Annals of Botany 89: 213-220, 2002
© 2002 Annals of Botany Company
Regulation of Rhizosphere Acidification by Photosynthetic Activity in Cowpea (Vigna unguiculata L. Walp.) Seedlings
1Laboratory of Crop Science, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464–8601, Japan
* For correspondence. Fax: +81 (0) 52 789 5558, e-mail tprao{at}agr.nagoya-u.ac.jp
Received 1 August 2001; Returned for revision 4 October 2001; Accepted 5 November 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In contrast to cereals or other crops, legumes are known to acidify the rhizosphere even when supplied with nitrates. This phenomenon has been attributed to N2 fixation allowing excess uptake of cations over anions; however, as we have found previously, the exposure of the shoot to illumination can cause rhizosphere acidification in the absence of N2 fixation in cowpea (Vigna unguiculata L. Walp). In this study, we examined whether the light-induced acidification can relate to photosynthetic activity and corresponding alterations in cation–anion uptake ratios. The changes of rhizosphere pH along the root axis were visualized using a pH indicator agar gel. The intensity of pH changes (alkalization/acidification) in the rhizosphere was expressed in proton fluxes, which were obtained by processing the images of the pH indicator agar gel. The uptake of cations and anions was measured in nutrient solution. The rhizosphere was alkalinized in the dark but acidified with exposure of the shoots to light. The extent of light-induced acidification was increased with leaf size and intensity of illumination on the shoot, and completely stopped with the application of photosynthesis inhibitor. Although the uptake of cations was significantly lower than that of anions, the rhizosphere was acidified by light exposure. Proton pump inhibitors N,N'-dicyclohexyl carbodimide and vanadate could not stop the light-induced acidification. The results indicate that light-induced acidification in cowpea seedlings is regulated by photosynthetic activity, but is not due to excess uptake of cations.
Key words: Acidification, agar gel, bromocresol purple, cation–anion uptake, Vigna unguiculata L. Walp, pH, photosynthesis, proton flux, proton pump inhibitors, rhizosphere.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Root-induced changes of pH in the rhizosphere have important consequences for plant nutrition (Marschner, 1995; Hinsinger, 1998). Some crop species, particularly legumes, take up significant amounts of sparingly soluble nutrients from the rhizosphere using their ability to acidify the rhizosphere (Aguilar and van Diest, 1981; Bekele et al., 1983; Hinsinger et al., 1993; Hinsinger and Gilkes, 1995).
Rhizosphere acidification by legume roots is largely attributed to the release of protons following excess uptake of cations over anions during N2 fixation (Israel and Jackson, 1982; Haynes, 1983; Lui et al., 1989). The legumes, therefore, are found to acidify their rhizosphere even when they are fed with nitrate (Marschner and Römheld, 1983). In a previous study, we have shown that seedlings of some legumes: cowpea (Vigna unguiculata L. Walp), chickpea (Cicer aritinum L. Millp) and adzuki bean [V. angularis (Willd)] fed with nitrate acidified their rhizosphere even without fixing N2 (Rao et al., 2000a). However, rhizosphere acidification was observed only with shoots exposed to light, and was localized in the middle portion of the taproot axis. With the shoot in darkness, the rhizosphere became alkaline all along the root axis. We therefore suggested that photosynthetic activity of the young legume plant might regulate rhizosphere acidification, probably via enhanced cation uptake under light conditions.
This study was conducted to explore the relationships between light-induced acidification in the cowpea and (1) photosynthetic activity and (2) cation–anion uptake ratios.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant culture
Cowpea (V. unguiculata L. Walp. cv. HAF-43) seedlings were grown for 1 week in seed-pack growth pouches (Vaughan’s Seed Company, Minneapolis, MN, USA) under controlled conditions in a growth chamber. The conditions in the growth chamber were maintained at 30/25 °C day/night temperature, 12 h photoperiod, 60 ± 5 % relative humidity and 150 µM m–2 s–1 light intensity provided by fluorescent tubes. During the growth period, one-quarter strength Hoagland nutrient solution (Johnson et al., 1957) containing nitrate at 10 mM concentration was supplied. The seedlings were not innoculated with rhizobium and the supply of high concentration of nitrate in growth medium did not allow the formation of nodules; therefore, the plants used in all experiments were non-nitrogen-fixing plants.
