Abstract
Light is a limiting factor in plant establishment and growth in the understory of forests. In this paper, we assessed acclimation capacity of Siparuna guianensis, an early secondary successional species. We used seedlings and saplings in three regeneration areas with different irradiance regimes to determine the traits that confer photoplasticity. We examined whether these traits differ at different developmental stages. Anatomical characteristics, photochemical efficiency, photosynthetic capacity, and growth were analyzed. Multivariate component analysis revealed the formation of six clusters: three for seedlings (one for each regeneration area) and three for saplings (following the same pattern of seedlings, considering the area). Increased irradiance favored photosynthetic performance, independently of the developmental stage. The same trend was observed for most data on chlorophyll (Chl) a fluorescence and the ratios of net photosynthetic rate/intercellular CO2 concentration (P N/Ci) and P N/PPFD. No parameter indicated photoinhibition stress. The CO2− and light-response curve data indicated that seedlings were already acclimated to tolerate variation in irradiance. Anatomical adaptations, such as thickness of leaf blade and of adaxial cuticle, were observed in individuals growing in areas with higher irradiation. Thinning of spongy parenchyma and higher investment into a plant height were observed in seedlings, possibly due to the vertical stratification of CO2 and light in the understory; because light is a more limiting resource than CO2 in the lower stratum of the forest. Photoplasticity in S. guianensis is associated with a set of morphological, anatomical, photochemical, and biochemical traits, whereas biochemical performance is best acclimated to variation in irradiance. These traits differed in seedlings and saplings but they were modulated mainly by irradiance in both developmental stages.
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Abbreviations
- ab:
-
abaxial surface
- ad:
-
adaxial surface
- Car:
-
carotenoids
- CCU:
-
closed canopy understory
- Chl:
-
chlorophyll
- C i :
-
intercellular CO2 concentration
- ct:
-
cuticle
- DGL:
-
diameter at ground level
- DMSO:
-
dimethylsulfoxide
- ETR:
-
electron transport rate
- FV:
-
final value
- Fv/Fm :
-
maximal quantum yield of PSII
- g s :
-
stomatal conductance
- GN:
-
percentage gain
- H:
-
height
- ICU:
-
intermediate canopy understory
- IV:
-
initial values
- Jmax :
-
maximal electron transport rate
- L s :
-
relative stomatal limitation to photosynthesis
- NL:
-
number of leaves
- NPQ:
-
nonphotochemical quenching
- OCU:
-
open canopy understory
- PCA:
-
principal component analysis
- PC1:
-
first principal component
- PC2:
-
second principal component
- P N :
-
net photosynthetic rate
- P Neff :
-
effective net photosynthetic rate
- P NmaxC :
-
potential net photosynthetic capacity
- P Nmax :
-
maximal net photosynthetic rate
- P NmaxL :
-
maximal net photosynthetic capacity
- pp:
-
palisade parenchyma
- LSP:
-
light-saturation point
- qP :
-
photochemical quenching
- RH:
-
relative humidity
- SAC:
-
shade adjustment coefficient
- sp:
-
spongy parenchyma
- T:
-
temperature
- TLA:
-
total leaf area
- TPU:
-
use of triose-phosphate
- Vcmax :
-
maximal carboxylation speed of Rubisco
- VPD:
-
vapor pressure deficit
- ΔG:
-
delta growth
- ΔF/Fm′:
-
effective quantum yield
References
Araújo S.A.C., Deminicis B.B.: [Photosynthesis and photoinhibition: a review.] — Rev. Bras. Biociên. 7: 463–472, 2009. [In Portuguese]
Azevedo G.F.C., Marenco R.A.: Growth and physiological changes in saplings of Minquartia guianensis and Swietenia macrophylla during acclimation to full sunlight. — Photosynthetica 50: 86–94, 2012.
Bazzaz F.A.: Physiological ecology of plant succession. — Annu. Rev. Ecol. Syst. 10: 351–371, 1979.
