Abstract
Exposure of plants to high-heavy metals concentration inhibits multiple metabolic processes in plants and leads to an oxidative stress commonly referred as heavy metal ion toxicity. Chlorophyll a fluorescence has enhanced understanding of heavy metal ion action on the photosynthetic system. A rapid and non-invasive technique involving imaging of chlorophyll fluorescence is a useful tool for early detection of plant responses to heavy metal ion toxicity. In this work chlorophyll fluorescence emission and photochemical parameters in plants of Populus x euramericana clone I-214 were investigated by the portable Imaging PAM fluorometer at different days after soil treatment with zinc. Custom software for analysis of the photochemical parameters images has been developed in order to gain a better assessing of the plant performance in response of metal stress. The imaging analysis allowed visualizing heterogeneity in plant response to high zinc concentrations. The heterogeneity of images suggests spatial differences in photochemical activity and changes in the antenna down-regulation.
References
Ait Ali N, Dewez D, Didur O (2006) Inhibition of photosystem II photochemistry by Cr is caused by the alteration of both D1 protein and oxygen evolving complex. Photosynth Res 89:81–87
Ait Ali N, Juneau P, Didur PO, Perreault F, Popovic R (2008) Effect of dichromate on photosystem II activity in xanthophylls-deficient mutants of Chlamydomonas reinhardtii. Photosynth Res 95:45–53
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Baker NR, Rosenqvist E (2004) Application of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621
Barbagallo RP, Oxborough K, Pallet KE, Baker NR (2003) Rapid, non-invasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132:485–493
Boucher N, Carpentier R (1999) Hg2+, Cu2+, and Pb2+-induced changes in Photosystem II photochemical yield and energy storage in isolated thylakoid membranes: a study using simultaneous fluorescence and photoacoustic measurements. Photosynth Res 59:167–174
Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystems I and II. Biochim Biophys Acta 635:542–551
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702
Castiglione S, Todeschini V, Franchin C, Torrigiani P, Gastaldi D, Cicatelli A, Rinaudo C, Berta G, Biondi S, Lingua G (2009) Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine leaves in poplar: a large-scale field trial on heavily polluted soil. Environ Pollut 157:2108–2117
Chaerle L, Van Der Straeten D (2000) Imaging techniques and the early detection of plant stress. Trends Plant Sci 5:495–501
Chaerle L, Hulsen K, Hermans C, Strasser RJ, Valcke R, Höfte M, Van Der Straeten D (2003) Robotized time-lapse imaging to assess in-planta uptake of phenylurea herbicides and their microbial degradation. Physiol Plant 118:613–619
Chaerle L, Leinonen I, Jones H, Van Der Straeten D (2006) Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging. J Exp Bot 58:773–784
Ciscato M, Valcke R (1998) Chlorophyll fluorescence imaging of heavy metal treated plants. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 2661–2663
Ciscato M, Vansgronsveld J, Valcke R (1999) Effects of heavy metals on the fast chlorophyll fluorescence induction kinetics of photosystem II: a comparative study. Bioscience 54:735–739
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486
Crimi M, Dorra D, Bösinger CS, Giuffra E, Holzwarth AR, Bassi R (2001) Time-resolved fluorescence analysis of the recombinant photosystem II antenna complex CP29. Effects of zeaxanthin, pH and phosphorylation. Eur J Biochem 268:260–267
D’Ambrosio N, Guadagno CR, Virzo De Santo A (2008) Is qE always the major component of non-photochemical quenching?. In: Allen JF, Gantt E, Golbeck JH, Osmond B (Eds.) Photosynthesis Energy from the Sun: 14th International Congress on Photosynthesis, Springer, Dordrecht, pp 1007–1010
Dan TV, KrishnaRaj S, Saxena PK (2000) Metal tolerance of scented geranium (Pelargonium sp. “Frensham”): effects of cadmium and nickel on chlorophyll fluorescence kinetics. Int J Phytorem 2:91–104
Di Baccio D, Tognetti R, Sebastiani L, Vitagliano C (2003) Response of Populus deltoids x Populus nigra (Populus x euramericana) clone I-214 to high zinc concentrations. New Phytol 159:443–452
Fischerová Z, Tlustos P, Szakova J, Sichorova K (2006) A comparison of phytoremediation capability of selected plant species for given trace elements. Environ Pollut 144:93–100
Govindjee, Nedbal L (2000) The chlorophyll fluorescence imaging and its application in plant science and technology. Seeing is believing. Photosynthetica 38:481–482
Iannelli M, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Biochem 40:977–982
