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Fluorescence imaging of light acclimation of brazilian atlantic forest tree species

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Photosynthetica

Abstract

In the pursuit of knowledge on the biological behavior of Brazilian Atlantic Forest tree species, this study evaluated the susceptibility of the light-demanding species, Schinus terebinthifolia Raddi., Pseudobombax grandiflorum (Cav.) A. Robyns and Joannesia princeps Vell., and of the shade-tolerant species, Hymenaea courbaril L. var. stilbocarpa and Lecythis pisonis Camb, to photoinhibition and acclimation capacity. These species were first cultivated under two irradiance conditions, I20 (20% direct sunlight radiation) and I100 (all-sky or direct sunlight) and then transferred from I20 to I100. The effects of the sudden increase in light radiation intensity on photosynthetic activity were then evaluated through chlorophyll (Chl) fluorescence imaging, HPLC xanthophylls analysis, and cell membrane lipid peroxidation measurements. Light-demanding species were found to present a higher photochemical efficiency and higher acclimation capacity under high light irradiance than shade-tolerant species. The higher photoinhibition tolerance observed in light-demanding species was associated to their higher capacity for photochemical dissipation and dissipation of excess excitation energy via the xanthophyll cycle, leading to a lower ROS generation. The obtained results suggested that a knowledge of acclimation capacity, by means of Chl fluorescence imaging yields, is a useful indicator of species successional grouping.

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Abbreviations

A:

antheraxanthin

DEPS:

de-epoxidation state

F:

transient fluorescence

F0 :

dark fluorescence yield

Fm :

maximum fluorescence yield after dark adaptation

Fm′:

maximum fluorescence in the light-adapted state

Fv/Fm :

maximum quantum yield of PSII

HPLC:

high performance liquid chromatography

LHCs:

light-harvesting complexes

MDA:

malondialdehyde

V:

violaxanthin

Y(II):

effective quantum yield of PSII

Y(NO):

quantum yield of nonregulated nonphotochemical energy dissipation in PSII

Y(NPQ):

quantum yield of regulated nonphotochemical energy dissipation in PSII

Z:

zeaxanthin

References

  • Ali, M.B., Hahn, E., Paek, K.: Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. — Environ. Exp. Bot. 54: 109–120, 2005.

    Article  CAS  Google Scholar 

  • Alves, P.L.C.A., Magalhães, A.C.N., Barja, P.R.: The phenomenon of photoinhibition of photosynthesis and its importance in reforestation. — Bot. Rev. 68: 193–208, 2002.

    Article  Google Scholar 

  • Baker, N.R., Rosenqvist, E.: Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. — J. Exp. Bot. 55: 1607–1621, 2004.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Barbosa, L.M.: [Forest restoration of degraded areas in São Paulo State: history, current situation and projects. — In: Barbosa L.M. (ed.): Manual for Restoration of Degraded Areas of São Paulo State — Riparian Forests of Inland São Paulo State.] Pp. 4–25. Instituto de Botânica, São Paulo 2006. [In Portuguese.]

    Google Scholar 

  • Barros, N.F., Brandi, R.M.: [Influence of three forest species over soil fertility of pasture in Viçosa, Minas Gerais State.] — Brasil Florestal 6: 24–29, 1975. [In Portuguese.]

    Google Scholar 

  • Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77k among vascular plants of diverse origins. — Planta 170: 489–504, 1987.

    Article  Google Scholar 

  • Bros, E., Meyer, S., Genty, B.: Heterogeneity of leaf CO2 assimilation during photosynthetic induction. — Plant Cell Environ. 19: 1349–1358, 1996.

    Article  Google Scholar 

  • Burritt, D.J., Mackenzie, S.: Antioxidant Metabolism during Acclimation of Begonia x erythrophylla to High Light Levels. — Ann. Bot. 91: 783–794, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Calatayud, A., Roca, D., Martínez, P.F.: Spatial-temporial variations in rose leaves under water stress conditions studies by chlorophyll fluorescence imaging. — Plant Physiol. Biochem. 44: 564–573, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Carneiro, M.A.C., Siqueira, J.O., Davide, A.C., Gomes, L.J., Curi, N., do Vale, F.R.: Mycorrhizal fungi and superphosphate and the growth of tropical woody species. — Sci. Forest. 50: 21–36, 1996.

    Google Scholar 

  • Carpanezzi, A.A.: [Grounds for rehabilitation of ecosystems forest. — In: Galvão, A.P.M., Porfírio-da-Silva V. (ed.): Forest Restoration — Fundamentals and Case Studies.] Pp. 27–46. Embrapa, Colombo-PR 2005. [In Portuguese.]

