Photosynthetic Performance of Banana ( Gros Michel, AAA) under a Natural Shade Gradient

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1 Photosynthetic Performance of Banana ( Gros Michel, AAA) under a Natural Shade Gradient P. Siles 1, O. Bustamante 1, E. Valdivia 2, J. Burkhardt 3 and C. Staver 4 1 Bioversity International, C/o CATIE, Turrialba, Costa Rica 2 CATIE, Turrialba, Costa Rica 3 University of Bonn, Bonn, Germany 4 Bioversity International, Parc Scientifique Agropolis II, Montpellier Cedex 5, France Keywords: agroforestry systems, banana leaf, light, photosynthesis model, shade acclimation Abstract Bananas are frequently grown in coffee and cacao agroforestry systems. We asked whether tree shade affects leaf photosynthesis beyond simply the effects of the reduction in light availability. Does the leaf compensate for lower light availability to achieve greater than expected leaf photosynthesis? In this study, the photosynthetic performance at leaf level of banana (Musa, AAA, Gros Michel ) under three levels of natural shade (25, 50 and 75% of full solar irradiance) was compared with a full sun control. Gas exchange measurements of light and CO 2 response curves on the third youngest leaf were conducted to estimate the parameters of a biochemical model of leaf photosynthesis. The estimated parameters were potential lightsaturated electron transport rate (J max ), maximum carboxylation rate (V cmax ) and day respiration (R d ) standardized at 25 C. The mean parameters of photosynthesis varied under the different levels of shade. J max decreased with increasing shade, falling from 163 for full sun to 134, 124 and 95 μmol m -2 s -1 for 75, 50 and 25%, respectively. V cmax was reduced only with the heaviest shade from 104 μmol m -2 s -1 in full sun to 69 at 25% light, while no significant differences were found for R d. Light response curves showed a reduction of maximal leaf photosynthesis only at 50 and 25% full solar irradiance. No saturation value for the photosynthetic photon flux density was apparent in full sun or the 75% treatment, while the saturating photon flux density varied from 1,200 to 1,500 μmol m -2 s -1 in the 50 and 25% treatments. The results in conjunction with whole plant performance and indirect effects of shade on disease levels and nutrient cycles provide insight into improving the productivity and ecological services of bananas in multi-strata agroforestry systems. INTRODUCTION Banana is commonly grown in monocrop and agroforestry plantations in tropical or subtropical conditions (Dold et al., 2007). In Central America, bananas are found in agroforestry systems of cacao or coffee under the shade of tall trees, and under a wide range of environmental conditions from sea level to 1500 m a.s.l. (Haggar et al., 2001; Schibli, 2001). The cultivars used in agroforestry systems vary from region to region with a high diversity of cultivars. Gros Michel (AAA, Gros Michel subgroup) which is susceptible to Fusarium wilt, is the preferred cultivar for national dessert banana markets and is the most common cultivar found in coffee agroforestry systems in Central America and Peru (Siles et al., 2010a). In coffee agroforestry systems, the shade experienced by banana ranges from 30 to 80% of full irradiance depending on tree density (Siles et al., 2010a). Furthermore, the reduction in photosynthetic photon flux density (PPFD) is not the only environmental variable affected by trees. Air and leaf temperature and evaporative demand also are reduced (Barradas and Fanjul, 1986; Siles et al., 2010b; Siles and Vaast, 2002). While monocrop banana yields increase with radiation interception when no other factors are limiting, at leaf level the form of light response curves of banana net photosynthesis (A n ) varies considerably. The maximum rates of A n vary from 5 to 25 µmol m -2 s -1 and the Proc. Int. ISHS-ProMusa Symp. on Bananas and Plantains: Towards Sustainable Global Production and Improved Uses Eds.: I. Van den Bergh et al. Acta Hort. 986, ISHS

