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Fluorescence F 0 of photosystems II and I in developing C3 and C4 leaves, and implications on regulation of excitation balance

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Abstract

This work addresses the question of occurrence and function of photosystem II (PSII) in bundle sheath (BS) cells of leaves possessing NADP-malic enzyme-type C4 photosynthesis (Zea mays). Although no requirement for PSII activity in the BS has been established, several component proteins of PSII have been detected in BS cells of developing maize leaves exhibiting O2-insensitive photosynthesis. We used the basal fluorescence emissions of PSI (F 0I) and PSII (F 0II) as quantitative indicators of the respective relative photosystem densities. Chl fluorescence induction was measured simultaneously at 680 and 750 nm. In mature leaves, the F m(680)/F 0(680) ratio was 10.5 but less in immature leaves. We propose that the lower ratio was caused by the presence of a distinct non-variable component, F c, emitting at 680 and 750 nm. After F c was subtracted, the fluorescence of PSI (F 0I) was detected as a non-variable component at 750 nm and was undetectably low at 680 nm. Contents of Chls a and b were measured in addition to Chl fluorescence. The Chl b/(a + b) was relatively stable in developing sunflower leaves (0.25–0.26), but in maize it increased from 0.09 to 0.21 with leaf tissue age. In sunflower, the F 0I/(F 0I + F 0II) was 0.39 ± 0.01 independent of leaf age, but in maize, this parameter was 0.65 in young tissue of very low Chl content (20–50 mg m−2) falling to a stable level of 0.53 ± 0.01 at Chl contents >100 mg m−2. The values of F 0I/(F 0I + F 0II) showed that in sunflower, excitation was partitioned between PSII and PSI in a ratio of 2:1, but the same ratio was 1:1 in the C4 plant. The latter is consistent with a PSII:PSI ratio of 2:1 in maize mesophyll cells and PSI only in BS cells (2:1:1 distribution). We suggest, moreover, that redox mediation of Chl synthesis, rather than protein accumulation, regulates photosystem assembly to ensure optimum excitation balance between functional PSII and PSI. Indeed, the apparent necessity for two Chls (a and b) may reside in their targeted functions in influencing accumulation of PSI and PSII, respectively, as opposed to their spectral differences.

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Abbreviations

ASP:

Aspartate

BS:

Bundle sheath

Chl:

Chlorophyll

F(680), F(750):

wavelength windows of fluorescence measurements

F 0, F m, F v :

minimal, maximal and variable fluorescence yields as measured

F I, F II :

additional subscripts to indicate PSI and PSII fluorescence yields separately

F c :

Invariant fluorescence yield associated with immature tissue

LED:

Light-emitting diode

M:

Mesophyll

MAL:

Malate

ME:

Malic enzyme

NDH:

NAD(P)H dehydrogenase

OAA:

Oxaloacetate

PAGE:

Polyacrylamide gel electrophoresis

PEP:

Phosphoenol-pyruvate

PSI, PSII:

Photosystems I and II

SE:

Standard error of the mean

References

  • Andersen KS, Bain JM, Bishop DG, Smillie RM (1972) Photosystem II activity in agranal bundle sheath chloroplasts from Zea mays. Plant Physiol 49:461–466

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180

    Article  PubMed  CAS  Google Scholar 

  • Ballotari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behaviour of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958

    Article  Google Scholar 

  • Bassi R, Marquardt J, Lavergne J (1995) Biochemical and functional properties of photosystem II in agranal membranes from maize mesophyll and bundle sheath chloroplasts. Eur J Biochem 233:709–719

    Article  PubMed  CAS  Google Scholar 

  • Bazzaz MB, Govindjee (1973) Photochemical properties of mesophyll and bundle sheath chloroplasts of maize. Plant Physiol 52:257–262

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Carbonera D, Agostini G, Morosinotto T, Bassi R (2005) Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. Biochemistry 44:8337–8346

    Article  PubMed  CAS  Google Scholar 

  • Chapman KSR, Hatch MD (1981) Aspartate decarboxylation in bundle sheath cells of Zea mays and its possible contribution to C4 photosynthesis. Aust J Plant Physiol 8:237–248

    Article  CAS  Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116:153–166

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Croce R, Zucchelli G, Garlaschi FM, Bassi R, Jennings RC (1996) Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35:8572–8579

    Article  PubMed  CAS  Google Scholar 

  • de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23:2659–2679

    Article  PubMed  PubMed Central  Google Scholar 

  • Edwards G, Walker DA (1983) C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. Blackwell, Oxford, London

    Google Scholar 

  • Franck F, Juneau P, Popovic R (2002) Resolution of the photosystem I and photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246

    Article  PubMed  CAS  Google Scholar 

  • Friso G, Majeran W, Huang M, Sun Q, van Wijk KJ (2010) Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant Physiol 152:1219–1250

