Photosynthetic induction and activity of enzymes related to carbon metabolism: insights into the varying net photosynthesis rates of coffee sun and shade leaves

Abstract

The shade leaves of coffee (Coffea arabica L.) apparently retain a robust photosynthetic machinery that is comparable to that of sun leaves and can fix CO2 at high rates when subjected to high light intensities. This raises the question of why the coffee plant would construct such a robust photosynthetic machinery despite the low photosynthetic rates achieved by the shade leaves at low light supply. Here, we grew coffee plants at 100% or 10% full sunlight and demonstrated that the shade leaves exhibited faster photosynthetic induction compared with their sun counterparts, in parallel with lower loss of induction states under dim light, and were well protected against short-term sudden increases in light supply (mimicking sunflecks). These findings were linked to similar photosynthetic capacities on a per mass basis (assessed under nonlimiting light), as well as similar extractable activities of some enzymes of the Calvin cycle, including Rubisco, when comparing the shade and sun leaves. On the one hand, these responses might represent an overinvestment of resources given the low photosynthetic rates of the shade leaves when light is limiting; on the other hand, such responses might be associated with a conservative behavior linked to the origin of the species as a shade-dwelling plant, allowing it to maximize the use of the energy from sunflecks and thus ultimately contributing to a positive carbon balance under conditions of intense shading.

Coffea; photosynthesis; photosynthetic induction kinetics; sun/shade tolerance; sunflecks

• Araújo WL, Dias PC, Moraes GABK, Celin EF, Cunha RL, Barros RS, DaMatta FM (2008) Limitations to photosynthesis in coffee leaves from different canopy positions. Plant Physiology and Biochemistry 46:884-90.
• Bai K, Liao D, Jiang D, Cao K (2008) Photosynthetic induction in leaves of co-occurring Fagus lucida and Castanopsis lamontii saplings grown in contrasting light environments. Trees 22:449-62.
• Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28:355-77.
• Cavatte PC, Oliveira AAG, Morais LE, Martins SCV, Sanglard LMVP, DaMatta FM (2012) Could shading reduce the negative impacts of drought on coffee? A morphophysiological ¡analysis. Physiologia Plantarum 144:111-22.
• DaMatta FM (2004) Ecophysiological constraints on the production of shaded and unshaded coffee: a review. Field Crops Research 86:99-114.
• DaMatta FM, Ronchi CP, Maestri M, Barros RS (2010) Coffee: environment and crop physiology. In: DaMatta FM, editor. Ecophysiology of Tropical Tree Crops. New York: Nova Science Publishers. pp.181-216.
• Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78-90.
• Fernie AR, Roessner U, Trethewey RN, Willmitzer L (2001) The contribution of plastidial phosphoglucomutase to the control of starch synthesis within the potato tuber. Planta 213:418-26.
• Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990:87-92.
• Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79:209-18.
• Kursar TA, Coley PD (1993) Photosynthetic induction times in shade-tolerant species with long and short-lived leaves. Oecologia 93:165-70.
• Logan BA, Adams WW, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Functional Plant Biology 34:853-59.
• Lusk C, Reich, PB, Montgomery, RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends in Ecology and Evolution 23:299-303.
• Makino A, Miyake C, Yokota, A (2002) Physiological functions of the water-water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant and Cell Physiology 43:1017-26.
• Martins SCV, Galmés J, Molins A, DaMatta FM (2013) Improving the estimation of mesophyll conductance to CO2: on the role of electron transport rate correction and respiration. Journal of Experimental Botany In press.
• Matos FS, Wolfgramm R, Gonçalves FV, Cavatte PC, Ventrella MC, DaMatta FM (2009) Phenotypic plasticity in response to light in the coffee tree. Environmental and Experimental Botany 67:421-27.
• Moraes GABK, Chaves ARM, Martins SCV, Barros RS, DaMatta FM (2010) Why is it better to produce coffee seedlings in full sunlight than in the shade? A morphophysiological approach. Photosynthetica 48:199-207.
• Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant, Cell and Environment 30:1052-71.
• Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant Journal 50:1093-1106.
• Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ (2008) Rubisco regulation: a role for inhibitors. Journal of Experimental Botany 59:1569-80.
• Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annual Review of Plant Physiology and Plant Molecular Biology 41:421-53.
• Pearcy RW, Chazdon RL, Gross LJ, Mott KA (1994) Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. In: Caldwell MM, Pearcy RW, editors. Exploitation of Environmental Heterogeneity by Plants. San Diego: Academic Press. pp.175-208.
• Sage RF, Cen Y-P, Li M (2002) The activation state of Rubisco directly limits photosynthesis at low CO2 and low O2 partial pressures. Photosynthesis Research 71:241-50.
• Environment 30:1163-75.
• Tausz M, Warren CR, Adams MA (2005) Dynamic light use and protection from excess light in upper canopy and coppice leaves of Nothofagus cunninghamii in an old growth, cool temperate rainforest in Victoria, Australia. New Phytologist 165:143-55.
• Urban O, KoÜvancová M, Marek MV, Lichtenthaler HK (2007) Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. Tree Physiology 27:1207-15.
• Urban O, Sprtová M, KoÜvancová M, Tomásková I, Lichtenthaler HK, Marek MV (2008) Comparison of photosynthetic induction and transient limitations during the induction phase in young and mature leaves from three poplar clones. Tree Physiology 28:1189-97.
• Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111:505-14.
• Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution and Systematics 39:237-57.
• Walters RG (2005) Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany 56:435-47.
• Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiology 32:1066-81.
• Wayne PM, Bazzaz FA (1993) Birch seedling responses to daily time courses of light in experimental forest gaps and shadehouses. Ecology 74:1500-15.
• Wong SL, Chen CW, Huang HW, Weng JH (2012) Using combined measurements for comparison of light induction of stomatal conductance, electron transport rate and CO2 fixation in woody and fern species adapted to different light regimes. Tree Physiology 32:535-44.
• Woodrow IE, Mott KA (1989) Rate limitation of non-steady state photosynthesis by ribulose-1,5-bisphosphate carboxylase in spinach. Functional Plant Biology 16:487-500.

Publication Dates

• Publication in this collection
  23 June 2015
• Date of issue
  2013

History

• Received
  16 May 2013
• Accepted
  21 May 2013