Skip to main content
Log in

Fluorescence parameters among leaf photosynthesis-related traits are the best proxies for CO2 assimilation in Central Amazon trees

  • Original Article
  • Published:
Brazilian Journal of Botany Aims and scope Submit manuscript

Abstract

We investigated whether photosynthesis along the vertical profile of tropical forest can be represented by JIP-test parameters derived from the fluorescence induction curve instead of more commonly utilized traits. Photosynthesis-related traits were measured during four seasons in 45 trees along a vertical forest profile in the Central Amazon, and their combined (interspecific) correlations with canopy openness and PNmax (light-saturated photosynthesis) were examined. PNmax, canopy openness, the efficiency of electron transport in PSI (IP-phase and RE0/ET0), leaf mass per area and leaf phosphorus content had strong positive correlations (r > 0.6). JIP-test parameters related to the final steps of electron transport (IP-phase, RE0/ET0 and PItotal) were good predictors of PNmax during all seasons, whereas stomatal conductance had the strongest correlation with PNmax during the dry season. The JIP-test parameters related to PSII efficiency (PIABS and FV/FM) were poorly associated with PNmax. Therefore, the PNmax variation along the vertical profile of Central Amazonian forest can be represented by JIP-test parameters, especially those related to the final steps of the electron transport chain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Aguiar TV, Sant’anna-Santos BF, Azevedo AA, Santos RF (2007) Anati quanti: software de análises quantitativas para estudos em anatomia vegetal. Planta Daninha 25:649–659

    Article  Google Scholar 

  • Araújo AC, Nobre AD, Kruijt B, Elbers JA, Dallarosa R, Stefani P, Randow C, Manzi AO, Culf AD, Gash JHC, Valentini R, Kabat P (2002) Comparative measurements of carbon dioxide fluxes from two nearby towers in a central Amazonian rainforest: the Manaus LBA site. J Geophys Res 107:80–90

    Article  Google Scholar 

  • Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24:163–176

    Article  CAS  Google Scholar 

  • Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355–377

    Article  CAS  Google Scholar 

  • Bremner JM (1996) Nitrogen-total. In: Sparks DL (ed) Methods of soil analysis, part 3, chemical methods. American Society of Agronomy, Madison, WI, pp 1085–1121

    Google Scholar 

  • Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Manes F (2011) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19–30

    Article  CAS  Google Scholar 

  • Campos H, Trejo C, Valdiva P, Nava G, Martinez C, Ortega C (2014) Stomatal and non-stomatal limitations of bell pepper plants under water stress and re-watering: delayed restoration of growth and photosynthesis during recovery. Environ Exp Bot 98:56–64

    Article  CAS  Google Scholar 

  • Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol 20:179–186

    Article  PubMed  Google Scholar 

  • Cascio C, Schaub M, Novak K, Desotgiu R, Bussotti F, Strasser RJ (2010) Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions. Environ Exp Bot 68:188–197

    Article  CAS  Google Scholar 

  • Castro F (2000) Light spectral composition in a tropical forest: measurements and model. Tree Physiol 20:49–56

    Article  PubMed  Google Scholar 

  • Castro Y, Fetcher N, Fernández DS (1995) Chronic photoinhibition in seedlings of tropical trees. Physiol Plantarum 94:560–565

    Article  CAS  Google Scholar 

  • Cavaleri MA, Oberbauer SF, Clark DB, Clark DA, Ryan MG (2010) Height is more important than light in determining leaf morphology in a tropical forest. Ecology 91:1730–1739

    Article  PubMed  Google Scholar 

  • Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plantarum 144:277–288

    Article  CAS  Google Scholar 

  • Chazdon RL, Fetcher N (1984) Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. J Ecol 72:553–564

    Article  Google Scholar 

  • Craine JM, Reich PB (2005) Leaf-level light compensation points in shade-tolerant woody seedlings. New Phytol 166:710–713

    Article  PubMed  Google Scholar 

  • Cunha HFV, Gonçalves JFC, Santos Junior UM, Ferreira MJ, Peixoto PHP (2016) Biomassa, trocas gasosas e aspectos nutricionais de plantas jovens de pau de balsa (Ochroma pyramidale (Cav. Ex Lamb.) Urb.) submetidas à fertilização fosfatada em ambientes contrastantes de irradiância. Sci For 44:215–230

    Google Scholar 

  • Demmig-Adams B, Adams WW III (2000) Photosynthesis: harvesting sunlight safely. Nature 403:371–374

