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Leaf vs. inflorescence: differences in photosynthetic activity of grapevine

Abstract

Using measures of gas exchange and photosynthetic chain activity, we found some differences between grapevine inflorescence and leaf in terms of photosynthetic activity and photosynthesis regulations. Generally, the leaf showed the higher net photosynthesis (P N) and lower dark respiration than that of the inflorescence until the beginning of the flowering process. The lower (and negative) P N indicated prevailing respiration over photosynthesis and could result from a higher metabolic activity rather than from a lower activity of the photosynthetic apparatus. Considerable differences were observed between both organs in the functioning and regulation of PSI and PSII. Indeed, in our conditions, the quantum yield efficiency and electron transport rate of PSI and PSII were higher in the inflorescence compared to that of the leaf; nevertheless, protective regulatory mechanisms of the photosynthetic chain were clearly more efficient in the leaf. This was in accordance with the major function of this organ in grapevine, but it highlighted also that inflorescence seems to be implied in the whole carbon balance of plant. During inflorescence development, the global PSII activity decreased and PSI regulation tended to be similar to the leaf, where photosynthetic activity and regulations remained more stable. Finally, during flowering, cyclic electron flow (CEF) around PSI was activated in parallel to the decline in the thylakoid linear electron flow. Inflorescence CEF was double compared to the leaf; it might contribute to photoprotection, could promote ATP synthesis and the recovery of PSII.

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Abbreviations

BBCH:

Biologische Bundesanstalt, Bundessortenamt and Chemical Industry

CEF:

cyclic electron flow

Chl:

chlorophyll

cyt b6f :

cytochrome b6f complex

DS:

developmental stage

ETRI :

electron transport rate of PSI

ETRII :

electron transport rate of PSII

F0 :

minimal fluorescence yield of the dark-adapted state

F0':

minimal fluorescence yield of the light-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

Fm':

maximal fluorescence yield of the light-adapted state

Fd:

ferredoxin

FNR:

ferredoxin NADP+ reductase

FM:

fresh mass

Fv/Fm :

maximum quantum yield of PSII photochemistry

NPQ:

nonphotochemical quenching

LEF:

linear electron flow

PC:

plastocyanin

PEPC:

phosphoenolpyruvate carboxylase

P N :

net photosynthetic rate

PQ:

plastoquinone

R D :

dark respiration

ROS:

reactive oxygen species

RuBP:

ribulose-1,5-bisphosphate

YCEF :

quantum yield of cyclic electron flow

YI :

efficient quantum yield of PSI

YII :

efficient quantum yield of PSII

YNA :

PSI acceptor side limitation

YND :

PSI donor side limitation

YNO :

quantum yield of nonregulated energy dissipation

YNPQ :

quantum yield of regulated energy dissipation

References

  1. Abdel-Reheem S., Belal M.H., Gupta G.: Photosynthesis inhibition of soybean leaves by insecticides. - Environ. Pollut. 74: 245–250, 1991.

    CAS  Article  PubMed  Google Scholar 

  2. Allakhverdiev S.I., Nishiyama Y., Takahashi S. et al.: Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem IIin Synechocystis. - Plant Physiol. 137: 263–273, 2005.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Antlfinger A., Wendel L.: Reproductive effort and floral photosynthesis in Spiranthes cernua (Orchidaceae). - Am. J. Bot. 84: 769, 1997.

    CAS  Article  PubMed  Google Scholar 

  4. Aschan G., Pfanz H.: Non-foliar photosynthesis–a strategy of additional carbon acquisition. - Flora 198: 81–97, 2003.

    Article  Google Scholar 

  5. Avenson T.J., Cruz J.A., Kanazawa A. et al.: Regulating the proton budget of higher plant photosynthesis. - P. Natl. Acad. Sci. USA 102: 9709–9713, 2005.

    CAS  Article  Google Scholar 

  6. Bazzaz F.A., Carlson R.W., Harper J.L.: Contribution to reproductive effort by photosynthesis of flowers and fruits. - Nature 279: 554–555, 1979.

    Article  Google Scholar 

  7. Bendall D.S., Manasse R.S.: Cyclic photophosphorylation and electron transport. - BBA-Bioenergetics 1229: 23–38, 1995.

    Article  Google Scholar 

  8. Bertamini M., Muthuchelian K., Rubinigg M. et al.: Photoinhibition of photosynthesis in leaves of grapevine (Vitis vinifera L. cv. Riesling). Effect of chilling nights. - Photosynthetica 43: 551–557, 2005.

    CAS  Article  Google Scholar 

  9. Bertamini M., Nedunchezhian N.: Photoinhibition of photosynthesis in Vitis berlandieri and Vitis rupestris leaves under field conditions. - Photosynthetica 40: 597–603, 2002.