2 saturation values of the PPFD vary from 700 to more than 2,000 µmol m -2 s -1 (Turner, 1998a,b; Turner et al., 2007). Additionally, there is some evidence of acclimation of the leaf to maximize photosynthesis under low light conditions (Norgrove, 1998), but few reports exist that show the effect of shade acclimation on the photosynthetic parameters of banana. The objective of this study was to determine if the photosynthetic parameters of leaves of Gros Michel under four light levels indicated a photosynthetic compensation response by the leaves. MATERIALS AND METHODS The study was conducted at the Centro Agronómico Tropical de Investigación y Enseñanza (CATIE), Turrialba (9 53 N; W, 602 m a.s.l.), Costa Rica. The region is classified in the Holdridge life zone system as humid mid-altitude tropical forest with average annual precipitation above 2700 mm, average temperature of 22 C and average global radiation of 16.6 MJ m -2 d -1. In May 2010 ten common Musa spp. cultivars found in coffee agroforestry systems were planted under three levels of natural shade (25, 50 and 75% of full solar irradiance) and a full sun control treatment. In each plot, five individuals per cultivar were established. For gas exchange, four individuals of Gros Michel per shade level were measured. Leaf Gas Exchange Gas exchange was measured with an infrared gas analyzer and leaf chamber system with a red (635 nm) + blue (460nm) light source (LI-6400, Li-Cor, Lincoln, NE). Calculations of gas exchange (net assimilation rate, stomatal conductance, transpiration and CO 2 concentration in the sub-stomatal space) were performed according to von Caemmerer and Farquhar (1981). The measurements were carried out on four replicate plants in a healthy, green, recently expanded third or fourth leaf in the canopy in each treatment at about 4 months after planting. For each leaf, light response curves (A n -Q) and the photosynthetic response to carbon dioxide concentrations (A n -C i ) were carried out to determine important parameters related to leaf physiology. Leaves were exposed to high irradiance and ambient CO 2 concentration for at least 15 min before starting A n -C i curves. Twelve measurements were taken (C a =50 to 1200 µmol mol -1 CO 2 ) for each A n -C i curve. The value of photosynthetic photon flux density (PPFD) was set at 1500 μmol m -2 s -1 for the complete A n -C i curve. On the same leaf, an A n -Q response curve performed at high CO 2 (C a =1000 µmol mol -1 ) was completed. For each A n -Q-response curve, 11 measurements were taken (PPFD=0 to 2000 µmol m -2 s -1 ). For A n -C i and A n -Q responses, leaf temperature and vapor pressure deficit in the leaf chamber were maintained at 25±0.2 C and 1±0.1 kpa, respectively. In all cases, a 4-day minimum interval was allowed between two successive observations (i.e., A n -C i or A n -Q curves) on the same leaf to avoid carry-over effects resulting from measurements. Data Analysis The most frequently used method for understanding how C3 photosynthesis responds to perturbations is the Farquhar-von Caemmerer-Berry biochemical model of net photosynthesis (FvCB model). The simplest form of the FvCB model summarizes the dependence of the net photosynthesis (A n ) on the intercellular CO 2 concentration (C i ) as determined by saturation of ribulose 1 5-bisphosphate carboxylase/oxygenase (Rubisco) with respect to carboxylation (A c ) and electron transport as limited by ribulose bisphosphate (RuBP) regeneration (A j ) (Farquhar et al., 1980; von Caemmerer and Farquhar, 1981). The most common purpose of the A n -C i curve is to estimate in vivo the apparent Rubisco activity (maximum carboxylation rate V cmax ), the maximum rate of electron transport used in the regeneration of RuBP (J max ) and the day (nonphotorespiratory) respiration rate (R d ) under ambient conditions. The parameters V cmax, J max and R d were estimated using regression analysis of the 72

3 curves based on the equations presented by Dubois et al. (2007). This step was carried out by fitting the equations of the FvCB model (Bernacchi et al., 2003) of each curve using the non-linear regression routine with Gaussian algorithm in SAS (SAS Institute Inc., Cary, NC, USA). The measured photosynthetic compensation point ( measured) which is the CO 2 concentration at which the respiratory efflux of CO 2 equals the rate of photosynthetic CO 2 uptake, was estimated from each A-C i curve by linear regression for the five lowest C i values ( µmol mol -1 CO 2 ); at the same time the C i transition (µmol mol -1 ) from A c to A j was estimated following the procedure of (Dubois et al., 2007). The apparent efficiency of light energy conversion (mol electrons per mol photons, ) was estimated for each individual A n -Q curve, also by non-linear regression routine with Gaussian algorithm in SAS. Thereafter an ANOVA-F-test was used to determine whether the irradiance treatments affected the leaf photosynthetic parameters. RESULTS Carbon Dioxide Response The response of net photosynthesis (A n ) to intercellular carbon dioxide concentration (C i ) for banana Gros Michel leaves, examined at an irradiation of 1,500 μmol m -2 s -1 and leaf temperature 25 C, followed typical A n -C i response patterns of C 3 plants. In all natural