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  PubMed  Google Scholar 

  • Desotgiu R, Pollastrini M, Cascio C, Gerosa G, Marzuoli R, Bussotti F (2012) Chlorophyll a fluorescence analysis along a vertical gradient of the crown in a poplar (Oxford clone) subjected to ozone and water stress. Tree Physiol 32:976–986

    Article  CAS  PubMed  Google Scholar 

  • Domingues TF, Berry JA, Martinelli LA, Ometto JP, Ehleringer JR (2005) Parameterization of canopy structure and leaf-level gas exchange for an eastern Amazonian tropical rain forest (Tapajos National Forest, Para, Brazil). Earth Interact 9:1–23

    Article  Google Scholar 

  • Domingues TF, Martinelli LA, Ehleringer JR (2013) Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest. Plant Ecol Divers 7:189–203

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767

    Article  CAS  Google Scholar 

  • Girardin CA, Malhi Y, Doughty CE, Metcalfe DB, Meir P, Aguila-Pasquel J, Araujo-Murakami A, da Costa ACL, Silva-Espejo JE, Amézquita FF, Rowland L (2016) Seasonal trends of Amazonian rainforest phenology, net primary productivity, and carbon allocation. Global Biogeochem Cy 30:700–715

    Article  CAS  Google Scholar 

  • Graham EA, Mulkey SS, Kitajima K, Phillips NG, Wright SJ (2003) Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons. Proc Natl Acad Sci USA 100:572–576

    Article  CAS  PubMed  Google Scholar 

  • Hendry GAF, Price AH (1993) Stress indicators: chlorophylls and carotenoids. In: Hendry GAF, Grime JP (eds) Methods in comparative plant ecology. Chapman & Hall, London, pp 148–152

    Chapter  Google Scholar 

  • Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991

    Article  CAS  Google Scholar 

  • Hidaka A, Kitayama K (2013) Relationship between photosynthetic phosphorus-use efficiency and foliar phosphorus fractions in tropical tree species. Ecol Evol 3:4872–4880

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishii H, Azuma W, Nabeshima E (2013) The need for a canopy perspective to understand the importance of phenotypic plasticity for promoting species coexistence and light-use complementarity in forest ecosystems. Ecol Res 28:191–198

    Article  Google Scholar 

  • Jiménez-Muñoz JC, Mattar C, Barichivich J, Santamaría-Artigas A, Takahashi K, Malhi Y, Sobrino JA, van der Schrier G (2016) Record-breaking warming and extreme drought in the Amazon rainforest during the course of El Niño 2015–2016. Sci Rep UK 6:33130

    Article  CAS  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  CAS  Google Scholar 

  • Kenzo T, Ichie T, Yoneda R, Kitahashi Y, Watanabe Y, Ninomiya I, Koike T (2004) Interspecific variation of photosynthesis and leaf characteristics in canopy trees of five species of Dipterocarpaceae in a tropical rain forest. Tree Physiol 24:1187–1192

    Article  PubMed  Google Scholar 

  • Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T (2006) Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol 26:865–873

    Article  CAS  PubMed  Google Scholar 

  • Kenzo T, Inoue Y, Yoshimura M, Yamashita M, Tanaka-Oda A, Ichie T (2015) Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees. Oecologia 177:191–202

    Article  PubMed  Google Scholar 

  • Kosugi Y, Takanashi S, Yokoyama N, Philip E, Kamakura M (2012) Vertical variation in leaf gas exchange parameters for a Southeast Asian tropical rainforest in Peninsular Malaysia. J Plant Res 125:735–748

    Article  PubMed  Google Scholar 

  • Krause GH, Winter K, Matsubara S, Krause B, Janhs P, Virgo A, Aranda J, García M (2012) Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight. Photosynth Res 113:273–285

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Babani F (2004) Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 713–736

    Chapter  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc T 11:591–592

    Article  CAS  Google Scholar 

  • Lin ZH, Chen LS, Chen RB, Zhang FZ, Jiang HX, Tang N (2009) CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport probed by the JIP-test, of tea leaves in response to phosphorus supply. BMC Plant Biol 9:43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyazawa M, Pavan MA, Muraoka T, Carmo CAFS, Mello WJ (1999) Análise química de tecidos vegetais. In: Silva FC (ed) Manual de Análise Química de Solos, Plantas e Fertilizantes. EMBRAPA, Brasília, pp 172–223

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nicotra AB, Chazdon RL, Iriarte SV (1999) Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80:1908–1926

    Article  Google Scholar 

  • Niinemets Ü (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714

    Article  Google Scholar 

  • Nikiforou C, Manetas Y (2011) Inherent nitrogen deficiency in Pistacia lentiscus preferentially affects photosystem I: a seasonal field study. Funct Plant Biol 38:848–855