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Genty B, Wonders J, Baker NR (1990) Non-photochemical quenching of F 0 in leaves is emission wavelength dependent: consequences for quenching analysis and its interpretation. Photosynth Res 26:133–139

    Article  PubMed  CAS  Google Scholar 

  • Gilmore AM, Itoh S, Govindjee G (2000) Global spectral-kinetic analysis of room temperature chlorophyll a fluorescence from light-harvesting antenna mutants of barley. Phil Trans R Soc Lond 355:1371–1384

    Article  CAS  Google Scholar 

  • Hatch MD (1971) The C4-pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C4-dicarboxylic acid. Biochem J 125:425–432

    PubMed  CAS  PubMed Central  Google Scholar 

  • Holzwarth AR, Müller MG, Niklas J, Lubitz W (2006) Ultrafast transient absorption studies on photosystem I reaction centers from Chlamydomonas reinhardtii. 2 Mutations near the P700 reaction center chlorophylls provide new insight into the nature of the primary electron donor. Biophys J 90:552–565

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jennings RC, Elli G, Garlaschi FM, Santabarbara S, Zucchelli G (2000) Selective quenching of the fluorescence of core chlorophyll–protein complexes by photochemistry indicates that photosystem II is partly diffusion limited. Photosynth Res 66:225–233

    Article  PubMed  CAS  Google Scholar 

  • Kanai R, Edwards GE (1973) Separation of mesophyll protoplasts and bundle sheath cells from maize leaves for photosynthetic studies. Plant Physiol 51:1133–1137

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim E-H, Li X-P, Razeghifard R, Anderson JM, Niyogi KK, Pogson BJ, Chow WS (2009) The multiple roles of light-harvesting chlorophyll a/b–protein complexes define structure and optimize function of Arabidopsis chloroplasts: a study using two chlorophyll b-less mutants. Biochim Biophys Acta 1787:973–984

    Article  PubMed  CAS  Google Scholar 

  • Ku SB, Gutierrez M, Kanai R, Edwards GE (1974) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. II. Chlorophyll and Hill reaction studies. Z Pflanzenphysiol 72:320–337

    Article  CAS  Google Scholar 

  • Laisk A, Edwards GE (2000) A mathematical model of C4 photosynthesis: the mechanism of concentrating CO2 in NADP-malic enzyme type species. Photosynth Res 66:199–224

    Article  PubMed  CAS  Google Scholar 

  • Laisk A and Edwards G (2009) Leaf C4 photosynthesis in silico: the CO2 concentrating mechanism. In: eds Laisk S, Nedbal L and Govindjee (eds) Photosynthesis in silico: understanding Complexity from Molecules to Ecosystems pp. 323–348. Springer Science + Business Media B.V., The Netherlands

  • Laisk A, Oja V (2013) Thermal phase and excitonic connectivity in fluorescence induction. Photosynth Res 117:431–448

    Article  PubMed  CAS  Google Scholar 

  • Laisk A, Oja V, Dall’Osto L (2014) Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in State 1. Biochim Biophys Acta 1837:315–325

    Article  PubMed  CAS  Google Scholar 

  • Lazár D (2009) Modelling of light-induced chlorophyll a fluorescence rise (O-J-I-P transient) and changes in 820 nm-transmittance signal of photosynthesis. Photosynthetica 47:483–498

    Article  Google Scholar 

  • Lazár D (2013) Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise. J Theor Biol 335:249–264

    Article  PubMed  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. In: Wrolstad RE, Acree TE, Decker EA, Penner MH, Reid DS, Schwartz SJ, Shoemaker CF, Smith D, Sporns P (eds) Handbook of food analytical chemistry. Wiley-Interscience, Hoboken, pp 171–178

    Google Scholar 

  • Majeran W, van Wijk K (2009) Cell-type-specific differentiation of chloroplasts in C4 plants. Trends Plant Sci 14:100–109

    Article  PubMed  CAS  Google Scholar 

  • Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7:1609–1638

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marder JB, Raskin VI (1993) The assembly of chlorophyll into pigment–protein complexes. Photosynthetica 28:243–248

  • Mckinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322

    Google Scholar 

  • Meurer J, Meierhoff K, Westhoff P (1996) Isolation of high-chlorophyll-fluorescence mutants in the analysis of chloroplast thylakoid membrane assembly and function. Planta 198:385–396

    Article  PubMed  CAS  Google Scholar 

  • Nelson T (2011) The grass leaf developmental gradient as a platform for a systems understanding of the anatomical specialization of C4 leaves. J Exp Bot 62:3039–3048

    Article  PubMed  CAS  Google Scholar 

  • Nelson T, Langdale JA (1989) Patterns of leaf development in C4 plants. Plant Cell 1:3–13