shade treatments, the net photosynthesis (A n ) increased with increasing intercellular CO 2 up to the concentration of 650 µmol mol -1 (Fig. 1a) with no significant differences in the measured CO 2 compensation point ( measured) or in the value of C i at the transition point between the rate of photosynthesis when Rubisco (ribulose 1 5-bisphosphate carboxylase/oxygenase) activity is limiting (A c ) and the rate of photosynthesis when ribulose-1,5-bisphosphate (RuBP)-regeneration is limiting by the electron transport (A j ) (Table 1). While for the maximum carboxylation rate (V cmax standardized to 25 C) there were no differences between 50, 75 and 100% of full sun this parameter was reduced significantly for the highest shade levels (Table 1). V cmax varied between 103(±5.6), 103(±14), 97(±7) and 69(±2) for 100, 75, 50 and 25% of full sun irradiance respectively. The maximum rate of electron transport used in the regeneration of RuBP (J max standardized to 25 C) presented significant differences among the irradiance treatments and varied from 162(±4), 133.5(±9), 124.1(±5) to 95.3(±7) for the 100, 75, 50 and 25% irradiance treatments respectively. The R d parameter for the A n /C i curve were statistically different and varied from 2.1(±0.43) to 0.9(±0.35) for 100 and 25% of full sun irradiance treatments, respectively. Light Response Regarding the leaf traits describing the photosynthesis acclimation to natural shade, the PPFD saturated rate of net photosynthesis (A sat ) was significantly modified with the irradiance treatments. A sat was lower in 25 and 50% full sun treatments compared with 75 and 100% sun (Fig. 1b; Table 1). A sat increased with the increase of the irradiance level by a factor of 1.6 between the 25% of irradiance compared to 75 and 100% irradiance (Table 1). PPFD at photosynthesis saturation (PPFD sat ), at 80% (PPFD 80 ) and 50% (PPFD 50 ) of saturation was significantly different among shading treatments, showing that, for all those parameters, there was no difference between the 75 and 100% irradiance and values for 50 and 25% irradiance treatments were significantly lower. The acclimation to shade did not influence the light compensation point of photosynthesis (Table 1). No saturation value was apparent for the photosynthetic photon flux density in full sun or the 75% treatment, while for the 25 and 50% treatments, the saturating photon flux density varied from µmol m -2 s -1. The apparent efficiency of light energy conversion (α) estimated from the light curves averaged 0.35, but ranged from 0.31(±0.02) to 0.40(±0.04) mol mol -1 (Table 1). The 25% treatment was significantly lower than the 50% full sun treatment, but the treatments with the most irradiance were not different from either, indicating there is no clear pattern of the shade effect on this parameter. 73

4 DISCUSSION In the present study, key parameters of the Farquhar-von Caemmerer-Berry (FvCB) biochemical model of photosynthesis (Farquhar et al., 1980; von Caemmerer and Farquhar, 1981) were estimated for Gros Michel under a natural light gradient. For banana plants grown at 100% irradiance, values of V cmax of 103.7(±6), J max of 162.5(±4) and R d 2.2(±0.4) µmol m -2 s -1 were obtained for leaves at the reference temperature (25 C). However, care must be taken when comparing these values with other studies because the estimation of these values is dependent on the Rubisco kinetic parameters and temperature dependent functions (Bernacchi et al., 2001). In a review of V cmax and J max by Wullschleger (1993) for 109 species estimated from the A/C i curves, no parameters were included for Musa spp. Our values of V cmax and J max for Gros Michel are in the range of the Wullschleger s values for monocotyledonous crops, but are above average values suggesting a high photosynthetic capacity of banana plants. However, our estimates for V cmax, J max and R d are lower than the values presented in Turner et al. (2007) derived from the original work of Schaffer et al. (1996) in growth chambers. Additional and independent measurements of A n -C i response curves on Gros Michel (AAA) and FHIA-17 (Musa AAAA) presented maximum values of 145 μmol m -2 s -1 and 190 μmol m -2 s -1 for V cmax and J max respectively at leaf temperatures of 29 C (Bustamante et al., 2011). The parameters presented by Turner et al. (2007) range from 539 to 1,249 μmol m -2 s -1 for V cmax and 252 to 296 μmol m -2 s -1 for J max. These values are higher than the maximum values for all crops reported by Wullschleger (1993) (V cmax range 29 to 194, J max range 29 to 372, with a mean ratio J max :V max of 1.6). Additionally, the A-C