    Google Scholar 

  • Carvalho, P.E.R.: [Brazilian tree species.] Vol 1 and 2. Embrapa, Colombo-PR, 2006. [In Portuguese.]

    Google Scholar 

  • Chen, X., Li, W., Lu, Q., Wen, X., Li, H., Kuang, T., Li, Z., Lu, C.: The xanthophyll cycle and antioxidative defense system are enhanced in the wheat hybrid subjected to high light stress. — J. Plant Physiol. 168: 1828–1836, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, L.: Xanthophyll cycle pool size and composition in relation to the nitrogen content of apple leaves. — J. Exp. Bot. 54: 385–393, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Delagrange, S., Messier, C., Lechowicz, M.J., Dizengremel, P.: Physiological, morphological and allocational plasticity in understory deciduous trees: importance of plant size and light availability. — Tree Physiol. 22: 775–84, 2004.

    Article  Google Scholar 

  • Demming-Adams, B.; Adams, W.W., III: Photoprotection and other responses of plants to high light stress. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 599–626, 1992.

    Article  Google Scholar 

  • Demming-Adams, B.; Adams, W.W., III: The role of xanthophylls cycle carotenoids in the protection of photosynthesis. — Trends Plant Sci 1: 21–26, 1996.

    Article  Google Scholar 

  • Demmig-Adams, B., Ebbert, V., Zarter, C.R., Adams, W.W., III.: Characteristics and species-dependent employment of flexible versus sustained thermal dissipation and photoinhibition. — In: Demming-Adams, B.; Adams W.W., III, Matoo, K. (ed.): Advances in Photosynthesis and Respiration — Photoprotection, Photoinhibition, Gene Regulation and Environment. Vol. 21. Pp. 39–48. Springer, Dordrecht 2006.

    Chapter  Google Scholar 

  • Ebbert, V., Demmig-Adams B., Adams, W.W., III., Mueh, K.E., Staehelin, L.A.: Correlation between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. — Photosynth. Res. 67: 63–78, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Ebbert, V., Adams W.W., III, Mattoo, A.K., Sokolenko A., Demmig-Adams B.: Upregulation of a PSII core protein phosphatase inhibitor and sustained D1 phosphorylation in zeaxanthin-retaining, photoinhibited needles of overwintering Douglas fir. — Plant Cell Environ. 28: 232–240, 2005.

    Article  CAS  Google Scholar 

  • Einhorn, K.S., Rosenqvist, E., Leverenz, J.W.: Photoinhibition in seedlings of Fraxinus and Fagus under natural light conditions: implications for forest regeneration? — Oecologia 140: 241–251, 2004.

    Article  PubMed  Google Scholar 

  • Gandolfi, S.: [Light regime in semidecidual forests and its possible consequences. — In: Alfredo, Jún. (ed.): Brazilian Ecosystems: Management and Conservation.] Pp. 305–311. Expressão Gráfica e Editora, Fortaleza-Ceará 2003. [In Portuguese.]

    Google Scholar 

  • Genty, B., Briantais, J., 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.

    Article  CAS  Google Scholar 

  • Govindjee, Nedbal, L.: The chlorophyll fluorescence imaging and its application in plant science and technology — 3rd Regional Photosynthetic Workshop — Photosynthetica 38: 481–482, 2000.

    Article  Google Scholar 

  • Gray, G.R., Hope, B.J., Qin, X., Taylor, B.G., Whitehead, C.L.: The characterization of photoinhibition and recovery during cold acclimation in Arabidopsis using chlorophyll fluorescence imaging. — Physiol. Plant. 119: 365–375, 2003.

    Article  CAS  Google Scholar 

  • Guidi L., Degl’Innocenti E.: Ozone effects on high light-induced photoinhibition in Phaseolus vulgaris. — Plant Sci. 174: 590–596, 2008.

    Article  CAS  Google Scholar 

  • Guo, X.R., Cao, K.F., Xu, Z.F.: Acclimation to irradiance in seedlings of three tropical rain forest Garcinia species after simulated gap formation. — Photosynthetica 44: 193–201, 2006.

    Article  Google Scholar 

  • Heddad, M., Adamska, I.: Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. — Proc. Natl. Acad. Sci. U.S.A. 97: 3741–3746, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Hendrickson, L., Furbank, R.T., Chow, W.S.: A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. — Photosynth. Res. 82: 73–81, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Hodges, D.M., Delong, J.M., Forney, C., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. — Planta 207: 604–611, 1999.

