J Plant Res (2010) 123:371–379 DOI 10.1007/s10265-009-0279-8
REGULAR PAPER
Effect of nitrogen nutrition on the carbohydrate repression of photosynthesis in leaves of Phaseolus vulgaris L. Takao Araya • Ko Noguchi • Ichiro Terashima
Received: 29 July 2009 / Accepted: 18 October 2009 / Published online: 2 December 2009 Ó The Botanical Society of Japan and Springer 2009
Abstract When carbohydrates accumulate in leaves, photosynthesis is repressed. Limited nitrogen nutrition is thought to enhance this repressing effect. However, the interaction between carbohydrate and nitrogen limitation in leaf photosynthesis has not been examined intensively. In this study, we grew Phaseolus vulgaris L. plants at three different nitrogen levels, and examined the effects of sucrose feeding to the roots on the nitrogen content, carbohydrate content and photosynthetic properties of the primary leaves. Nitrogen content and photosynthetic rate were lower and the carbohydrate content was greater in
Electronic supplementary material The online version of this article (doi:10.1007/s10265-009-0279-8) contains supplementary material, which is available to authorized users. T. Araya K. Noguchi I. Terashima Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan e-mail:
[email protected] I. Terashima e-mail:
[email protected] T. Araya Department of Biological Sciences, Graduate School of Science, Osaka University, 1-1 Machikaneyama-cho, Toyonaka 560-0043, Japan Present Address: T. Araya (&) Metabolic Function Research Group, Plant Nutrition and Basal Metabolism Research Team, Riken PSC, 641-12 Maioka, Totsuka-ku, Yokohama 244-0813, Japan e-mail:
[email protected]
plants grown with limited nitrogen than in well-fertilized plants. Sucrose feeding to the plants increased carbohydrate content and decreased photosynthetic rate and nitrogen content. The increase in carbohydrate content and the decreases in nitrogen content and photosynthetic rate occurred at the same time, and the negative relationship between the carbohydrate content and photosynthetic rate did not differ among nitrogen nutrition levels. These results show that carbohydrate accumulation in the leaves leads to a decrease in photosynthetic rate. At low nitrogen nutrition levels, carbohydrates accumulated markedly, which accelerated this effect. It appears that the nitrogen nutrition level influences leaf photosynthesis through changing the carbohydrate level rather than through modifying sensitivity of the leaf to the carbohydrate level. Keywords A–Ci curve Bean (Phaseolus vulgaris L.) Carbohydrate Carbohydrate repression of photosynthesis Nitrogen Photosynthesis Abbreviations A360 Photosynthetic rate at PPFD of 1,000 lmol m-2 s-1 and CO2 concentration of 360 lL L-1 Amax Photosynthetic rate at PPFD of 1,000 lmol m-2 s-1 and CO2 concentration of 1,500 lL L-1 Ci CO2 concentration in the intercellular space PPFD Photosynthetic photon flux density Rubisco Ribulose-1,5-bisphosphate carboxylase/ oxygenase RuBP Ribulose-1,5-bisphosphate TNC Total nonstructural carbohydrates
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Introduction In leaves that accumulate carbohydrates, expression of photosynthetic genes such as Rubisco small subunit (RBCS) and the light harvesting complex of PSII (LHCB) is repressed (Sheen 1990; Krapp and Stitt 1995; Koch 1996; Ono et al. 2001; Tholen et al. 2007). Accumulation of carbohydrates in leaves also accelerates the decline in the photosynthetic capacity and senescence (Wingler et al. 1998; Yoshida 2003; Parrott et al. 2005). These effects of carbohydrate accumulation on photosynthesis are argued to be enhanced in nitrogen deficient plants (Paul and Driscoll 1997). For example, sugar feeding to the roots of Arabidopsis thaliana induced a decrease in the maximum quantum yield of PSII (Fv/Fm) in the leaves in nitrogen deficient plants, while a decrease was not observed in plants grown with sufficient