    Article  CAS  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927

    Article  Google Scholar 

  • Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol Plantarum 137:188–199

    Article  CAS  Google Scholar 

  • Pollastrini M, Holland V, Brüggemann W, Bruelheide H, Dănilă I, Jaroszewicz B, Valladares F, Bussotti F (2016) Taxonomic and ecological relevance of the chlorophyll a fluorescence signature of tree species in mixed European forests. New Phytol 212:51–65

    Article  CAS  PubMed  Google Scholar 

  • Pollastrini M, Nogales AG, Benavides R, Bonal D, Finer L, Fotelli M, Gessler A, Grossiord C, Radoglou K, Strasser RJ, Bussotti F (2017) Tree diversity affects chlorophyll a fluorescence and other leaf traits of tree species in a boreal forest. Tree Physiol 37:199–208

    CAS  PubMed  Google Scholar 

  • Poorter L, Arets EJMM (2003) Light environment and tree strategies in a Bolivian tropical moist forest: an evaluation of the light partitioning hypothesis. Plant Ecol 166:295–306

    Article  Google Scholar 

  • Quesada CA, Phillips OL, Schwarz M et al (2012) Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9:2203–2246

    Article  Google Scholar 

  • Quevedo-Rojas A, García-Núñez C, Jerez-Rico M, Jaimez R, Schwarzkopf T (2018) Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest. Funct Plant Biol 45:968–982

    Article  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Ribeiro RV, Souza GM, Oliveira RF, Machado EC (2005) Photosynthetic responses of tropical tree species from different successional groups under contrasting irradiance conditions. Braz J Bot 28:149–161

    Article  Google Scholar 

  • Santos-Junior UM, Gonçalves JFC, Fearnside PM (2013) Measuring the impact of flooding on Amazonian trees: photosynthetic response models for ten species flooded by hydroelectric dams. Trees Struct Funct 27:193–210

    Article  CAS  Google Scholar 

  • Santos VAHFD, Ferreira MJ, Rodrigues JVFC, Garcia MN, Ceron JVB, Nelson BW, Saleska SR (2018) Causes of reduced leaf-level photosynthesis during strong El Niño drought in a Central Amazon forest. Glob Change Biol 24:4266–4279

    Article  Google Scholar 

  • Schansker G, Srivastava A, Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785–796

    Article  CAS  Google Scholar 

  • Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta 1706:250–261

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photoch Photobio B 104:236–257

    Article  CAS  Google Scholar 

  • Stirbet A, Lazár D, Kromdijk J, Govindjee (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica. https://doi.org/10.1007/s11099-018-0770-3

    Article  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In: Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security. SSARM, Hisar, pp 72–115

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Giang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    Article  CAS  PubMed  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art. Genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer, Dordrecht, pp 679–703

    Chapter  Google Scholar 

  • Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol S 39:237–257

    Article  Google Scholar 

  • Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Ann Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • Weerasinghe LK, Creek D, Crous KY, Xiang S, Liddell MJ, Turnbull MH, Atkin OK (2014) Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland. Tree Physiol 34:564–584

    Article  CAS  PubMed  Google Scholar 

  • Wright SJ, Colley M (1994) Accessing the canopy: Phase I. United Nation Environmental Program, Nairobi, Kenya, Assessment of Biological Diversity and Microclimate of the Tropical Forest Canopy

    Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Nava ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1999) Biostatical analysis. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgements

We thank the Federal University of Amazonas (UFAM), Brazil’s National Institute for Amazon Research (INPA) and the Large-Scale Biosphere–Atmosphere Experiment in Amazonia Program (LBA) for logistic support; the GOAmazon project, funded jointly by the US Department of Energy (DOE, # DE. SC0008383), by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and by the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM, # 062.00570/2014); the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a fellowship.

Author information

Authors and Affiliations

Authors

Contributions

VAHFS and MJF designed the research. VAHFS, MNG and JVBC collected the data. VAHFS analyzed the data and wrote a draft of the manuscript. BWN and JVFCR revised the text. All authors contributed to the final version of the manuscript and approved submission.

Corresponding author

Correspondence to Marciel José Ferreira.

Ethics declarations

Conflict of interest

None declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 43 kb)

Supplementary material 2 (XLSX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

dos Santos, V.A.H.F., Nelson, B.W., Rodrigues, J.V.F.C. et al. Fluorescence parameters among leaf photosynthesis-related traits are the best proxies for CO2 assimilation in Central Amazon trees. Braz. J. Bot 42, 239–247 (2019). https://doi.org/10.1007/s40415-019-00533-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-019-00533-2

Keywords

Navigation