Bazzaz F.A., Pickett S.T.A.: Physiological ecology of tropical succession: a comparative review. — Annu. Rev. Ecol. Syst. 11: 287–310, 1980.
Bilger W., Schreiber U., Bock M.: Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. — Oecologia 102: 425–432, 1995.
Bolhàr-Nordenkampf H.R., Long S.P., Baker N.R.: Chlorophyll fluorescence as probe of the photosynthetic competence of leaves in the field: a review of current instrument. — Funct. Ecol. 3: 497–514, 1989.
Brodersen C.R., Vogelmann T.C.: Do epidermal lens cells facilitate the absorptance of diffuse light? — Am. J. Bot. 94: 1061–1066, 2007.
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.
Chazdon R.L., Pearcy R.W., Lee D.W. et al.: Photosynthetic response of tropical forest plants to contrasting light environments. — In: Mulkey S.S., Chazdon R.L., Smith A.P. (ed.): Tropical Forest Plant Ecophysiology. Pp. 5–55. Chapman and Hall, New York 1996.
de Lucia E.H., Nelson K., Vogelmann T.C. et al.: Contribution of intercellular reflectance to photosynthesis in shade leaves. — Plant Cell Environ. 19: 159–170, 1996.
Demmig-Adams B., Adams W.W., Heber U. et al.: Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. — Plant Physiol. 92: 293–301, 1990.
Demmig-Adams B., Adams W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis. — Trends Plant Sci. 1: 21–26, 1996.
de Pury D.G.G., Farquhar, G.D.: Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. — Plant Cell Environ. 20: 537–557, 1997.
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.
Evans J.R.: Leaf anatomy enables more equal access to light and CO2 between chloroplasts. — New Phytol. 143: 93–104, 1999.
Evaristo V.T., Braga J.M.A., Nascimento M.T.: Atlantic Forest regeneration in abandoned plantations of eucalypt (Corymbia citriodora) in Rio de Janeiro, Brazil. — Interciência 36: 431–436, 2011.
Farquhar G.D., Sharkey T.D.: Stomatal conductance and photosynthesis. — Annu. Rev. Plant Phys. 33: 317–345, 1982.
Gandolfi S., Joly C.A., Filho H.F.L.: “Gaps of deciduosness”: cyclical gaps in tropical forests. — Sci. Agr. 66: 280–284, 2009.
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.
Haberlandt G.: Physiological Plant Anatomy (4th Ed). Pp. 807. Macmillan & Co. Ltd. London 1914.
Hendry G.A.F., Price A.H.: Stress indicators: chlorophylls and carotenoids. — In: Hendry G.A.F., Grime J.P. (ed.): Methods in comparative Plant Ecology. Pp 148–152. Chapman & Hall, London 1993.
Holloway P.J.: Structure and histochemistry of plant cuticular membranes: an overview. — In: Cutler D.F., Alvin K.L., Price C.E. (ed.): The Plant Cuticle. Pp. 1–32. Academic Press, London 1982.
Huang D., Wu L., Chen J.R. et al.: Morphological plasticity, photosynthesis and chlorophyll fluorescence of Athyrium pachyphelebium at different shade levels. — Photosynthetica 49: 611–618, 2011.
IBGE (Instituto Brasileiro de Geografia e Estatística). [Technical Manual of Brazilian Vegetation. Technical Manuals Series in Geosciences n. 1]. Pp 91. IBGE, Rio de Janeiro 1992. [In Portuguese]
Ishida A., Yazaki K., Hoe A.L.: Ontogenetic transition of leaf physiology and anatomy from seedlings to mature trees of a rain forest pioneer tree, Macaranga gigantean. — Tree Physiol. 25: 513–522, 2005.
Johnson D.M., Smith W.K., Vogelmann T.C. et al.: Leaf architecture and direction of incident light influence mesophyll fluorescence profiles. — Am. J. Bot. 92: 1425–1431, 2005.
Kao W.Y., Chin Y.S., Chen W.H.: Vertical profiles of CO2 concentrations and δ13C values in a subalpine forest of Taiwan. — Bot. Bull. Acad. Sinica 41: 213–218, 2000.