nitrogen (Wingler et al. 2004, 2006). Furthermore, a senescenceassociated gene, SAG12, was induced by sugar feeding only in nitrogen deficient A. thaliana plants (Pourtau et al. 2006). Based on similar experimental results with Phaseolus vulgaris L., Ono and Watanabe (1997) proposed that low nitrogen nutrition decreases photosynthetic activities via enhancing carbohydrate accumulation in the leaves. These studies all suggest that the effect of nitrogen deficiency and carbohydrate accumulation are closely linked. However, it has been unclear whether low nitrogen nutrition really enhances carbohydrate effects on photosynthesis, or enhances carbohydrate accumulation of leaves. It has been postulated that glucose is a signaling molecule (Sheen 1990). Accumulation of glucose has been shown to suppress expression of photosynthetic genes and induce leaf senescence—both via the signaling pathway involving hexokinase (Jang and Sheen 1997; Dai et al. 1999). However, in our previous study, repression of photosynthesis occurred mainly in leaves that had accumulated starch (Araya et al. 2006). Starch per se is not metabolically active, and thus it is unlikely that starch itself is involved in repressing photosynthetic genes. Although hexokinase is a probable sensor for sugar repression of photosynthesis, the roles of carbohydrate species other than glucose in the repression of photosynthesis still need to be examined. Because limited nitrogen nutrition induces carbohydrate accumulation in leaves, growing plants under various nitrogen nutrition levels may lead to increased variation in the carbohydrate content of the leaves. The purpose of this study was to examine the effect of nitrogen nutrition on carbohydrate repression of photosynthesis. In addition, we paid particular attention to the question of which carbohydrate species exerted the repressive effects on photosynthesis. To elucidate the
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relationship between carbohydrate species, nitrogen and photosynthesis, we conducted several regression analyses. To increase the carbohydrate content of the primary leaves, we fed 20 mM sucrose solution for 5 days to the roots of bean plants grown with nutrient solution containing 0, 0.72 or 6 mM NO3– as described previously (Araya et al. 2006), and measured the photosynthetic rates, and carbohydrate and nitrogen contents in the primary leaves.
Materials and methods Plant material Seeds of common bean (Phaseolus vulgaris L. cv. Yamashiro-Kurosando) were placed on wet paper on day 0. On day 4, germinated seedlings were planted in 12.7 cm diameter pots filled with vermiculite. Plants were grown in an environment-controlled room at a photosynthetic photon flux density (PPFD) of 300 lmol photons m-2 s-1 with a light period of 14 h (0600–2000 hours), at 25°C. From day 7 onwards, the plants were fertilized every day with 50 ml half-strength Hoagland’s solution (2 mM K?, 2 mM Ca2?, 0.75 mM MgSO4, 0.665 mM NaHPO4, 25 lM Fe-EDTA, 5 lM ZnSO4, 0.5 lM CuSO4, 0.25 lM NaMoO4, 50 lM NaCl, and 0.1 lM CoSO4) that contained 0, 0.72 or 6 mM nitrate. The plants were thus referred to as ‘‘0 mM N’’, ‘‘0.72 mM N’’ and ‘‘6 mM N’’ plants, respectively. The NO3- of the 0 and 0.72 mM Hoagland’s solutions was replaced by Cl-. Sugar treatment To increase the carbohydrate content of the primary leaves, we supplied 50 ml 20 mM sucrose solution to the bean roots every day for 5 days from day 15 as described previously (Araya et al. 2006). After sugar treatment for 5 days, we measured various photosynthetic properties of the primary leaves; the measurements were, therefore, conducted on day 20. Plants fed only water and nutrient solution are referred to as ‘control’ plants. After gasexchange measurements, leaf discs with a diameter of 1 cm were sampled at 1500–1800 hours and quickly frozen in liquid nitrogen for measuring carbohydrate contents. Five leaf discs were dried at 80°C for a week for the measurement of carbon and nitrogen contents. Photosynthetic rate The photosynthetic rate was measured with a portable infrared CO2 gas analyzer (LI-6400, Li-Cor, Lincoln, NE)
