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Structural and functional properties of the coleoptile chloroplast: Photosynthesis and photosensory transduction

Photosynthesis Research volume 44, pages 207–219 (1995)Cite this article

Abstract

Recent studies have shown that guard cell and coleoptile chloroplasts appear to be involved in blue light photoreception during blue light-dependent stomatal opening and phototropic bending. The guard cell chloroplast has been studied in detail but the coleoptile chloroplast is poorly understood. The present study was aimed at the characterization of the corn coleoptile chloroplast, and its comparison with mesophyll and guard cell chloroplasts. Coleoptile chloroplasts operated the xanthophyll cycle, and their zeaxanthin content tracked incident rates of solar radiation throughout the day. Zeaxanthin formation was very sensitive to low incident fluence rates, and saturated at around 800–1000 μmol m−2 s−1. Zeaxanthin formation in corn mesophyll chloroplasts was insensitive to low fluence rates and saturated at around 1800 μmol m−2 s−1. Quenching rates of chlorophyll a fluorescence transients from coleoptile chloroplasts induced by saturating fluence rates of actinic red light increased as a function of zeaxanthin content. This implies that zeaxanthin plays a photoprotective role in the coleoptile chloroplast. Addition of low fluence rates of blue light to saturating red light also increased quenching rates in a zeaxanthin-dependent fashion. This blue light response of the coleoptile chloroplast is analogous to that of the guard cell chloroplast, and implicates these organelles in the sensory transduction of blue light. On a chlorophyll basis, coleoptile chloroplasts had high rates of photosynthetic oxygen evolution and low rates of photosynthetic carbon fixation, as compared with mesophyll chloroplasts. In contrast with the uniform chloroplast distribution in the leaf, coleoptile chloroplasts were predominately found in the outer cell layers of the coleoptile cortex, and had large starch grains and a moderate amount of stacked grana and stroma lamellae. Several key properties of the coleoptile chloroplast were different from those of mesophyll chloroplasts and resembled those of guard cell chloroplasts. We propose that the common properties of guard cell and coleoptile chloroplasts define a functional pattern characteristic of chloroplasts specialized in photosensory transduction.

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Abbreviations

Ant or A:

antheraxanthin

dv/dt:

fluorescence quenching rate

Fm:

maximum yield of fluorescence with all PS II reaction centers closed

Fo:

yield of instantaneous fluorescence with all PS II reaction centers open

Vio or V:

violaxanthin

Zea or Z:

zeaxanthin

References

  • Adams WW III and Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186: 390–398

    Google Scholar 

  • Atkins CA and Graham D (1971) Light-induced pH changes of cells of Chlamydomonas reinhardtii: Dependence on CO2 uptake. Biochim Biophys Acta 226: 481–485

    Google Scholar 

  • Bensadoun A and Weinstein D (1976) Assay of proteins in presence of interfering materials. Anal Biochem 70: 241–250

    Google Scholar 

  • Bown AW and Nicholls F (1985) An investigation into the role of photosynthesis in regulating ATP levels and rates of H+ efflux in isolated mesophyll cells. Plant Physiol 79: 825–828

    Google Scholar 

  • Coetzee J (1985) Fixation of plant cells for electron microscopy. In: Robards AW (ed) Botanical Microscopy, pp 17–38 Oxford University Press New York

    Google Scholar 

  • D'Amelio ED and Zeiger E (1988) Diversity in guard cell plastids of Orchidaceae: a structural and functional study. Can J Bot 66: 257–271

    Google Scholar 

  • Demmig B, Winter K, Krüger A and Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84: 218–224

    Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants. A role of the xanthophyll zeaxanthin. Biochim Biophys Acta 1020: 1–24

    Google Scholar 

  • Demmig-Adams B and Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626

    Google Scholar 

  • Firn RD (1986) Phototropism. In: Kendrick RE and Kronenberg GHM (eds) Photomorphogenesis in Plants, pp 367–389. Martinus Nijhoff, Dordrecht

    Google Scholar 

  • Fischer RA (1968) Stomatal opening: Role of potassium uptake by guard cells. Science 160: 784–785

    Google Scholar 

  • Gilmore AM and Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped lightly carbon loaded C-18 high performance liquid chromatographic column. J Chromatogr 543: 137–145

    Google Scholar 

  • Gilmore AM and Yamamoto HY (1992) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc Natl Acad Sci USA 89: 1899–1903

    Google Scholar 

  • Gotow K, Taylor S and Zeiger E (1988) Photosynthetic carbon fixation in guard cell protoplasts of Vicia faba L. Plant Physiol 86: 700–705

    Google Scholar 

  • Hager A (1980) The reversible, light-induced conversions of xanthophylls in the chloroplasts. In: Zygan FC (ed) Pigments in Plants, pp 57–79. Gustav Fischer, Stuttgart

    Google Scholar 

  • Horton P, Ruban AV and Walters RG (1994) Regulation of light harvesting in green plants. Plant Physiol 106: 415–420

    Google Scholar 

  • Horwitz BA (1994) Properties and transduction chains of the UV and blue light photoreceptors. In: Kendrick RE and Kronenberg GHM (eds) Photomorphogenesis in Plants, pp 327–348. Martinus Nijhoff Dordrecht

    Google Scholar 

  • Iino M, Ogawa T and Zeiger E (1985) Kinetic properties of the blue light response of stomata. Proc Natl Acad Sci USA 82: 8019–8023

