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An exceptional irradiance-induced decrease of light trapping in two Tradescantia species: an unexpected relationship with the leaf architecture and zeaxanthin-mediated photoprotection

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Biologia Plantarum

Abstract

Leaf anatomy and irradiance-dependent leaf transmittance changes serving as irradiance acclimation mechanisms in leaves were studied in two ecologically contrasting Tradescantia species, a shade plant T. fluminensis Vell. and a sun plant T. sillamontana Matuda, grown at different irradiances. A dramatic increase in leaf thickness (2 to 4-fold) under a high growth irradiance (800 μmol m−2 s−1) compared with a low growth irradiance (60 μmol m−2 s−1), achieved mainly by expansion of the epidermis, was recorded in both species. The effect took place on the background of modest changes in mesophyll thickness (1.8-fold in T. fluminensis and 1.15-fold in T. sillamontana) and chloroplast size (0.8-fold in T. fluminensis and an insignificant change in T. sillamontana). Mesophyll structure and growth irradiance response did not seem to facilitate significantly light-dependent chloroplast (avoidance) movement in these species. Nevertheless, an exceptionally large (2 to 4-fold) irradiance-induced increase in light transmittance attributable to chloroplast avoidance movement was revealed. This increase by far exceeded that in other higher plants according to available literature. The magnitude of the irradiance-dependent transmittance changes positively correlated both with the rate of photosystem II recovery and with the extent of xanthophyll deepoxidation in the leaves. This was opposite to a negative correlation observed between the same parameters in different plant species. We hypothesize that, at the evolutionary timescale, chloroplast avoidance movement might adjust independently from other photoprotective mechanisms, e.g., non-photochemical quenching, whereas, on the ontogenetic timescale, adjustment of these mechanisms inevitably follows the same trend.

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Abbreviations

DE:

coefficient of deepoxidation

HI:

high irradiance

IIT:

irradiance-induced increase in leaf light transmittance

LI:

low irradiance

NPQ:

non-photochemical quenching

PS:

photosystem

qNPQ :

coefficient of non-photochemical quenching

T:

transmittance

ΦPSII :

quantum yield of photochemical reaction in photosystem II

References

  • Adamson, H.Y., Chow, W.S., Anderson, J.M., Vesk, M., Sutherland, M.W.: Photosynthetic acclimation of Tradescantia albiflora to growth irradiance: morphological, ultrastructural and growth responses. — Physiol. Plant. 82: 353–359, 1991.

    Article  Google Scholar 

  • Anderson, J., Chow, W.S., Goodchild, D.J.: Thylakoid membrane organisation in sun/shade acclimation. — Funct. Plant Biol. 15: 11–26, 1988.

    Google Scholar 

  • Anderson, J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. — Annu. Rev. Plant Physiol. 37: 93–136, 1986.

    Article  CAS  Google Scholar 

  • Anderson, J.M., Chow, W.S., Park, Y.-I., Franklin, L.A., Robinson, S.P.A., Van Hasselt, P.R.: Response of Tradescantia albiflora to growth irradiance: change versus changeability. — Photosynth. Res. 67: 103–112, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Baker, N.R.: Chlorophyll fluorescence: a probe of photo-synthesis in vivo. — Annu. Rev. Plant Biol. 59: 89–113, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Barber, J., Andersson, B.: Too much of a good thing: light can be bad for photosynthesis. — Trends Biochem. Sci. 17: 61–66, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Berger, J.J.: Ecological restoration and nonindigenous plant species: a review. — Restoration Ecol. 1: 74–82, 1993.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chow, W.S., Adamson, H.Y., Anderson, J.M.: Photosynthetic acclimation of Tradescantia albiflora to growth irradiance: lack of adjustment of light-harvesting components and its consequences. — Physiol. Plant. 81: 175–182, 1991.

    Article  CAS  Google Scholar 

  • Davis, P.A., Caylor, S., Whippo, C.W., Hangarter, R.P.: Changes in leaf optical properties associated with light-dependent chloroplast movements. — Plant Cell Environ. 34: 2047–2059, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Demmig, B., Winter, K., Krüger, A., Czygan, F.C.: 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, 1987.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demmig-Adams, B.: Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. — Biochim. biophys. Acta. 1020: 1–24, 1990.

    Article  CAS  Google Scholar 

  • Hunt, D.R.: Sections and series in Tradescantia: American Commelinaceae: IX. — Kew Bull. 35: 437–442, 1980.

    Article  Google Scholar 

  • Jeong, W.J., Park, Y.-I., Suh, K., Raven, J.A., Yoo, O.J., Liu, J.R.: A large population of small chloroplasts in tobacco leaf cells allows more effective chloroplast movement than a few enlarged chloroplasts. — Plant Physiol. 129: 112–121, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Konert, G., Rahikainen, M., Trotta, A., Kangasjärvi, S.: Systemic signaling in light acclimation of leaves. - In: Baluška, F. (ed.): Long-Distance Systemic Signaling and Communication in Plants. Pp. 231–250. Springer-Verlag, Berlin - Heidelberg 2013.

    Chapter  Google Scholar 

  • Königer, M.: Chloroplast movement in higher plants, ferns and bryophytes: a comparative point of view. - In: Hanson, D.T., Rice, S.K. (ed.): Photosynthesis in Bryophytes and Early Land Plants. Vol. 37. Pp. 131–150. Springer, Dordrecht 2014.