    CAS  Article  Google Scholar 

  10. Blanke M.M., Lenz F.: Fruit photosynthesis. - Plant Cell Environ. 12: 31–46, 1989.

    CAS  Article  Google Scholar 

  11. Breyton C., Nandha B., Johnson G.N. et al.: Redox modulation of cyclic electron flow around photosystem I in C3 plants. - Biochemistry 45: 13465–13475, 2006.

    CAS  Article  PubMed  Google Scholar 

  12. Carpentier R., Larue B., Leblanc R.M.: Photoacoustic spectroscopy of Anacystis nidulans: III. Detection of photosynthetic activities. - Arch. Biochem. Biophys. 228: 534–543, 1984.

    CAS  Article  PubMed  Google Scholar 

  13. Carrara S., Pardossi A., Soldatini G. et al.: Photosynthetic activity of ripening tomato fruit. - Photosynthetica 39: 75–78, 2001.

    CAS  Article  Google Scholar 

  14. Clément C., Mischler P., Burrus M. et al.: Characteristics of the photosynthetic apparatus and CO2-fixation in the flower bud of Lilium. II. Anther. - Int. J. Plant Sci. 158: 801–810, 1997..

    Article  Google Scholar 

  15. Clément C., Mischler P., Burrus M. et al.: Characteristics of the photosynthetic apparatus and CO2-fixation in the flower bud of Lilium. I. Corolla. - Int. J. Plant Sci. 158: 794–800, 1997.

    Article  Google Scholar 

  16. Dogane Y., Ando T.: An estimation of carbon evolution during flowering and capsule development in a Laeliocattleya orchid. - Sci. Hortic.-Amsterdam 42: 339–349, 1990.

    Article  Google Scholar 

  17. Dueker J., Arditti J.: Photosynthetic CO2 fixation by Green Cymbidium (Orchidaceae) flowers. - Plant Physiol. 43: 130–132, 1968.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Finazzi G., Rappaport F., Furia A. et al.: Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. - EMBO Rep. 3: 280–285, 2002.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Gambarova N.G.: Activity of photochemical reactions and accumulation of hydrogen peroxide in chloroplasts under stress conditions. - Russ. Agric. Sci. 34: 149–151, 2008.

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  21. Golbeck J.H.: Structure, function and organization of the Photosystem I reaction center complex. - BBA-Bioeneretics 895: 167–204, 1987.

    CAS  Google Scholar 

  22. Golbeck J.H., Bryant D.A.: Photosystem I. - Curr. Top. Bioenerg. 16: 83–177, 1991.

    CAS  Article  Google Scholar 

  23. Heber U., Walker D.: Concerning a dual function of coupled cyclic electron transport in leaves. - Plant Physiol. 100: 1621–1626, 1992.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Heilmeier H., Whale D.M.: Carbon dioxide assimilation in the flowerhead of Arctium. - Oecologia 73: 109–115, 1987.

    Article  Google Scholar 

  25. Huang W., Zhang S.B., Cao K.F.: Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. - Plant Cell Physiol. 51: 1922–1928, 2010.

    CAS  Article  PubMed  Google Scholar 

  26. Huang W., Zhang S.B, Cao K.F.: Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. - Plant Cell Physiol. 52: 297–305, 2011.

    CAS  Article  PubMed  Google Scholar 

  27. Jia H., Oguchi R., Hope A.B. et al.: Differential effects of severe water stress on linear and cyclic electron fluxes through Photosystem I in spinach leaf discs in CO2-enriched air. - Planta 228: 803–812, 2008.

    CAS  Article  PubMed  Google Scholar 

  28. Joët T., Cournac L., Peltier G. et al.: Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. - Plant Physiol. 128: 760–769, 2002.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Johnson G.N.: Physiology of PSI cyclic electron transport in higher plants. - BBA-Bioenergetics 1807: 384–389, 2011.

    CAS  Article  PubMed  Google Scholar 

  30. Joliot P., Joliot A.: Cyclic electron transfer in plant leaf. - P. Natl. Acad. Sci. USA 99: 10209–10214, 2002.

    CAS  Article  Google Scholar 

  31. Jurik T.W.: Differential costs of sexual and vegetative reproduction in wild strawberry populations. - Oecologia 66: 394–403, 1985.

    Article  Google Scholar 

  32. Keijzer C.J., Willemse M.T.M.: Tissue interactions in the developing locule of Gasteria verrucosa during microsporogenesis. - Plant Biol. 37: 493–508, 1988.

    Google Scholar 

  33. Kirichenko E.B., Chernyad'ev I., Voronkova T.V. et al.: Activity of the photosynthesis apparatus in orchids during flowering.–Fiziol. Rastenii 36: 710–716, 1989.