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as described previously (Araya et al. 2006). The slope of the A–Ci curve in the range of Ci (CO2 concentration in the intercellular space) below 150 lL L-1 was calculated by the least squares regression method and regarded as the initial slope of the A–Ci curve. The initial slope of the A–Ci curve was thought to reflect the ribulose-1,5-bisphosphate (RuBP) carboxylation capacity, and the maximum photosynthetic rate (Amax), the rate of photosynthesis at 1,000 lmol photon m-2 s-1 and CO2 concentration of 1,500 lL L-1, was regarded to represent the RuBP regeneration capacity (von Caemmerer and Farquhar 1981). Nitrogen and carbon contents Samples (2–5 mg) of dried leaf discs were wrapped in tin foil, and the nitrogen and carbon contents were analyzed with an NC analyzer (Vario EL III, Elementar Analysensysteme, Hanau, Germany). Acetoanilide was used as a standard. Non-structural carbohydrates Non-structural carbohydrates of leaves were measured as described previously (Araya et al. 2006). Two frozen leaf discs were ground to a powder in liquid nitrogen and suspended in 1 ml 80% ethanol. The suspension was incubated at 80°C for 1 h and centrifuged at 15,000 g for 10 min. The supernatant was used for estimation of glucose and sucrose, and the pellet for starch. Distilled water (600 ll) was added to the pellet and mixed well. The mixture was incubated at 95°C for an hour to denature starch, then mixed with the same volume of 35 unit/ml amyloglucosidase. The mixture was incubated at 55°C for an hour to hydrolyze starch into glucose. The glucose concentration was estimated with a glucose assay kit (Glucose-CII-test Wako, Wako Pure Chemical Industries, Osaka, Japan). The supernatant was evaporated to remove ethanol with a centrifugal concentrator (CC-105, Tomy Seiko, Tokyo, Japan). The same volumes of distilled water and chloroform were added to the concentrated supernatant and mixed well. The mixture was centrifuged at 15,000 g for 10 min and the supernatant was transferred to a 1.5 ml microtube. The upper clear phase was used for the estimation of glucose and sucrose. A part of the supernatant was mixed with the same volume of invertase solution (Wako Pure Chemical Industries, Osaka, Japan) and mixture was incubated at 27°C for 1 h to hydrolyze sucrose into fructose and glucose. The glucose concentration was estimated with a glucose assay kit. The glucose assay kit cannot determine fructose. However, in bean leaves, fructose is minor sugar species, and
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the glucose content of leaves is much higher than fructose content (Castrillo 1992). Thus, we did not measure fructose. Statistical analyses The effects of sugar-treatment and nitrogen fertilization were analyzed with two-way analysis of variance (ANOVA). The results of two-way ANOVA are shown in Supplementary Table S1. The P value for the sugar-treatment is shown above the column in the figures when the difference between sugar-treated and control leaves is significant. In addition, significant differences (P \ 0.05) among the different nitrogen levels were calculated with Tukey’s multiple comparison test, and are indicated with different letters in Table S1. Differences of slopes of regression lines among nitrogen levels were analyzed with analysis of co-variance (ANCOVA). To estimate the contribution of carbohydrate species to photosynthetic parameters, we also conducted multiple regression analysis. The results are shown in Supplementary Table S2. The number of samples was as follows: 0 mM control, n = 4; 0 mM suc, n = 4; 0.72 mM control, n = 4; 0.72 mM suc, n = 4; 6 mM control; n = 10; 6 mM suc, n = 9.
