrag zur Optik der Farbanstriche. Z Tech Physik 11:593–601

    Google Scholar 

  • Kulandaivelu GA, Nooruden AM, Sampath PS, Pyriyana S, Rama K (1983) Assessment of the photosynthetic electron transport properties of upper and lower leaf sides in vivo by fluorometric method. Photosynthetica 17:206–209

    Google Scholar 

  • Losciale P, Oguchi R, Hendrickson L, Hope AB, Corelli-Grappadelli L, Chow WS (2008) A rapid, whole-tissue determination of the functional fraction of PSII after photoinhibition of leaves based on flash-induced P700 redox kinetics. Physiol Plant 132:23–32. doi:10.1111/j.1399-3054.2007.01000.x

    CAS  PubMed  Google Scholar 

  • Moss DN (1964) Optimum lighting of leaves. Crop Sci 4:131–136

    Article  Google Scholar 

  • Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotsis G (2002) The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiol 129:235–243

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nishio JN (2000) Why are higher plants green? Evolution of the higher plant photosynthetic pigment complement. Plant Cell Environ 23:539–548

    CAS  Article  Google Scholar 

  • Nishio JN, Sun J, Vogelmann TC (1993) Carbon fixation gradients across spinach leaves do not follow internal light gradient. Plant Cell 5:953–961

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ögren E, Evans JR (1993) Photosynthetic light-response curves. 1. The influence of CO2 partial pressure and leaf inversion. Planta 189:182–190

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hiura T, Hirose T (2006) Leaf anatomy and light acclimateion in woody seedlings after gap formation in a cool-temperate deciduous forest. Oecologia 149:571–582

    CAS  Article  PubMed  Google Scholar 

  • Oguchi R, Terashima I, Chow WS (2009) The involvement of dual mechanisms of photoinactivation of photosystem II in Capsicum annuum L. plants. Plant Cell Physiol 50:1815–1825. doi:10.1093/pcp/pcp123

    CAS  Article  PubMed  Google Scholar 

  • Oguchi R, Douwstra P, Fujita T, Chow WS, Terashima I (2011a) Intra-leaf gradients of photoinhibition induced by different color lights: implication s for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159. doi:10.1111/j.1469-8137.2011.03669.x

    Article  PubMed  Google Scholar 

  • Oguchi R, Terashima I, Kou J, Chow WS (2011b) Operation of dual mechanisms that both lead to phoinactivation of photosystem II in leaves by visible light. Physiol Plant 142:47–55. doi:10.1111/j.1399-5054.2011.04152.x

    CAS  Article  PubMed  Google Scholar 

  • Oja VM, Laisk AK (1976) Adaptation of the photosynthesis apparatus to the light profile in the leaf. Soviet Plant Physiol 23:381–386

    Google Scholar 

  • Richter T, Fukshansky L (1996a) Optics of a bifacial leaf: 1. A novel combined procedure for deriving the optical parameters. Photochem Photobiol 63:507–516

    CAS  Article  Google Scholar 

  • Richter T, Fukshansky L (1996b) Optics of a bifacial leaf: 2. Light regime as affected by leaf structure and the light source. Photochem Photobiol 63:517–527

    CAS  Article  Google Scholar 

  • Sage TL, Sage RF (2009) The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant Cell Physiol 50:756–772. doi:10.1093/pcp/pcp033

    CAS  Article  PubMed  Google Scholar 

  • Schanderl H, Kaempfert W (1933) Über die Strahlungdruchlässigkeit von Blättern und Blattgeweben. Planta 18:700–750

    CAS  Article  Google Scholar 

  • Schreiber U, Fink R, Vidaver W (1977) Fluorescence induction in whole leaves: differentiation between the two leaf sides and adaptation to different light regimes. Planta 133:121–129

    CAS  Article  PubMed  Google Scholar 

  • Schreiber U, Kühl M, Klimant I, Reising H (1996) Measurement of chlorophyll fluorescence within leaves using a modified PAM fluorometer with a fiber-optic microprobe. Photosynth Res 47:103–109

    CAS  Article  PubMed  Google Scholar 

  • Seyfried M, Fukshansky L (1983) Light gradients in plant tissue. Appl Opt 22:1402–1408. doi:10.1364/AO.22.001402

    CAS  Article  PubMed  Google Scholar 

  • Skene D (1974) Chloroplast structure in mature apple leaves grown under different levels of illumination and their response to changed illumination. Proc R Soc Lond B 186:75–78

    Article  Google Scholar 

  • Suetsugu N, Wada M (2012) Chloroplast photorelocation movement: a sophisticated strategy for chloroplasts to perform efficient photosynthesis. In: Najafpour M (ed) Advances in photosynthesis-fundamental aspects. InTech, Shanghai, pp 215–234. ISBN 978-953-307-928-8

    Google Scholar 

  • Sun J, Nishio JN (2001) Why abaxial illumination limits photosynthesis carbon fixation in spinach leaves. Plant Cell Physiol 42:1–8

    CAS  Article  PubMed  Google Scholar 

  • Sun J, Nishio JN, Vogelmann TC (1998) Green light drives CO2 fixation deep within leaves. Plant Cell Physiol 39:1020–1026

    CAS  Article  Google Scholar 

  • Syvertsen JP, Cunningham GL (1979) The effects of irradiating adaxial or abaxial leaf surface on the rate of net photosynthesis of Perecia nana and Helianths annuus. Photosynthetica 13:287–293