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Oja V, Eichelmann H, Anijalg A, Rämma H, Laisk A (2010) Equilibrium or disequilibrium? A dual-wavelength investigation of photosystem I donors. Photosynth Res 103:153–166

    Article  PubMed  CAS  Google Scholar 

  • Oswald A, Streubel M, Ljungberg U, Hermans J, Eskins K, Westhoff P (1990) Differential biogenesis of photosystem-II in mesophyll and bundle-sheath cells of ‘malic’ enzyme NADP+-type C4 plants. A comparative protein and RNA analysis. Eur J Biochem 190:185–194

    Article  PubMed  CAS  Google Scholar 

  • Palombi L, Cecchi G, Lognoli D, Raimondi V, Toci G, Agati G (2011) A retrieval algorithm to evaluate the photosystem I and photosystem II spectral contributions to leaf chlorophyll fluorescence at physiological temperatures. Photosynth Res 108:225–239

    Article  PubMed  CAS  Google Scholar 

  • Peter GF, Takeuchi T, Thornber JP (1991) Solubilization and two-dimensional electrophoretic procedures for studying the organization and composition of photosynthetic membrane polypeptides. Methods 3:115–124

    Article  CAS  Google Scholar 

  • Peterson R, Oja V, Laisk A (2001) Chlorophyll fluorescence at 680 and 730 nm and its relationship to photosynthesis. Photosynth Res 70:185–196

    Article  PubMed  CAS  Google Scholar 

  • Pfündel E (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195

    Article  Google Scholar 

  • Pfündel E, Meister A (1996) Flow cytometry of mesophyll and bundle sheath chloroplast thylakoids of maize (Zea mays L.). Cytometry 23:97–105

    Article  PubMed  Google Scholar 

  • Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, Fahnenstich H, Pieruschka R, Rascher U, Sonnewald U, Weber APM (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23:1–13

    Article  Google Scholar 

  • Porra R (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156

    Article  PubMed  CAS  Google Scholar 

  • Rätsep M, Linnanto J, Freiberg A (2009) Mirror symmetry and vibrational structure in optical spectra of chlorophyll a. J Chem Phys 130:194501

    Article  PubMed  Google Scholar 

  • Schansker G, To´th SC, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the Q A model. Photosynth Res 120:43–58

  • Schultes NP, Sawers RJH, Brutnell TP, Krueger RW (2000) Maize high chlorophyll fluorescence 60 mutation is caused by an Ac disruption of the gene encoding the chloroplast ribosomal small subunit protein 17. Plant J 21:317–327

    Article  PubMed  CAS  Google Scholar 

  • Stirbet A and Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61

  • Sušila P, Lazár D, Ilik P, Tomek P, Nauš P (2004) The gradient of exciting radiation within a sample affects the relative height of steps in the fast chlorophyll a fluorescence rise. Photosynthetica 42:161–172

    Article  Google Scholar 

  • Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807:968–976

    Article  PubMed  CAS  Google Scholar 

  • Thornber JP, Highkin HR (1974) Composition of the photosynthetic apparatus of normal barley leaves and a mutant lacking chlorophyll b. Eur J Biochem 41:109–116

    Article  PubMed  CAS  Google Scholar 

  • Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203

    Article  PubMed  Google Scholar 

  • Vernon LP (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Anal Chem 32:188–194

    Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Wientjes E, Croce R (2011) The light-harvesting complexes of higher-plant photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J 433:477–485

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

A.L., V.O., H.E., and I.B. were supported by Targeted Financing Theme SF0180045s08 from Estonian Ministry of Education and Science and Grants 8283 and 8344 from Estonian Science Foundation. We wish to thank Gerald Edwards and Joseph Berry for helpful conversations.

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Authors and Affiliations

  1. Department of Biochemistry and Genetics, The Connecticut Agricultural Experiment Station, 123 Huntington St., New Haven, CT, 06511, USA

    Richard B. Peterson

  2. Institute of Cell and Molecular Biology, Tartu University, 23 Riia St., 51010, Tartu, Estonia

    Vello Oja, Hillar Eichelmann & Agu Laisk

  3. Institute of Physics, Tartu University, 142 Riia St., 51014, Tartu, Estonia

    Irina Bichele

  4. Department of Biotechnology, University of Verona, Strada Le Grazie, 15, 37135, Verona, Italy

    Luca Dall’Osto

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  1. Richard B. Peterson
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Correspondence to Richard B. Peterson.

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Peterson, R.B., Oja, V., Eichelmann, H. et al. Fluorescence F 0 of photosystems II and I in developing C3 and C4 leaves, and implications on regulation of excitation balance. Photosynth Res 122, 41–56 (2014). https://doi.org/10.1007/s11120-014-0009-5

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