Joshi MK, Mohanty P (2004) Chlorophyll a fluorescence as a probe of heavy metal ion toxicity in plants. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, the Netherlands, pp 637–661
Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493
Koprivova A, Kopriva S, Jager D, Will B, Jouanin L, Rennenberg H (2002) Evaluation of transgenic poplars over-expressing enzymes of glutathione synthesis for phytoremediation of cadmium. Plant Biol 4:664–670
Maxell K, Johnson G (2000) Chlorophyll fluorescence—a pratical guide. J Exp Bot 51:659–668
Mohanty N, Vass I, Demeter S (1990) Copper toxicity affects photosystem II electron transport at the secondary quinone acceptor, QB. Plant Physiol 90:175–179
Monnet F, Vaillant N, Vernay P, Coudret A, Sallanon H, Hitmi A (2001) Relationship between PSII activity, CO2 fixation, and Zn, Mn and Mg contents of Lolium perenne under zinc stress. J Plant Physiol 158:1137–1144
Morosinotto T, Caffaria S, Dall’Ostoa L, Bassia R (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol Plant 119:347–354
Muller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot. doi:10.1093/jxb/ert208
Ouzounidou G, Moustakas M, Strasser R (1997) Sites of action of copper in the photosynthetic apparatus of maize leaves: kinetic analysis of chlorophyll fluorescence oxygen evolution, absorption changes and thermal dissipation as monitored by photoacoustic signals. Aust J Plant Physiol 24:81–90
Page V, Weisskopf L, Feller U (2006) Heavy metals in white lupin: uptake, root—to-shoot transfer and redistribution within the plant. New Phytol 171:329–342
Papovic R, Dewez D, Juneau P (2003) Applications of Chlorophyll Fluorescence in Ecotoxicology: heavy metals, herbicides, and air pollutants. In: DeEllJR ToivonenPMA (ed) Practical applications of chlorophyll fluorescence in plant biology. Kluwer, Boston, pp 151–184
Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Strudel. Plant Physiol 133:829–837
Pietrini F, Zacchini M, Iori V, Pietrosanti L, Ferretti M, Massacci A (2010) Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biol 12:355–363
Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540
Robinson BH, Mills TM, Green S, Chancerel B, Clothier B, Fung LE (2005) Trace element accumulation by poplars and willows used for stock fodder. New Zeland J Agric Res 48:489–497
Rosenqvist E (2001) Light acclimation maintains the redox state of PSII electron acceptor QA within a narrow range over a broad range of light intensities. Photosynth Res 70:299–310
Rousseau C, Belin E, Bove E, Rousseau D, Fabre F, Berruyer R, Guillaumès J, Manceau C, Jacques MA, Boureau T (2013) High thtoughput quantitative phenotyping of plant resistance using chlorophyll fluorescence image analysis. Plant Methods 9(17):1–13
Ruley AT, Sharma NC, Sahi SV (2004) Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiol Biochem 42:899–906
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Sgardelis S, Cook CM, Pantis JD, Lanaras T (1994) Comparison of chlorophyll fluorescence and some heavy metal concentrations in Sonchus spp. and Taraxacum spp. along an urban pollution gradient. Sci Total Environ 158:157–164
Terashima I (1992) Anatomy of non-uniform leaf photosynthesis. Photosynth Res 31:195–212
Tognetti R, Sebastiani L, Minnocci A (2004) Gas exchange and foliage characteristics of two poplar clones grown in soil amended with industrial waste. Tree Physiol 24:75–82
Valcke R, Ciscato M, Heisel F, Miehe J, Sowinska M (1999) Analysis of heavy-metal stressed plants by fluorescence imaging. In: Kamerman GW, Werner C (eds) Proceedings of SPIE, 13th annual international symposium on aerosense, Orlando, 3707: 82–90
Verbruggen N, Hermans C, Schat H (2008) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Yruela I, Pueyo JJ, Alonso PJ, Picorel R (1996) Photo-inhibition of photosystem II from higher plants: effect of copper inhibition. J Biol Chem 271:27408–27415
Zacchini M, Pietrini F, Scarascia Mugnozza G, Iori V, Pietrosanti L, Massacci A (2009) Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. Water Air Soil Pollut 197:23–34
Acknowledgments
This work was funded by ENEA (Italian National Agency for New Technologies, Energy and Sustainable Economic Development) during PhD fellowship period of Dr. M. Sighicelli. The authors also wish to thank Dr. A. Lai (ENEA) for research collaboration within the PhD research project and Dr. P. Menesatti (CRA-ING) and Dr. C. Costa (CRA-ING) for valuable technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sighicelli, M., Guarneri, M. Assessing the poplar photochemical response to high zinc concentrations by image processing and statistical approach. Photosynth Res 122, 315–322 (2014). https://doi.org/10.1007/s11120-014-0028-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-014-0028-2