Klein D.E., Gomes V.M., Neto S.J.S. et al.: The structure of collecters in several species of Simira (Rubiaceae). — Ann Bot.-London 94: 733–740, 2004.
Kitajima K.: Ecophysiology of tropical tree seedlings. — In: Mulkey S. S., Chazdon R. L. Smith A. P. (ed.): Tropical Forest Plant Ecophysiology. Pp. 559–597. Chapman & Hall, New York 1996.
Kitajima K.: Relative importance of photosynthetic traits an allocation patterns as correlates of seedling shad tolerance of 13 tropical trees. — Oecologia 98: 419–428, 1994.
Köppen W.: [Climatology: a Study of the Climates of the Earth.] Pp. 479. Fondo de Cultura Econômica (FCE), México 1948. [In Spanish]
Küppers M., Timm H., Orth F. et al.: Effects of light environment and successional status on light fleck use by understorey trees of temperate and tropical forests. — Tree Physiol. 16: 69–80, 1996.
Lage-Pinto F., Bernini E, Oliveira J.G. et al.: Photosynthetic analyses of two native Atlantic Forest species in regenerative understorey of eucalyptus plantation. — Braz. J. Plant Physiol. 24: 95–106, 2012.
Laisk H., Eichelmann V., Oja B. et al.: Adjustment of leaf photosynthesis to shade in a natural canopy: rate parameters. — Plant Cell Environ. 28: 375–388, 2005.
Lemos J.P., Mendonça C.V.: Seasonal changes in the water status of three woody legumes from the Atlantic forest, Caratinga, Brazil. — J. Trop. Ecol. 16: 21–32, 2000.
Long S. P., Bernacchi C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. — J. Exp. Bot. 54: 2393–2401, 2003.
Marenco R.A., Vieira G.: Specific leaf area e photosynthetic parameters of tree species in the forest understorey as a function of the microsite light environment in Central Amazonia. — J. Trop. For. Sci. 17: 265–278, 2005.
Merzlyak M.N., Solovchenko A.E.: Photostability of pigments in ripening apple fruit: a possible photoprotective role of carotenoids during plant senescence. — Plant Sci. 163: 881–888, 2002.
Miyashita A., Sugiura D., Sawakami K. et al.: Long-term, shortinterval measurements of the frequency distributions of the photosynthetically active photon flux density and net assimilation rates of leaves in a cool-temperate forest. — Agr. Forest Meteorol. 152: 1–10, 2012.
Monteiro J.A.F., Prado C.H.B.A.: Apparent carboxylation efficiency and relative stomatal and mesophyll limitations of photosynthesis in an evergreen cerrado species during water stress. — Photosynthetica 44: 39–45, 2006.
Montgomery R.A, Givnish T.J.: Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: dynamic photosynthetic responses. — Oecologia 155: 455–467, 2008.
Montgomery R.A.: Relative importance of photosynthetic physiology and biomass allocation for tree seedling growth across a broad light gradient. — Tree Physiol. 24: 155–167, 2004.
Montgomery R.A., Chazdon R.L.: Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. — Oecologia 131: 165–174, 2002.
Mott K.A., Woodrow I.E.: Effects of O2 and CO2 on non steady state photosynthesis. — Plant Physiol. 102: 859–866, 1993.
Myers N., Mittermeier R.A., Mittermeier C.G. et al.: Biodiversity hotspots for conservation priorities. — Nature 403: 853–858, 2000.
Nascimento H.C.S, Marenco R.A.: Mesophyll conductance variations in response to diurnal environmental factors in Myrcia paivae and Minquartia guianensis in Central Amazonia. — Photosynthetica 51: 457–464, 2013.
O’Brien T.P., Feder N., McCully M.E.: Polychromatic staining of plant cell walls by toluidine blue O. — Protoplasma 59: 368–373, 1964.