    Article  CAS  Google Scholar 

  • Hogewoning, S.W., Harbinson, J.: Insights on the development, kinetics, and variation of photoinhibition using chlorophyll fluorescence imaging of a chilled, variegated leaf. — J. Exp. Bot. 58: 453–463, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Horton, P., Wentworth, M., Ruban, A.: Control of the light harvesting function of chloroplast membranes: the LHCII-agreegation model for non-photochemical quenching. — FEBS Lett. 579: 4201–4206, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Houter, N.C., Pons, T.L.: Gap size effects on photoinhibition in understorey saplings in tropical rainforest. — Plant Ecol. 179: 43–51, 2005.

    Article  Google Scholar 

  • Johnson, G.N., Scholes, J.D., Horton, P., Young, A.J.: Relationship between carotenoid composition and growth habit in British plant species. — Plant Cell Environ. 16: 681–686, 1993.

    Article  CAS  Google Scholar 

  • Kageyama, P.Y., Gandara, F.B.: [Grounds for rehabilitation of ecosystems forest.] — In: Galvão A.P.M., Porfírio-da-Silva V. (ed.): Forest Restoration — Fundamentals and Case Studies. Pp. 47–58. Embrapa, Colombo-PR 2005. [In Portuguese.]

    Google Scholar 

  • Kitajima, M., Butler, W.L.: Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. — Biochim. Biophys. Acta 376: 105–115, 1975.

    Article  PubMed  CAS  Google Scholar 

  • Kitao, M., Yoneda, R., Tobita, H., Matsumoto, Y., Maruyama, Y., Arifin, A., Azani, M., Muhamad, M.N.: Susceptibility to photoinhibition in seedlings of six tropical fruit tree species native to Malaysia following transplantation to a degraded land. — Trees 20: 601–610, 2006.

    Article  Google Scholar 

  • Klughammer, C., Schreiber, U.: Complementary FSII quantum yield calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. — PAM Application Notes 1: 27–35, 2008.

    Google Scholar 

  • Kramer, D.M., Johnson, G., Kiirats, O., Edwards, G.E.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. — Photosynth. Res. 79: 209–218, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Leitsch, J., Schnettger, B., Critchley, C., Krause, G.H.: Two mechanisms of recovery from photoinhibition in vivo: reactivation of photosystem II related and unrelated to D1-protein turnover. — Planta 194: 15–21, 1994.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H.K., Langsdorf, G., Lenk, S., Buschmann, C.: Chlorophyll fluorescence imaging of photosynthetic activity with the flash-lamp fluorescence imaging system. — Photosynthetica 43: 355–369, 2005.

    Article  CAS  Google Scholar 

  • Lichtenthaler, H.K., Ac, A., Marek, M.V., Kalina, J., Urban, O.: Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. — Plant Physiol. Biochem. 45: 577–588, 2007a.

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler, H.K., Babani, F., Langsdorf, G.: Chlorophyll fluorescence imaging of photosynthetic activity in sun and shade leaves of trees. — Photosynth. Res. 93: 235–244, 2007b.

    Article  PubMed  CAS  Google Scholar 

  • Lorenzi, H.: [Brazilian Trees: Manual of Identification and Growing of Native Tree Plants of Brazil.] — Instituto Plantarun de Estudos da Flora Ltda, Nova Odessa — São Paulo 2000. [In Portuguese.]

  • Meng, Q., Siebke, K., Lippert, P., Baur, B., Mukherjee, U., Weis, E.: Sink-source transition in tobacco leaves visualized using chlorophyll fluorescence imaging. — New Phytol. 151: 585–595, 2001.

    Article  CAS  Google Scholar 

  • Mittermeier, R.A., Myers, N., Gil, P.R., Mittermeier, C.G.: HOTSPOTS — Earth’s biologically richest and most endangered terrestrial ecoregions. — Conservation International, the Mexican conservation organization Agrupación Sierra Madre and the cement company CEMEX, Mexico City 1999.

  • Naidu, S.L., DeLucia, E.H.: Growth, allocation and water relations of shade-grown Quercus rubra L. saplings exposed to a late-season canopy gap. — Ann. Bot. 80: 335–344, 1997.

    Article  Google Scholar 

  • Öquist, G., Anderson, J.M., McCaffery, S., Chow, W.S.: Mechanistic differences in photoinhibition of sun and shade plants. — Planta 188: 422–431, 1992a.