Visualization and quantification of pH changes
Changes of rhizosphere pH along the taproot axis were first visualized and then quantified into proton fluxes according to Rao et al. (2000b) by using pH indicator agar gel and image analysis. A 3-mm thick agar gel (9·0 g l–1) film containing bromocresol purple (0·1 g l–1) and nutrients (details are given in each experiment) was prepared. The cowpea seedlings were carefully removed from the growth pouches and the few laterals, found at the basal portion of the taproot, were cut to leave only the taproot. Next, the taproot of the cowpea seedlings was gently washed in 0·2 mM CaSO4 solution and then in de-ionized water for a few minutes. Subsequently, the taproot was pasted on the surface of the agar gel film in such a way that approx. three-quarters of the root surface was embedded in the gel. The initial pH of the agar gel was adjusted to 5·6. The agar gel films were covered with aluminum foil to avoid light access to the root. The agar gel films, together with the seedlings, were incubated for 6 h in a growth chamber at 30 °C temperature and 60 ± 5 % relative humidity. After 6 h incubation, the agar gel films were scanned using a scanner (EPSON GT-6000) with the settings at 90 d.p.i., full colour and brightness level 4. The digitized images were processed with image analysis to identify the pH gradient in the rhizosphere using a previously established pH versus colour density calibration. Then, the pH changes were transformed into apparent proton fluxes to quantify the degree of acidification/alkalization along the root axis (Rao et al., 2000b). The proton flux was calculated based on the difference between measured and initial pH (Versel and Pilet, 1986). The influx of protons (negative values) indicates alkalinization of the rhizosphere, whereas the efflux of protons (positive values) represents acidification.
Effect of photosynthesis on rhizosphere pH
The effect of photosynthesis on pH changes in the rhizosphere was studied in the following experiments in which only potassium nitrate at a concentration of 1 mM was added to the pH indicator agar gel. The photosynthetic activity in the following experiments was modulated with different sizes of leaf, light intensity on shoot or by the inhibition of photosynthesis.
Experiment 1: effect of illumination
The shoots of uniformly sized seedlings (Table 1) were exposed to either complete darkness or light (150 µM m–2 s–1) provided by fluorescent lamps. Plants were exposed to these conditions for 6 h.
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Experiment 2: effect of leaf area
Seedlings with large, normal and small leaf size but with similar root length (Table 1) were selected from plants grown under uniform conditions. These seedlings were exposed to light (150 µM m–2 s–1) provided by fluorescent lamps for 6 h.
Experiment 3: effect of light intensity
Seedlings of similar leaf size (Table 1) were exposed to various light intensities (45, 90 and 110 µM m–2 s–1) from a red LED lamp (EYELA, Tokyo, Japan). The exposure period was 6 h.
Experiment 4: effect of photosynthesis inhibition
The photosynthetic activity of the seedlings was inhibited during the incubation period by application of 3-(3,4-dichlorophenyl)-1,1-dimethyl urea (DCMU; Sigma Chemicals, St Louis, MO, USA) to the leaves. Prior to incubation the leaves of the seedlings were soaked in 5 mM DCMU solution for 1 h. In addition, DCMU solution was occasionally sprayed on leaves during the incubation period. Seedlings treated with DCMU and seedlings without treatment (control) were incubated under light (150 µM m–2 s–1) from fluorescent lamps for 6 h.
Each of the above experiments followed a completely randomized block design with four replicates. Each experiment was repeated twice. Data represent the means of all replicates. The intensity of pH changes along the root axis was expressed in apparent proton flux and plotted against relative root length. Relative root length has been used for better comparison as the root lengths were varied among the plants used in different experiments. Relative root length of each plant was calculated by considering their total root length from the root base to root tip as the value 1. The photosynthetic activity was measured on a single leaf at the beginning of each experiment for approx. 10 min by using a portable photosynthesis system (LI6200; Licor Inc., Lincoln, NB, USA) and was expressed on a leaf area basis.
Cation and anion uptake and rhizosphere pH
The pH changes and the uptake of cations and anions were studied in the following experiments with the supply of (a) all nutrients or (b) potassium nitrate alone. In the former case, the concentrations (mM) of major cations and anions were: K+ 1·50; Ca2+ 0·50; Mg2+ 0·50; NO3– 1·00; PO43– 0·50 and SO42– 1·00. The concentrations of the minor nutrients were similar to those in quarter strength Hoagland nutrient solution (Johnson et al., 1957). In the latter case, the concentration of both K+ and NO3– was 1 mM.