Oguchi R., Hikosaka K., Hirose T.: Does the photosynthetic lightacclimation need change in leaf anatomy? — Plant Cell Environ. 26: 505–512, 2003.
Pandey S., Kushwaha R.: Leaf anatomy and photosynthetic acclimation in Valeriana jatamansi L. grown under high and low irradiance. — Photosynthetica 43: 85–90, 2005.
Pearcy R.W., Chazdon R.L., Gross L.J. et al.: Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. — In: Caldwell M.M., Pearcy R.W. (ed.): Exploitation of Environmental Heterogeneity by Plants: Ecophysiology Processes Above and Below Ground. Pp. 175–208. Academic Press, New York 1994.
Poorter H., Pothmann P.: Growth and carbon economy of a fast growing and a slow-growing grass species as dependent on ontogeny. — New Phytol. 120: 159–166, 1992.
Poorter L.: Growth responses of 15 rainforest tree species to a light gradient: the relative importance of morphological and physiological traits. — Funct. Ecol. 13: 396–410, 1999.
Portes M.T., Damineli D.S.C., Ribeiro R.V. et al.: Evidence of higher photosynthetic plasticity in the early successional Guazuma ulmifolia Lam. compared to the late successional Hymenaea courbaril L. grown in contrasting light environments. — Braz. J. Biol. 70: 75–83, 2010.
Prado C.H.B.A., Moraes J.A.P.V.: Photosynthetic capacity and specific leaf mass in twenty woody species of cerrado vegetation under field conditions. — Photosynthetica 33: 103–112, 1997.
Rabelo G.R., Klein D.E., da Cunha M.: Does selective logging affect the leaf structure of a late successional species? — Rodriguesia 63: 419–427, 2012.
Rabelo R.G., Vitória A.P., da Silva M.V.A. et al.: Structural and ecophysiological adaptations to forest gaps. — Trees-Struct. Funct. 27: 259–272, 2013.
Renner S.S., Hausner G.: Monograph of Siparunaceae. — In: New York Botanical Garden: Flora Neotropica 95. Pp. 256. Hafner Publ. Co., New York 2005.
Ribeiro R.F., Souza G.M., Oliveira R.F. et al: Photosynthetic responses of tropical tree species from different successional groups under contrasting irradiance conditions. — Rev. Bras. Bot. 28: 149–161, 2005.
Ronquim C.C., Prado C.H.B.A., Paula N.F.: Growth and photosynthetic capacity in two woody species of cerrado vegetation under different radiation availability. — Braz. Arch. Biol. Techn. 46: 243–252, 2003.
Rosevear M.J., Young A.J., Johnson G.N.: Growth conditions are more important than species origin in determining leaf pigment content of British plant species. — Funct. Ecol. 15: 474–480, 2001.
Rozema J., Chardonnens A., Tossermams M. et al.: Leaf thickness and UV-B absorbing pigments of plants in relation to an elevational gradient along the Blue Montains, Jamaica. — Plant Ecol. 128: 150–159, 1997.
Santiago L.S., Dawson T.E.: Light use efficiency of California redwood understorey plants along a moisture gradient. — Oecologia 174: 351–363, 2014.
Sassenrath-Cole G.F., Pearcy R.W.: The role of ribulose-1,5-bisphosphate regeneration in the induction requirement of photosynthetic CO2 exchange under transient light conditions. — Plant Physiol. 99: 227–234, 1992.
Sharkey T.D.: Estimating the rate of photorespiration in leaves. — Physiol. Plantarum 73: 147–152, 1988.
Sharkey T.D., Bernacchi C.J., Farquhar G.D. et al.: Fitting photosynthetic carbon dioxide response curves for C3 leaves. — Plant Cell Environ. 30: 1035–1040, 2007.
Silva A.S., Oliveira J.G., da Cunha M. et al.: Photosynthetic performance and anatomical adaptations in Byrsonima sericea DC. under contrasting light conditions in a remnant of the Atlantic forest. — Braz. J. Plant. Physiol. 22: 245–254, 2010.