    Article  Google Scholar 

  • Öquist, G., Chow, W.S., Anderson J.M.: Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem II. — Planta 186: 450–460, 1992b.

    Article  Google Scholar 

  • Oxborough, K.: Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthesis performance. — J. Exp. Bot. 55: 1195–1205, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Poole, I., Weyers, J.D.B., Lawson, T., Raven, J.A.: Variations in stomatal density and index: implications for palaeoclimatic reconstructions. — Plant Cell Environ. 19: 705–712, 1996.

    Article  Google Scholar 

  • Ramalho, J.C., Pons, T.L., Groeneveld, H.W., Nunes, M.A.: Photosynthetic responses of Coffea arabica leaves to a short-term high light exposure in relation to N availability. — Physiol. Plant 101: 229–239, 1997.

    Article  CAS  Google Scholar 

  • Ribeiro, A.C.: [Recommendation for liming and fertility of soil for seedling, pits and flowerbeds. — In: Ribeiro A.C., Guimarães P.T.G., Álvares V.H. (ed.): Commissions of Soil Fertility of Minas Gerais State — Recommendations for the use of lime and fertilizers in Minas Gerais State.] — 5th Ed. Aproximação. Departamento de Solos da Universidade Federal de Viçosa, Viçosa-MG 1999. [In Portuguese.]

    Google Scholar 

  • Ribeiro, R.V., Souza, G.M., Oliveira, R.F., Machado, E.C.: Photosynthetic responses of tropical tree species from different successional groups under contrasting irradiance conditions. — Ver. Bras. Bot. 28: 149–161, 2005.

    Article  Google Scholar 

  • Rozendaal, D.M.A., Hurtado, V.H., Pooter, L.: Plasticity in leaf traits of 38 tropical tree species in response to light: relationships with demand and adult stature. — Funct. Ecol. 20: 207–216, 2006.

    Article  Google Scholar 

  • Ruban, A. V.: Plants in light. — Communicative & Integrative Biology 2: 1, 2009.

    Article  Google Scholar 

  • Souza, G.M., Ribeiro, R.V., Prado, C.H.B.A., Damineli, D.S.C., Sato, A.M., Oliveira, M.S.: Using network connectance and autonomy analyses to uncover patterns of photosynthetic responses in tropical woody species. — Ecol. Complexity 6: 15–26, 2009.

    Article  Google Scholar 

  • Takahashi, S., Badger, M. R.: Photoprotection in plants: a new light on photosystem II damage. — Trends Plant Sci. 16: 1–1, 2011.

    Article  Google Scholar 

  • Takahashi, S., Murata, N.: How do environmental stresses accelerate photoinhibition? — Trends Plant Sci. 13: 178–182, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Terashima, I.: Anatomy of non-uniform leaf photosynthesis. — Photosynth. Res. 31: 195–212, 1992.

    Article  CAS  Google Scholar 

  • Thiele, A., Schirwitz, K., Winter, K., Krause, G.H.: Increase xanthophylls cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light. — J. Plant Sci. 155: 237–250, 1996.

    Google Scholar 

  • Tobita, H., Utsugi, H., Kitao, M., Kayama, M., Uemura, A., Kitaoka, S., Maruyama, Y.: Variation in photoinhibition among Sasa senanensis, Quercus mongolica, and Acer mono in understory of a deciduous broad-leaved Forest exposed to canopy gaps caused by typhoons. — Trees 24: 307–319, 2010.

    Article  Google Scholar 

  • Valladares, F., Niinemets, U.: Shade tolerance, a key plant feature of complex nature and consequences. — Annu. Rev. Ecol. Evol. System. 39: 237–257, 2008.

    Article  Google Scholar 

  • Walters, R.G.: Towards an understanding of photosynthetic acclimation. — J. Exp. Bot. 56: 435–447, 2005.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to L. Dos Anjos.

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Acknowledgements: The authors would like to thank Dr. Fábio Murillo DaMatta for providing the xanthophyll pigments and Dr. Raimundo Santos Barros for his permission to use their HLPC device. Our sincere thanks also go to the following institutions: CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and FAPEMIG (Fundação de Amparo à Pesquisa de Minas Gerais) for their invaluable financial support, and finally to Vale do Rio Doce Company for providing the seedlings used.

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Dos Anjos, L., Oliva, M.A. & Kuki, K.N. Fluorescence imaging of light acclimation of brazilian atlantic forest tree species. Photosynthetica 50, 95–108 (2012). https://doi.org/10.1007/s11099-012-0018-6

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  • DOI: https://doi.org/10.1007/s11099-012-0018-6

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