    CAS  Google Scholar 

  34. Kirichenko E., Krendeleva T., Kukarskikh G. et al.: Photochemical activities of anther and pericarp chloroplast of cereals. - Russ. J. Plant Physl+ 40: 229–233, 1993.

    Google Scholar 

  35. Klughammer C., Schreiber U.: An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. - Planta 192: 261–268, 1994.

    CAS  Article  Google Scholar 

  36. Klughammer C., Schreiber U.: Complementary PS IIquantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. - PAM Application Notes 1: 27–35, 2008.

    Google Scholar 

  37. Kotakis C., Kyzeridou A., Manetas Y.: Photosynthetic electron flow during leaf senescence: Evidence for a preferential maintenance of photosystem I activity and increased cyclic electron flow. - Photosynthetica 52: 413–420, 2014.

    CAS  Article  Google Scholar 

  38. Kramer D.M., Johnson G., Kiirats O. et al.: New fluorescence parameters for the determination of QAredox state and excitation energy fluxes. - Photosynth. Res. 79: 209–218, 2004.

    CAS  Article  PubMed  Google Scholar 

  39. Kubicki A., Funk E., Westhoff P. et al.: Differential expression of plastome-encoded ndh genes in mesophyll and bundlesheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. - Planta 199: 276–281, 1996.

    CAS  Article  Google Scholar 

  40. Laisk A., Talts E., Oja V. et al.: Fast cyclic electron transport around photosystem I in leaves under far-red light: a protonuncoupled pathway? - Photosynth. Res. 103: 79–95, 2010.

    CAS  Article  PubMed  Google Scholar 

  41. Lebon G., Brun O., Magné C. et al.: Photosynthesis of the grapevine (Vitis vinifera L.) inflorescence. - Tree Physiol. 25: 633–639, 2005.

    CAS  Article  PubMed  Google Scholar 

  42. Lebon G., Duchêne E., Brun O. et al.: Flower abscission and inflorescence carbohydrates in sensitive and non-sensitive cultivars of grapevine. - Sex. Plant Reprod. 17: 71–79, 2004.

    CAS  Article  Google Scholar 

  43. Lebon G., Duchêne E., Brun O. et al.: Phenology of flowering and starch accumulation in grape (Vitis vinifera L.) cuttings and vines. - Ann. Bot.-London 95: 943–948, 2005.

    CAS  Article  Google Scholar 

  44. Lebon G., Wojnarowiez G., Holzapfel B. et al.: Sugars and flowering in the grapevine (Vitis vinifera L.). - J. Exp. Bot. 59: 2565–2578, 2008.

    CAS  Article  PubMed  Google Scholar 

  45. Livak K.J, Schmittgen T.D.: Analysis of relative gene expression using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402–408, 2001.

    CAS  Article  PubMed  Google Scholar 

  46. Livingston A.K., Kanazawa A., Cruz J.A. et al.: Regulation of cyclic electron flow in C3 plants: differential effects of limiting photosynthesis at ribulose-1,5-bisphosphate carboxylase/ oxygenase and glyceraldehyde-3-phosphate dehydrogenase. - Plant Cell Environ. 33: 1779–1788, 2010.

    CAS  Article  PubMed  Google Scholar 

  47. Marcelis L.F.M., Hofman-Eijer L.R.B.: The contribution of fruit photosynthesis to the carbon requirement of cucumber fruits as affected by irradiance, temperature and ontogeny. - Physiol. Plantarum 93: 476–483, 1995.

    CAS  Article  Google Scholar 

  48. Meier U.: Grapevine. - In: Meier U. (ed.): Growth Stages of Mono- and Dicotyledonous Plants BBCH Monograph Federal Biological Research Centre for Agriculture andForestry. Pp. 93–95. Blackwell Wissenschafts-Verlag, Berlin 2001.

    Google Scholar 

  49. Miyake C., Miyata M., Shinzaki Y. et al.: CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves–relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence.–Plant Cell Physiol. 46: 629–637, 2005.

    CAS  Article  PubMed  Google Scholar 

  50. Munekage Y., Hashimoto M., Miyake C. et al.: Cyclic electron flow around photosystem I is essential for photosynthesis. - Nature 429: 579–582, 2004.

    CAS  Article  PubMed  Google Scholar 

  51. Munekage Y., Hojo M., Meurer J. et al.: PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. - Cell 110: 361–371, 2002.

    CAS  Article  PubMed  Google Scholar 

  52. Nandha B., Finazzi G., Joliot P. et al.: The role of PGR5 in the redox poising of photosynthetic electron transport. - BBABioenergetics 1767: 1252–1259, 2007.