    Chapter  Google Scholar 

  • Königer, M., Bollinger, N.: Chloroplast movement behavior varies widely among species and does not correlate with high light stress tolerance. — Planta 236: 411–426, 2012.

    Article  PubMed  Google Scholar 

  • Königer, M., Delamaide, J.A., Marlow, E.D., Harris, G.C.: Arabidopsis thaliana leaves with altered chloroplast numbers and chloroplast movement exhibit impaired adjustments to both low and high light. — J. exp. Bot. 59: 2285–2297, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouril, R., Wientjes, E., Bultema, J.B., Croce, R., Boekema, E.J.: High-light vs. low-light: effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. — Biochim. biophys. Acta 1827: 411–419, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence ? a practical guide. — J. exp. Bot. 51: 659–668, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Merzlyak, M., Solovchenko, A., Pogosyan, S.: Optical properties of rhodoxanthin accumulated in Aloe arborescens Mill. leaves under high-light stress with special reference to its photoprotective function. — Photochem. Photobiol. Sci. 4: 333–340, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Park, Y.I., Chow, W.S., Anderson, J.M.: Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. — Plant Physiol. 111: 867–875, 1996.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powles, S.B., Thorne, S.W.: Effect of high-light treatments in inducing photoinhibition of photosynthesis in intact leaves of low-light grown Phaseolus vulgaris and Lastreopsis microsora. — Planta 152: 471–477, 1981.

    Article  CAS  PubMed  Google Scholar 

  • Ptushenko, V.V, Ptushenko, E.A., Samoilova, O.P., Tikhonov, A.N.: Chlorophyll fluorescence in the leaves of Tradescantia species of different ecological groups: induction events at different intensities of actinic light. — Biosystems 114: 85–97, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ptushenko, V.V., Ptushenko, O.S., Tikhonov, A.N.: Chlorophyll fluorescence induction, chlorophyll content, and chromaticity characteristics of leaves as indicators of photosynthetic apparatus senescence in arboreous plants. — Biochemistry (Moscow) 79: 260–272, 2014.

    Article  CAS  Google Scholar 

  • Samoilova, O.P., Ptushenko, V.V, Kuvykin, I.V, Kiselev, S.A., Ptushenko, O.S., Tikhonov, A.N.: Effects of light environment on the induction of chlorophyll fluorescence in leaves: a comparative study of Tradescantia species of different ecotypes. — Biosystems 105: 41–48, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Schreiber, U., Schliwa, U., Bilger, W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. — Photosyn. Res. 10: 51–62, 1986.

    Article  CAS  PubMed  Google Scholar 

  • Seemann, J.R.: Light adaptation/acclimation of photosynthesis and the regulation of ribulose-1,5-bisphosphate carboxylase activity in sun and shade plants. — Plant Physiol. 91: 379–386, 1989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovchenko, A.: Photoprotection in Plants: Optical Screening-Based Mechanisms. - Springer, Dordrecht 2010.

    Book  Google Scholar 

  • Solovchenko, A.E., Chivkunova, O.B., Merzlyak, M.N., Reshetnikova, I.V.: A spectrophotometric analysis of pigments in apples. — Russ. J. Plant Physiol. 48: 693–700, 2001.

    Article  CAS  Google Scholar 

  • Solovchenko, A.E., Merzlyak, M.N.: Screening of visible and UV radiation as a photoprotective mechanism in plants. — Russ. J. Plant Physiol. 55: 719–737, 2008.

    Article  CAS  Google Scholar 

  • Suetsugu, N., Wada, M.: Chloroplast photorelocation movement: a sophisticated strategy for chloroplasts to perform efficient photosynthesis. - In: Najafpour, M.M. (ed.): Advances in Photosynthesis-Fundamental Aspects. Pp. 215–234. InTech Publishers, Rijeka 2012.

    Google Scholar 

  • Sztatelman, O., Waloszek, A., Katarzyna Banas, A., Gabrys, H.: Photoprotective function of chloroplast avoidance movement: in vivo chlorophyll fluorescence study. — J. Plant Physiol. 167: 709–716, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Tikhonov, A.N.: Induction events and short-term regulation of electron transport in chloroplasts: an overview. — Photosynth. Res. 125: 65–94, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Tikhonov, A.N.: pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. - Photosynth. Res. 116: 511–534, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Tyystjärvi, E., Aro, E.-M.: The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. — Proc. nat. Acad. Sci. USA 93: 2213–2218, 1996.

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber, E.: Invasive Plant Species of the World: a Reference Guide to Environmental Weeds. - CABI Publishing, Wallingford 2003.

    Google Scholar 

  • Zurzycki, J.: Chloroplasts arrangement as a factor in photosynthesis. — Acta Soc. Bot. Polon. 24: 27–63, 1955.

    Google Scholar 

Download references

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Correspondence to V. V. Ptushenko.

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Acknowledgments: This research was partially supported by the Russian Foundation for Basic Research (project 12-04-31162). The studies of pigment composition were funded by the Russian Scientific Fund (contract # 14-50-00029). The authors are grateful to Prof. A.N. Tikhonov for careful reading the manuscript and to Axioma Electrica LLC for consultations on and supply of the light emitting diodes equipment.

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Ptushenko, V.V., Ptushenko, O.S., Samoilova, O.P. et al. An exceptional irradiance-induced decrease of light trapping in two Tradescantia species: an unexpected relationship with the leaf architecture and zeaxanthin-mediated photoprotection. Biol Plant 60, 385–393 (2016). https://doi.org/10.1007/s10535-016-0593-7

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