    Google Scholar 

  • Takahashi K, Mineuchi K, Nakamura T, Koizumi M, Kano H (1994) A system for imaging transverse distribution of scattered light and chlorophyll fluorescence in intact rice leaves. Plant Cell Environ 17:105–110

    Article  Google Scholar 

  • Tanaka T, Matsushima S (1970) Analysis of yield-determining process and its application to yield-prediction and culture improvement of lowland rice 94: relation between the light intensity on both sides and the amount of carbon assimilation in each side of a single leaf-blade. Proc Crop Soc Japan 39:325–329

    Article  Google Scholar 

  • Terashima I (1986) Dorsiventrality in photosynthetic light response curves of a leaf. J Exp Bot 37:399–405

    Article  Google Scholar 

  • Terashima I (1989) Productive structure of a leaf. In: Briggs WR (ed) Photosynthesis. Alan R. Liss, New York, pp 207–226

    Google Scholar 

  • Terashima I, Hikosaka K (1995) Comparative ecophysiology/anatomy of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128

    Article  Google Scholar 

  • Terashima I, Inoue Y (1984) Comparative photosynthetic properties of palisade tissue chloroplasts and spongy tissue chloroplasts of Camellia japonica L.: functional adjustment of the photosynthetic apparatus to light environment within a leaf. Plant Cell Physiol 25:555–563

    CAS  Google Scholar 

  • Terashima I, Inoue Y (1985a) Palisade tisshe chloroplasts and spongy tissue chloroplasts in spinach: biochemical and ultrastructural differences. Plant Cell Physiol 26:63–75

    CAS  Google Scholar 

  • Terashima I, Inoue Y (1985b) Vertical gradient in photosynthetic properties of spinach chloroplasts dependent on intra-leaf light environment. Plant Cell Physiol 26:781–785

    CAS  Google Scholar 

  • Terashima I, Saeki T (1983) Light environment within a leaf. I. Optical properties of paradermal sections of Camellia leaves with special reference to differences in the optical properties of palisade and spongy tissues. Plant Cell Physiol 24:1493–1501

    CAS  Google Scholar 

  • Terashima I, Saeki T (1985) A new model for leaf photosynthesis incorporating the gradients of light environment and of photosynthetic properties of chloroplasts within a leaf. Ann Bot 56:489–499

    CAS  Google Scholar 

  • Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol 50:684–697. doi:10.1093/pcp/pcp034

    CAS  Article  PubMed  Google Scholar 

  • Tholen D, Boom C, Noguchi K, Ueda S, Katase T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Env 31:1688–1700. doi:10.1111/j.1365-3040.2008.01875.x

    CAS  Article  Google Scholar 

  • Vogelmann TC (1993a) Plant tissue optics. Annu Rev Plant Physiol Plant Mol Biol 44:233–251

    Article  Google Scholar 

  • Vogelmann TC (1993b) Light within a plant. In: Kendrick RE, Kronenberg CHM (eds) Photomorphogensis in plants, 2nd edn. Kluwer, Dordrecht, pp 491–535

    Google Scholar 

  • Vogelmann T, Evans JR (2002) Profiles of light absorption and chlorophyll within spinach from chlorophyll fluorescence. Plant Cell Environ 25:1313–1323

    Article  Google Scholar 

  • Vogelmann TC, Gorton HL (2014) Leaf: light capture in the photosynthetic organ. In: Hohmann-Marriott MF (ed) The structural basis of biological energy generation. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 363–377. doi:10.1007/978-94-017-8742-0_19

    Chapter  Google Scholar 

  • Vogelmann TC, Bornman JF, Josserand SA (1989) Photosynthetic light gradients and spectral regime within leaves of Medicago sativa. Phil Trans R Soc Lond B 323:411–421

    Article  Google Scholar 

  • Wooley JT (1971) Reflectance and transmittance of light by leaves. Plant Physiol 47:656–662. doi:10.1104/pp.47.5.656

    Article  Google Scholar 

Download references

Acknowledgments

We would like to dedicate this review article to late Professor Jan Anderson who passed away on 28 August 2015. She revealed the relationship between structure and functions of thylakoids. We thank Dr. Tom Vogelmann, Dr. Hiroyuki Muraoka, and Dr. Hibiki Noda-Muraoka for their useful and encouraging comments on the manuscript. Our studies have been supported by several grants form the Moritani Foundation, Yamada Science Foundation, and the Ministry of Eduation, Culture, Sports, Science and Technology, Japan, for these 20 years.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Terashima Ichiro, Ooeda Hiroki & Fujita Takashi

  2. Graduate School of Life Sciences, Tohoku University, 6-3 Aoba, Sendai, 980-8578, Japan

    Oguchi Riichi

Authors
  1. Terashima Ichiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ooeda Hiroki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fujita Takashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oguchi Riichi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Terashima Ichiro.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ichiro, T., Hiroki, O., Takashi, F. et al. Light environment within a leaf. II. Progress in the past one-third century. J Plant Res 129, 353–363 (2016). https://doi.org/10.1007/s10265-016-0808-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-016-0808-1

Keywords

  • Chloroplast movement
  • Diffuse light
  • Fluorescence
  • Palisade tissue
  • Photosynthesis
  • Spongy tissue