i response curve in our study showed that A n increased with C i up to 600, but did not vary systematically between 600 to 1100 μmol mol -1. In the treatments of root restriction (container volume, 20 or 200 L) and ambient CO 2 concentration reported by Schaffer et al. (1996), A n increased from 0 to a maximum of 70 μmol m -2 s -1 between 1500 and 2,000 μmol mol -1 C a. In our study, high values of A n were not observed perhaps because the highest C i values (1200 μmol mol -1 ) were too low. There is, however, no ready explanation for why A n presented a saturation at lower values (600 μmol mol -1 ), but increased steadily from 600 to 2000 μmol mol -1 in the Schaffer et al (1996) study. Additional studies are required to establish the range values of V cmax and J max for the Gros Michel cultivar and controlling factors. The three key parameters of the photosynthesis model (V cmax, J max and R d ) changed with the growth irradiance levels, thus representing an acclimation of the photosynthetic apparatus to shade. Several species exhibit remarkable acclimation and adaptability of leaf photosynthetic capacity to light during expansion and growth (Evans and Poorter, 2001; Williams et al., 1989). In our study of banana leaves, J max, V cmax and R d were higher in leaves adapted to full sun than in those adapted to shade. J max increased linearly with increasing irradiance, while for V cmax and R d the increment was not linear, nor were the changes in LMA (leaf mass:area ratio) (data not shown). For several species, LMA varies according to the light environment and is correlated with differences in leaf photosynthetic characteristics within the tree canopy (Frak et al., 2001; Le Roux et al., 1999). Although for our whole data set, there was a relationship for V cmax and J max (r 2 =0.63), plants in the full sun treatment presented a higher J max /V cmax ratio, indicating that plants under high irradiance invest more resources in the light harvesting process compared with the enzymatic process. Photosynthesis under field conditions is commonly Rubisco-limited. Therefore, leaf V cmax is more important in driving leaf photosynthesis under conditions where stomatal conductance could be limited. CONCLUSIONS In this study, we estimated the parameters of a biochemical model of photosynthesis for Gros Michel banana leaves. Our data suggest that there is a shade effect on photosynthetic capacity of the leaves, since the maximum carboxylation rate (V cmax ), maximum rate of electron transport (J max ) and day respiration (R d ) are lower in plants growing under natural shade. These changes in photosynthetic parameters were 74

5 related to changes of simple leaf traits as LMA, but also could be related to changes in total leaf nitrogen as well as changes in resources (mainly nitrogen) partitioning between the light harvesting process or the carboxylation process. It is expected, that instantaneous leaf photosynthesis rate of banana in agroforestry systems will be driven by the changes in the microclimatic conditions surrounding the leaf (especially light availability, temperature and vapor pressure deficit) but also by the intrinsic adaptations of the leaf photosynthetic capacity during leaf construction. Thus, leaves developed at low light and exposed to full irradiance conditions will present lower photosynthetic rate than leaves developed at high light conditions which remain in high light. In general, these results could be considered the first step toward the estimation of the banana potential photosynthesis under agroforestry systems. The effects of leaf acclimation to shade in combination with leaf stomatal conductance provide the basis for a coupled gas exchange model. Such a model can be used further as a module in a crop simulation model to explore optimization strategies for productivity of banana in agroforestry systems under different environmental conditions. Literature Cited Barradas, V.L. and Fanjul, L Microclimatic characterization of shaded and opengrown coffee (Coffea arabica L.) plantations in Mexico. Agricultural and Forest Meteorology 38: Bernacchi, C., Pimentel, C. and Long, S In vivo temperature response functions of parameters required to model RuBP limited photosynthesis. Plant, Cell & Environment 26: Bernacchi, C., Singsaas, E., Pimentel, C., Portis Jr., A. and Long, S Improved temperature response functions for models of Rubisco limited photosynthesis. Plant, Cell & Environment 24: Dold, C., Pocasangre, L. and Staver, C Bananas with trees: updating the research and development agenda to contribute to small holder income generation and food security and to biodiversity conservation. 