Results Carbohydrates Glucose content of the 0 mM N leaves was significantly higher than that of 0.72 and 6 mM N leaves; sugar treatment significantly increased the glucose content. Nitrogen nutrition did not affect sucrose content (Fig. 1a), whereas sugar treatment increased the sucrose content. The sugar treatment increased the starch content (Fig. 1c); the starch contents in the 0 and 0.72 mM N leaves were higher than that in the 6 mM N leaves. Nitrogen and carbon contents Nitrogen content of the 6 mM N control leaves was higher than those of the other treatments (Fig. 2a). Sugar treatment decreased nitrogen content in the 0.72 and 6 mM N leaves. Carbon content was lower in the 6 mM N leaves than in the 0 mM N leaves (Fig. 2b). Sugar treatment increased the carbon content. Carbon/nitrogen (C/N) ratios were higher in the 0 and 0.72 mM N leaves than those of the 6 mM N leaves. Sugar treatment significantly increased the C/N ratio. We also examined the relationships between nitrogen content and total nonstructural carbohydrate (TNC) content
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Fig. 1 Carbohydrate content on a leaf area basis. a Glucose; b sucrose; and c starch. Error bars SE [n = 4, except for 6 mM control (n = 10) and 6 mM suc (n = 9)]. The P values above the columns indicate significant differences between control and sugartreated leaves with two-way ANOVA. Different lower case letters indicate a significant difference between nitrogen levels according to Tukey’s multiple test (P \ 0.05)
(the sum of glucose, sucrose and starch content, Fig. 3). There was a strong negative correlation between nitrogen content and TNC (r = -0.697, P \ 0.001).
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Fig. 2 Nitrogen and carbon content on a leaf area basis. a Nitrogen content; b carbon content; and c carbon/nitrogen (C/N) ratio. Error bars SE [n = 4, except for 6 mM control (n = 10) and 6 mM suc (n = 9)]. The P values and lower case letters are explained in Fig. 1
Photosynthesis Photosynthetic rates measured at a PPFD of 1,000 lmol m-2 s-1 and at 360 lL L-1 CO2 (A360), which reflect photosynthetic capacity at saturating light, are
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Fig. 3 Correlation between total carbohydrate content (TNC) and nitrogen content of leaves. Pearson’s correlation coefficient between nitrogen content and TNC was -0.697 (P \ 0.001)
shown in Fig. 4a. A360 of the 0 and 0.72 mM N leaves was lower than that of the 6 mM N leaves. Sugar treatment decreased the A360. We also measured A–Ci curves to estimate RuBP carboxylation and regeneration capacities separately. The initial slope of the A–Ci curve, which reflects the RuBP carboxylation capacity, showed a trend similar to that of A360, with the lower nitrogen or sugar treatment having the lower initial slope (Fig. 4b). The rate of photosynthesis at 1,000 lmol photon m-2 s-1 and 1,500 lL L-1 ambient CO2 (Amax), which reflects the RuBP regeneration capacity, of the 0 and 0.72 mM N leaves was lower than that of the 6 mM N leaves, and sugar treatment significantly decreased Amax.
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Regression analysis between photosynthesis and carbohydrates To clarify which of the carbohydrate species exerted the repressive effect on photosynthesis, we analyzed the relationships between the photosynthetic parameters and carbohydrates (Fig. 5). Firstly, we examined the dependency of A360 on each carbohydrate species, and compared the slopes of regression lines between nitrogen nutrition levels (Fig. 5). Irrespective of the carbohydrate species, there were no significant differences in the slopes of the regression lines between the nitrogen levels (ANCOVA, P [ 0.05). We also conducted similar analyses on the other photosynthetic parameters, the initial slopes of A–Ci curve and Amax. These parameters showed results similar to those of A360 (data not shown).