Experiment 5: rhizosphere pH in agar gel
The pH changes along the root axis in the above nutrient treatments (a and b) were measured using the pH indicator agar gel method (as described above). The cowpea seedlings of similar root length and leaf size (Table 1) were pasted onto the agar gel that contained the above nutrient treatments and incubated for 8 h in dark or light (150 ìM m–2 s–1). Each treatment had three replicates. The experiment was repeated twice. The data expressed in proton fluxes are the means of all (six) replicates.
Experiment 6: uptake rates in solution medium
The uptake rates of major cations and anions were measured in a separate experiment using solutions ‘a’ and ‘b’. The uniform seedlings (Table 1) were placed in a test tube (1·6 x 17·0 cm) filled with 27 ml of the above nutrient solution treatments and incubated for 10 h with the shoot in either darkness or light (150 µM m–2 s–1). For each nutrient treatment, two seedlings were placed in each test tube and replicated four times. The solution was aerated (free from CO2) throughout the incubation period. Uptake rates of major cations (K+, Ca2+ and Mg2+) and major anions (NO3–, PO43– and SO42–) were determined from the depletion of ions in the solution at the end of the incubation period. The concentrations of cations and anions in the solution were determined using an atomic absorption spectrophotometer (AA-6400; Shimadzu, Tokyo, Japan) and a liquid chromatograph (LC-10AD; Shimadzu), respectively. The uptake rates were expressed on the basis of root length. The initial and final pH values of the solution were determined using a pH meter (F-11; Horiba, Kyoto, Japan).
Experiment 7: effect of proton pump inhibition on rhizosphere acidification.
To confirm whether the light-induced acidification is due to proton release, the proton pump-inhibitors N,N'-dicyclohexyl carbodimide (DCCD) and vanadate, which are widely known as the inhibitors of plasmalemma ATPase activity (Alcantara et al., 1991; Yan et al., 1998) were applied. DCCD (Sigma Chemicals) and vanadate (Kanto Chemicals, Tokyo, Japan) at a concentration of 200 µM were supplied along with 1 mM nitrate in the agar gel medium. During the experiment, the light intensity on the shoot was 150 µM m–2 s–1. The incubation period was 6 h. Each treatment had six replicates and the experiment was conducted only once. The pH changes were quantified into proton fluxes as described above.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Effect of photosynthesis on rhizosphere pH
The visual pH changes (Fig. 1) were transformed into proton fluxes (Fig. 2A), showing alkalization (proton influx) of the rhizosphere along the whole root axis in dark, and a strong acidification (proton efflux) in only the middle portion of the root axis in light. Since the pH changes were observed beyond the root tip (Fig. 1), the values of proton fluxes, which were calculated from the visual data, have been exceeded beyond one when plotted against relative root length (Fig. 2). The light-induced acidification increased with increasing leaf size (Fig. 2B) and increasing light intensity from 90 to 110 µM m–2 s–1 (Fig. 2C). At a light intensity of 45 µM m–2 s–1, no rhizosphere acidification occurred (Fig. 2C). Light-induced acidification was also stopped when the photosynthesis inhibitor DCMU was applied to the leaves (Fig. 2D). Photosynthetic activity also decreased with decreasing light intensity (Table 1) and was completely inhibited by the application of DCMU on leaves (Table 1). Total proton flux, which was the value of cumulative proton flux of the whole rhizosphere, showed a strong positive relationship with the total photosynthetic activity (Fig. 3).
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Cation and anion uptake and rhizosphere pH
Irrespective of nutrient treatments either with supplies of all nutrients or only potassium nitrate, the rhizosphere was alkalinized along the whole root axis in the dark and acidified in the middle portion of the root axis in the light (Fig. 4).
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The uptake rates of major cations and anions, calculated from the concentration changes in the nutrient solution, are shown in Table 2. With all nutrients supplied, the uptake of major cations was lower than the uptake of major anions, in both dark and light conditions. However, the pH of the solution increased in the dark and decreased in light. Similarly, with the supply of only K+ and NO3–, the uptake rate of NO3– was greater than that of K+ in both dark and light conditions. However, the pH of the solution decreased in light.
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Effect of proton pump inhibition on rhizosphere acidification
The effect of proton pump inhibitors on rhizosphere acidification is shown in Fig. 5. The application of proton pump inhibitors did not stop the light-induced acidification. In comparison with control treatment, the intensity of light-induced acidification was the same with DCCD and slightly less with vanadate.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In our previous observations, some legumes were found to acidify the rhizosphere even in the nitrate-fed condition and in the absence of N2 fixation, but the acidification was induced only when the shoots were exposed to illumination (Rao et al., 2000a). Generally, the cause of acidification in the rhizosphere by legume crops was considered to be proton release from the excess uptake of cations during the N2 fixation (Israel and Jackson, 1982; Haynes, 1983; Lui et al., 1989), but this could not be used to explain light-induced acidification in the absence of N2 fixation. Since the acidification was induced by the exposure of shoot to light, the acidification might be expected to relate to photosynthetic activity and could possibly be the result of alterations in cation–anion uptake rates between dark and light conditions in the shoot.