2 nd International Symposium on Multi-strata Agroforestry Systems with Perennial Crops. Turrialba, Costa Rica, September. 5p. Dubois, J.J.B., Fiscus, E.L., Booker, F.L., Flowers, M.D. and Reid, C.D Optimizing the statistical estimation of the parameters of the Farquhar-von Caemmerer-Berry model of photosynthesis. New Phytologist 176: Evans, J. and Poorter, H Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment 24: Farquhar, G.D., Caemmerer, S. and Berry, J A biochemical model of photosynthetic CO 2 assimilation in leaves of C 3 species. Planta 149: Frak, E., Le Roux, X., Millard, P., Dreyer, E., Jaouen, G., Saint Joanis, B. and Wendler, R Changes in total leaf nitrogen and partitioning of leaf nitrogen drive photosynthetic acclimation to light in fully developed walnut leaves. Plant, Cell & Environment 24: Haggar, J., Schibli, C. and Staver, C Como manejar arboles de sombra en cafetales? Agroforestería en las Américas 8: Le Roux, X., Grand, S., Dreyer, E. and Daudet, F.A Parameterization and testing of a biochemically based photosynthesis model for walnut (Juglans regia) trees and seedlings. Tree Physiology 19: Norgrove, L Musa in multi-strata systems - focus on shade. InfoMusa 7: Schaffer, B., Searle, C., Whiley, A. and Nissen, R Effects of atmospheric CO 2 enrichment and root restriction on leaf gas exchange and growth of banana (Musa). Physiologia Plantarum 97: Schibli, C Percepciones de familias productoras sobre el uso y manejo de sistemas agroforestales con café en el norte de Nicaragua. Agroforestería en las Américas 8:

6 Siles, P., Bustamante, O., Deras, M., Matute, O., Aguilar, C., Rojas, J., Castellon, J., Burkhardt, J. and Staver, C. 2010a. Bananos en cafetales con árboles en América Latina: Estrategias preliminares para mejorar su productividad, rentabilidad y sostenibiliad. XIX Reunión Internacional ACORBAT, Medellin, Colombia, 8-12 Noviembre p Siles, P., Harmand, J.M. and Vaast, P. 2010b. Effects of Inga densiflora on the microclimate of coffee (Coffea arabica L.) and overall biomass under optimal growing conditions in Costa Rica. Agroforestry Systems 78: Siles, P. and Vaast, P Comportamiento fisiológico del café asociado con Eucalyptus deglupta, Terminalia ivorensis o sin sombra. Physiological response of coffee associated with Eucalyptus deglupta, Terminalia ivorensis or without shade. Agroforestería en las Américas (CATIE) 9: Turner, D. 1998a. Ecophysiology of bananas: the generation and functioning of the leaf canopy. Acta Hort. 490: Turner, D. 1998b. The impact of environmental factors on the development and productivity of bananas and plantains. Proceedings of the XIII ACORBAT meeting, Guayaquil, Ecuador, November p Turner, D.W., Fortescue, J.A. and Thomas, D.S Environmental physiology of the bananas (Musa spp.). Brazilian Journal of Plant Physiology 19: von Caemmerer, S. and Farquhar, G Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: Williams, K., Field, C.B. and Mooney, H.A Relationships among leaf construction cost, leaf longevity, and light environment in rain-forest plants of the genus Piper. American Naturalist 133: Wullschleger, S.D Biochemical limitations to carbon assimilation in C3 plants - a retrospective analysis of the A/Ci curves from 109 species. Journal of Experimental Botany 44:907. Tables Table 1. Effect of growth irradiance on the parameter of the photosynthesis sub-model. Parameter Growth irradiance treatment 25% 50% 75% 100% measured (µmol mol -1 ) 50 ns 47 ns 50 ns 54 ns C i transition (μmol mol -1 ) 313 ns 286 ns 307 ns 365 ns V cmax (μmol m -2 s -1 ) 68.9 b 97.5 a a a J max (μmol m -2 s -1 ) 95.3 d c b a R d (μmol m -2 s -1 ) 0.9 b 0.8 b 1.5 ab 2.2 a J max /V cmax A sat (μmol m -2 s -1 ) 26.0 c 33.8 b 42.2 a 41.6 a PPFD comp (μmol m -2 s -1 ) 18 ns 11 ns 14 ns 4 ns PPFD 50 (μmol m -2 s -1 ) 232 b 257 ab 344 a 335 a PPFD 80 (μmol m -2 s -1 ) 639 b 704 ab 878 a 908 a PPFD sat (μmol m -2 s -1 ) 1565 b 1800 ab 1936 a 2234 a 0.31 b 0.40 a 0.36 ab 0.34 ab Means followed by different letters in the same row indicate significant differences, Duncan, P<0.05, n=4. 76

7 Figures (a) 40 A n ( mol m -2 s -1 ) % Light 75% Light 50% Light 25% Light C i ( mol mol -1 ) 40 (b) A n ( mol m -2 s -1 ) % Light 75% Light 50% Light 25% Light PPFD ( mol m -2 s -1 ) Fig. 1. Response of net photosynthesis to intercellular CO 2 concentration (a) and photosynthetically active photon flux density (b) for banana Gros Michel (AAA, Gros Michel subgroup) under a gradient of natural shade. Each point represents the average of four plants (one leaf per plant). Vertical bars are standard errors. 77

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