Fig. 4 Changes in photosynthetic rate on a leaf area basis. a Photosynthetic rate at a photosynthetic photon flux density (PPFD) of 1,000 lmol m-2 s-1 and CO2 concentration of 360 lL L-1 (A360). b Initial slope of the regression line of the A–Ci curve. c Photosynthetic rate at PPFD of 1,000 lmol m-2 s-1 and CO2 concentration of 1,500 lL L-1 (Amax). Error bars SE [n = 4, except for 6 mM control (n = 10) and 6 mM suc (n = 9)]. The P values and lower case letters are explained in Fig. 1
Next, we analyzed the relative contribution of the effect of each carbohydrate species on A360 using multiple regression analysis between A360 and the carbohydrates. The multiple coefficient of determination between A360 and carbohydrates was 0.630 (P \ 0.001, Table S1). The absolute value of the standardized partial regression coefficient of starch (-0.660, P \ 0.001) was much higher than
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those of sucrose (-0.0113, P = 0.931) and glucose (-0.234, P = 0.110). The same analyses were conducted for data of the initial slope of A–Ci curve and Amax (Supplementary Table S2). The results of multiple regression analyses with initial slope of A–Ci curve and Amax showed trends similar to that of A360. We also conducted regression analysis between photosynthetic parameters and nitrogen content or C/N ratio of the leaves (Fig. 6). There was a significant linear relationship between A360 and nitrogen content (coefficient of determination: R2 = 0.541, Fig. 6a). C/N ratio was also well correlated with A360 (R2 = 0.736, Fig. 6b). Discussion
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In this study, we examined the effects of nitrogen nutrition and carbohydrate accumulation on photosynthesis. Both low nitrogen nutrition and sugar treatment induced carbohydrate accumulation and decreased the photosynthetic rate. There were strong negative relationships between several photosynthetic parameters and the starch content. If, as has been suggested (Stitt and Krapp 1999; Wingler et al. 2006; Pourtau et al. 2006), nitrogen limitation enhances the carbohydrate effect on photosynthesis, the slope of the regression line between carbohydrate content and photosynthetic rate would change depending on the nitrogen nutrition level as shown in Fig. 7a. However, the slopes of the regression lines between photosynthetic parameters and the starch content (Fig. 5) appear to be independent of the level of nitrogen nutrition, and more similar to the pattern drawn in Fig. 7b. This analysis indicates that the effects of nitrogen nutrition level on the carbohydrate repression of photosynthesis may be related to the carbohydrate content, rather than to sensitivity to carbohydrates, at least within the time-range of the present study. Glucose derived from starch metabolism plays a crucial role in repression of photosynthesis by carbohydrate accumulation in leaves
Fig. 5 Relationships between photosynthesis and carbohydrate content of leaves. a Regression between A360 and glucose content. b Regression between A360 and sucrose content. c Regression between A360 and starch content. Solid, broken, and dotted lines are regression lines of 0, 0.72 and 6 mM leaves, respectively. The functions of the regression lines are shown in Supplementary Table S3
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Photosynthetic parameters, especially the initial slope of the A–Ci curve, were strongly related to starch content of the leaves (Fig. 5). Because starch is not physiologically active, it seems unlikely that starch per se directly affects Rubisco gene expression. Moore et al. (1998) suggested that ‘‘sucrose cycling’’ occurs in leaves that accumulate starch, and this may be responsible for the repression of photosynthetic genes. However, there are only a few reports that indicate the occurrence of sucrose cycling in vivo. This idea suggests that carbohydrate metabolism at night plays an important role in sugar repression of
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Fig. 6 Relationship between A360 and nitrogen content of leaves. a Regression between A360 and nitrogen content. b Regression between A360 and carbon/nitrogen (C/N) ratio. Symbols and lines as in Fig. 5. The functions of the regression lines are shown in Supplementary Table S3
photosynthetic genes in starch-accumulating plants (Paul and Foyer 2001). Stitt and Krapp (1999) also suggested that not only the hexose content but hexose metabolism controls sugar signaling. These studies suggest that the accumulation of carbohydrates does not directly affect gene expression of photosynthetic components, but that the metabolic fluxes of carbohydrates during the night period may act as an important signal in plants. Relationships between the metabolic flux of carbohydrates and the expression of photosynthetic genes should be studied to further elucidate essential steps in the carbohydrate repression of photosynthesis.