Silvestrini M., Válio I.F.M., Mattos E.A.: Photosynthesis and carbon gain under contrasting light levels in seedlings of a pioneer and a climax tree from a Brazilian semideciduous Tropical Forest. — Rev. Bras. Bot. 30: 463–474, 2007
Smith H.: Light quality, photoreception, and plant strategy. — Annu. Rev. Plant Phys. 33: 481–518, 1982.
Souza G.M., Balmant B.D., Vítolo H.F. et al.: [Light utilization strategies and developmental stability of Cordia superba Cham. (Boraginaceae) seedlings grown in different light environments.] — Acta Bot. Bras. 23: 474–485. 2009. [In Portuguese]
Souza G.M., Ribeiro R.V., Sato A.M. et al.: Diurnal and seasonal carbon balance of four tropical tree species differing in successional status. — Braz. J. Biol. 68: 781–793, 2008.
Strauss-Debenedetti S., Bazzaz F.A.: Photosynthetic characteristics of tropical trees along sucessional gradients. — In: Mulkey S.S., Chazdon R.L, Smith A.P. (ed.): Tropical Forest Plant Ecophysiology. Pp.162–186. Chapman & Hall, New York 1996.
Strauss-Debenedetti S., Berlyn G.P.: Leaf anatomical responses to light in five tropical Moraceae of different successional status. — Am. J. Bot. 81: 1582–1591, 1994.
Sultan S.E.: Phenotypic plasticity in plants: A case study in ecological development. — Evol. Dev. 5: 25–33, 2003.
Terashima I., Miyazawa S.I., Hanba Y.T.: Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. — J. Plant Res. 114: 93–105, 2001.
Unwin D.M.: Microclimate Measurement for Ecologists. Pp. 97. Academic Press, New York 1980.
Valentini C.M.A., Rodrigues-Ortiz C.E., Coelho M.F.B.: [Siparuna guianensis Aublet (negramina): a review.] — Rev. Bras. Plantas Med. 12: 96–104, 2010. [In Portuguese]
Valladares F., Allen M.T., Pearcy R.W.: Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. — Oecologia 111: 505–514, 1997.
Valladares F., Wright S.J., Lasso E. et al.: Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. — Ecology 81: 1925–1936, 2000.
Vieira T.O., Lage-Pinto F., Ribeiro D.R. et al.: [Photostress in Cariniana legalis, Lecythidaceae seedlings: monitoring of photosynthetic acclimation capacity under two irradiance regimes.] — Vértices 13: 129–142, 2011. [In Portuguese]
Vogelmann T.C., Nishio J.N., Smith W.K. et al.: Leaves and light capture: light propagation and gradients of carbon fixation within leaves. — Trends Plant Sci. 1: 65–70, 1996.
Vogelmann T.C., Martin G.: The functional significance of palisade tissue: Penetration of directional vs. diffuse light. — Plant Cell Environ. 16: 65–72, 1993.
Way D.A., Pearcy R.W.: Sunflecks in trees and forests: from photosynthetic physiology to global change biology. — Tree Physiol. 32: 1066–1081, 2012.
Wellburn A. R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. — J. Plant Physiol. 144: 307–313, 1994.
Yanhong T., Hiroshi K., Mitsumasa S. et al.: Characteristics of transient photosynthesis in Quercus serrata seedlings grown under lightfleck and constant light regimes. — Oecologia 100: 463–469, 1994.
Zhou S.B., Liu K., Zhang D. et al.: Photosynthetic performance of Lycoris radiata var. radiata to shade treatments. — Photosynthetica 48: 241–248, 2010.
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Vieira, T.O., Degli-Esposti, M.S.O., Souza, G.M. et al. Photoacclimation capacity in seedling and sapling of Siparuna guianensis (Siparunaeae): Response to irradiance gradient in tropical forest. Photosynthetica 53, 11–22 (2015). https://doi.org/10.1007/s11099-015-0073-x
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DOI: https://doi.org/10.1007/s11099-015-0073-x