    CAS  Article  Google Scholar 

  53. Palliotti A., Cartechini A.: Developmental changes in gas exchange activity in flowers, berries, and tendrils of fieldgrown Cabernet Sauvignon. - Am. J. Enol.Viticult. 52: 317–323, 2001.

    Google Scholar 

  54. Petit A.-N., Baillieul F., Vaillant-Gaveau N. et al.: Low responsiveness of grapevine flowers and berries at fruit set to UV-C irradiation. - J. Exp. Bot. 60: 1155–1162, 2009.

    CAS  Article  PubMed  Google Scholar 

  55. Reekie E.G., Bazzaz F.A.: Reproductive effort in plants. I. Carbon allocation to reproduction. - Am. Nat. 129: 876–896, 1987.

    Article  Google Scholar 

  56. Sawicki M., Aït Barka E., Clément C. et al.: Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission. - J. Exp. Bot. 66: 1707–1719, 2015.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Sawicki M., Jeanson E., Celiz V. et al.: Adaptation of grapevine flowers to cold involves different mechanisms depending on stress intensity. - PLoS ONE 7: e46976, 2012.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Sawicki M., Jacquens L., Baillieul F. et al.: Distinct regulation in inflorescence carbohydrate metabolism according to grapevine cultivars during floral development.–Physiol. Plantarum 154: 447–467, 2015.

    CAS  Article  Google Scholar 

  59. Sawicki M., Aït Barka E., Clément C. et al.: Cold-night responses in grapevine inflorescences. - Plant Sci. 239: 115–127, 2015.

    CAS  Article  PubMed  Google Scholar 

  60. Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. - In: Schulze E..D, Caldwell M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 49–70. Springer, Berlin Heidelberg 1994.

    Google Scholar 

  61. Shikanai T.: Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis.–Curr. Opin. Biotech. 26: 25–30, 2014.

    CAS  Article  PubMed  Google Scholar 

  62. Sonoike K.: Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. - Plant Cell Physiol. 36: 825–830, 1995.

    CAS  Google Scholar 

  63. Takahashi S., Milward S.E., Fan D.Y. et al.: How does cyclic electron flow alleviate photoinhibition in Arabidopsis? - Plant Physiol. 149: 1560–1567, 2009.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Vaillant-Gaveau N., Maillard P., Wojnarowiez G. et al.: Inflorescence of grapevine (Vitis vinifera L.): a high ability to distribute its own assimilates. - J. Exp. Bot. 62: 4183–4190, 2011.

    CAS  Article  PubMed  Google Scholar 

  65. Vemmos S., Goldwin G.: The photosynthetic activity of Cox's Orange Pippin apple flowers in relation to fruit setting. - Ann. Bot.-London 73: 385–391, 1994.

    Article  Google Scholar 

  66. von Caemmerer S., Farquhar G.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. - Planta 153: 376–387, 1981.

    Article  Google Scholar 

  67. Weiss D., Shomer-Ilan A., Vainstein A. et al.: Photosynthetic carbon fixation in the corollas of Petunia hybrida. - Physiol. Plantarum 78: 345–350, 1990.

    CAS  Article  Google Scholar 

  68. Weiss D., Schönfeld M., Halevy A.H.: Photosynthetic activities in the Petunia corolla. - Plant Physiol. 87: 666–670, 1988.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Werk K.S., Ehleringer J.R.: Photosynthesis by flowers in Encelia farinosa and Encelia californica (Asteraceae). - Oecologia 57: 311–315, 1983.

    Article  Google Scholar 

  70. Yonemori K., Itai A., Nakano R. et al.: Role of calyx lobes in gas exchange and development of Persimmon fruit. - J. Am. Soc. Hortic. Sci. 121: 676–679, 1996.

    Google Scholar 

  71. Zapata C., Deléens E., Chaillou S. et al.: Mobilisation and distribution of starch and total N in two grapevine cultivars differing in their susceptibility to shedding. - Funct. Plant Biol. 31: 1127–1135, 2004.

    CAS  Article  Google Scholar 

  72. Zapata C., Deléens E., Chaillou S. et al.: Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.). - J. Plant Physiol. 161: 1031–1040, 2004..

    CAS  Article  PubMed  Google Scholar 

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Correspondence to M. Sawicki.

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These authors contributed equally to this project and should be considered coauthors.

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Sawicki, M., Courteaux, B., Rabenoelina, F. et al. Leaf vs. inflorescence: differences in photosynthetic activity of grapevine. Photosynthetica 55, 58–68 (2017). https://doi.org/10.1007/s11099-016-0230-x

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Additional key words

  • cyclic electron flow
  • chlorophyll fluorescence
  • gas exchange
  • inflorescence
  • photosystem
  • Vitis vinifera