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Relationships between nitrogen, carbohydrate and photosynthesis There were strong linear relationships between carbohydrate content and photosynthetic parameters (Fig. 5). Goldschmidt and Huber (1992) showed similar results. We also found strong linear relationships between the nitrogen content and photosynthetic parameters of the primary leaves (Fig. 6); similar relationships have been reported for various plants (see Evans 1989). There was a strong negative correlation between nitrogen and the carbohydrate content of the leaves (Fig. 3). These results show that low nitrogen, high carbohydrate content and low photosynthetic capacity are closely linked. Many studies have examined the effects of the carbohydrate or nitrogen content of leaves on photosynthetic activity. However, the relationship between carbohydrate and nitrogen content is complicated and has not been sufficiently examined. Because sugar treatment decreased nitrogen content (Fig. 2a), it may indicate that carbohydrate accumulation represses de novo synthesis of Rubisco and other components, leading to a decrease in nitrogen content and leaf senescence (Sheen 1990; Krapp et al. 1993; Dai et al. 1999; Miller et al. 2000; Yoshida 2003; Parrott et al. 2005). On the other hand, limited nitrogen nutrition induced carbohydrate accumulation in leaves (Fig. 1). When nitrogen nutrition is insufficient, the sink size of the plant remains small because plant growth is restricted. Under these conditions, only small amounts of carbohydrates are translocated from the leaves, and thus carbohydrates accumulate in the leaves. The sink/source balance of the whole plant changes depending on plant developmental stage and/or on nitrogen nutrition levels, as reflected in the carbohydrate level in mature leaves (Ono et al. 2001). These results indicate that limited nitrogen increases the carbohydrate content and decreases the photosynthetic activity of the leaves. Based on these results, we propose a model for a positive feedback mechanism between the low carbon and high nitrogen level of a leaf. Low nitrogen nutrition accelerates carbohydrate accumulation, and a high carbohydrate accumulation in the leaves decreases photosynthetic proteins including Rubisco, leading to a further decrease in leaf nitrogen and photosynthetic capacity. Via these mechanisms, the C/N ratio of the leaves is increased. The high C/N ratio represses photosynthetic activity (Paul and Driscoll 1997; Martin et al. 2002; Wingler et al. 2006), and induces leaf senescence. On the other hand, when the leaf has high nitrogen and low carbohydrate (low C/N ratio), the photosynthetic activity of the leaves is maintained, and senescence of the leaves is repressed. If some environmental disturbance, such as drought, cold stress or limited nitrogen nutrition (Everard et al. 1994; Savitch and
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high N
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Fig. 7 Models of the relationship between carbohydrate content and photosynthesis at various levels of nitrogen nutrition: a limited nitrogen nutrition reinforces the negative effect of carbohydrates on photosynthesis; b limited nitrogen nutrition affects both carbohydrate content and photosynthesis. If nitrogen nutrition is limited, the slope of the regression line between carbohydrate content and photosynthesis
may decrease if the limited nitrogen condition reinforces the carbohydrate effects on photosynthesis (a). In this study, nitrogen nutrition did not affect the slope of the regression lines, suggesting that the limited nitrogen did not reinforce the carbohydrate effects. This suggests that carbohydrates accumulate under limited nitrogen availability and this is coupled to a decrease in photosynthesis (b)
Lorenzen 2001), affects the nitrogen or carbohydrate content of the leaves, the C/N ratio of the leaves is drastically increased, and senescence is induced. Such a mechanism may allow plants to respond quickly to changes in the environment by re-allocation of leaf nitrogen under unfavorable conditions.
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Acknowledgments This work was supported by the Sasagawa Scientific Research Grant from The Japan Science Society (No. 18220) and by the Ministry of Education, Science, Sports and Culture (No. 40211388). We thank Dr. D. Tholen, Ms. C. Boom and Dr. K. Ono for their helpful and invaluable advice.
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