In this study, photosynthetic activity, which was modulated by leaf size, light intensity and inhibitor greatly affected the light-induced acidification (Fig. 2). The intensity of acidification corresponded to the photosynthetic activity of the plant (Fig. 2 and Table 1). The total proton flux has shown a strong positive relationship with the total photosynthetic activity of the plant (Fig. 3). These results strongly support the hypothesis that in cowpea the photosynthetic activity regulates light-induced acidification. Previously, Jarvis and Hatch (1985) reported a diurnal pattern of acidification corresponding to the incoming radiation in nodulated Lucerne (Medicago sativa L.). This implies that the incoming radiation, which allows photosynthesis, has a significant effect on rhizosphere acidification. This not only supports our results but also shows the significance of the effect of photosynthetic activity on rhizosphere acidification in N2-fixing legumes.
The pH changes in the rhizosphere are mainly attributed to the imbalance in cation–anion uptake ratios (Haynes, 1990). In some crops, the uptake rates of cations and anions differ between dark and light conditions of the shoot (Le Bot and Kirkby, 1992; Ourry et al., 1996; Macduff et al., 1997). The pH changes are therefore expected to vary with changes in the uptake of cations and anions. In the present study, however, the light-induced acidification occurred even without the excess uptake of cations (Table 2). These results indicate that the acidification induced by light in cowpea was not related to excess uptake of cations. This assumption was further confirmed in the results, where the specific proton pump inhibitors of plasmalemma, DCCD and vanadate (Alcantara et al., 1991; Yan et al., 1998), could not stop the light-induced acidification (Fig. 5). This phenomenon suggests that the cause of acidification is not proton release, which was associated with excess cation uptake. Light-induced acidification occurring independently of ion uptake has been reported in maize (Mengel and Schubert, 1985; Schubert and Mengel, 1986) and vine (Mengel and Malissiovas, 1982) plants. These reports suggest that plants could be able to acidify the rhizosphere irrespective of the cation–anion uptake. In legumes, the acidification capability has often been related to excess cation uptake; however, the direct measurements of ion uptake are lacking. Most studies have related acidification to ash alkalinity, which is related to the excess cation content in the plant (Jarvis and Hatch, 1985; McLay et al., 1997; Tang, 1998). However, Tang (1998) accounted for only 40–50 % of acid production with plant excess cations and ash alkalinity. Our results suggest that the discrepancy could be related to light-induced acidification that is independent of ion uptake.
In general, rhizosphere acidification is reported to arise from the release of protons (Riley and Barber, 1971; Marschner and Römheld, 1983), from exudation of organic acids and amino acids (Marschner et al., 1987) or from the release of CO2 from the root (Laurent and Eric, 1994). The release of protons is generally related to excess cation uptake (Israel and Jackson, 1982; Haynes, 1983; Lui et al., 1989), but in the present study the cause for the acidification could not be explained through excess cation uptake and proton release. Though the cation/anion uptake balance could not fully explain light-induced acidification, the uptake ratios of cation/anion (Table 2) suggest relatively more uptakes of cations in light. Therefore, the uptake of cations coupled with other processes such as the exudation of organic or amino acids or CO2 release from root respiration could be causing the acidification in cowpea. Various amounts of organic acid exudation ranging from 0·14 to 14·0 nM h–1 cm–1 (Delhaize et al., 1993; Pellet et al., 1995; Neumann et al., 1999; Watt and Evans, 1999; Randall et al., 2001) in a number of crops could support the assumption. However, most studies have linked the exudation of organic acids either to the deficiency of nutrients or the tolerance of heavy metals or to the deformed roots (like proteiod roots). Therefore, the specific nature of root exudation in relationship to photosynthetic activity under normal conditions such as in the present study should be examined in detail. Also, the localized occurrence of acidification in the middle portion of the root axis and its regulation by the photosynthetic activity suggest that this phenomenon might depend on the supply of photosynthates to the root and their localized metabolism for the root exudation; both of these possibilities need to be thoroughly investigated. A detailed study is therefore warranted to resolve these issues.
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