    Google Scholar 

  • Karlsson PE (1986) Blue light regulation of stomata in wheat seedlings. I. Influence of red background illumination and initial conductance level. Physiol Plant 66: 202–206

    Google Scholar 

  • Kiss JZ and Sack FD (1990) Severely reduced gravitropism in dark-grown hypocotyls of a starch-deficient mutant of Nicotiana sylvestris. Plant Physiol 94: 1867–1873

    Google Scholar 

  • Krause GH and Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42: 313–349

    Google Scholar 

  • Lloyd FE (1908) The behavior of stomata. Carnegie Inst Wash Publ 82: 1–142

    Google Scholar 

  • Masamoto K, Kinoshita T and Shimazaki K (1993) Light-induced de-epoxidation of violaxanthin in guard cell protoplasts of Vicia faba. Plant Cell Physiol 34: 935–938

    Google Scholar 

  • Mawson BT (1993) Modulation of photosynthesis and respiration in guard and mesophyll cell protoplasts by oxygen concentration. Plant Cell Environ 16: 207–214

    Google Scholar 

  • Miller AG and Coman B (1980) Evidence for HCO3 − transport by the blue-green alga (cyanobacterium) Coccochloris peniocystis. Plant Physiol 65: 397–402

    Google Scholar 

  • Morse MJ and Satter RL (1979) Relationships between motor cell ultrastructure and leaf movements in Samanea saman. Physiol Plant 46: 338–346

    Google Scholar 

  • Neumann J and Levine RP (1971) Reversible pH changes in cells of Chlamydomonas reinhardtii resulting from CO2 fixation in the light and its evolution in the dark. Plant Physiol 47: 700–704

    Google Scholar 

  • Quiñones MA and Zeiger E (1994) A putative role of the xanthophyll, zeaxanthin, in blue light photoreception of corn coleoptiles. Science 264: 558–561

    Google Scholar 

  • Sanchez S (1977) The fine structure of guard cells of Helianthus annuus. Am J Bot 64: 814–824

    Google Scholar 

  • Serrano E, Zeiger E and Hagiwara S (1988) Red light stimulates an electrogenic proton pump in Vicia guard cell protoplasts. Proc Natl Acad Sci USA 85: 436–440

    Google Scholar 

  • Shimazaki K and Zeiger E (1987) Red light-dependent CO2 uptake and oxygen evolution in guard cell protoplasts of Vicia faba L.: Evidence for photosynthetic CO2 fixation. Plant Physiol 84: 7–9

    Google Scholar 

  • Shimazaki K, Gotow K and Kondo N (1982) Photosynthetic properties of guard cell protoplasts from Vicia faba L. Plant Cell Physiol 23: 871–879

    Google Scholar 

  • Shimazaki K, Iino M and Zeiger E (1986) Blue light-dependent proton extrusion by guard cell protoplasts of Vicia faba. Nature 319: 324–326

    Google Scholar 

  • Siefermann-Harms D (1977) The xanthophyll cycle in plants. In: Tevini M and Lichenthaler HK (eds) Lipids and Lipid Polymers in Higher Plants, pp 218–230. Springer-Verlag, Berlin

    Google Scholar 

  • Singh AP and Srivastava LM (1973) The fine structure of pea stomata. Protoplasma 76: 61–82

    Google Scholar 

  • Sorokin HP and Thimann KV (1960) Plastids of Avena coleoptile. Nature 187: 1038–1039

    Google Scholar 

  • Srivastava A and Zeiger E (1992) Fast fluorescence quenching from isolated guard cell chloroplasts of Vicia faba is induced by blue light and not by red light. Plant Physiol 100: 1562–1566

    Google Scholar 

  • Srivastava A and Zeiger E (1995a) The inhibitor of zeaxanthin formation, dithiothreitol, inhibits blue light-stimulated stomatal opening in Vicia faba. Planta (in press)

  • Srivastava A and Zeiger E (1995b) Guard cell zeaxanthin tracks photosynthetic active radiation and stomatal apertures in Vicia faba leaves. Plant, Cell and Envrionment (in press).

  • Talbott LD and Zeiger E (1993) Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light. Plant Physiol 102: 1163–1169

    Google Scholar 

  • Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure App Chem 51: 639–648

    Google Scholar 

  • Young AJ (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant 83: 702–708

    Google Scholar 

  • Willmer CM (1983) Stomata. pp 6–27. Longman Group Limited, New York

    Google Scholar 

  • Zeiger E (1990) Light perception in guard cells. Plant Cell Environ 13: 739–744

    Google Scholar 

  • Zeiger E, Gotow K, Mawson B and Taylor S (1987) The guard cell chloroplast: properties and function. In: Biggins J (ed) Progress in Photosynthesis Research IV. 5, pp 273–280. Martinus Nijhoff, Dordrecht

    Google Scholar 

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  1. Department of Biology, University of California, 90024, Los Angeles, CA, USA

    Jianxin Zhu, Roni Zeiger & Eduardo Zeiger

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  1. Jianxin Zhu
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  2. Roni Zeiger
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Zhu, J., Zeiger, R. & Zeiger, E. Structural and functional properties of the coleoptile chloroplast: Photosynthesis and photosensory transduction. Photosynth Res 44, 207–219 (1995). https://doi.org/10.1007/BF00018310

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  • DOI: https://doi.org/10.1007/BF00018310

Key words

  • blue light response
  • coleoptile chloroplast
  • photosynthetic properties
  • sensory transduction
  • xanthophyll cycle
  • zeaxanthin