The absorption, translocation, and assimilation of urea, nitrate or ammonium in tomato plants at different plant growth stages in hydroponic culture
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1 Scientia Horticulturae 84 (2000) 275±283 The absorption, translocation, and assimilation of urea, nitrate or ammonium in tomato plants at different plant growth stages in hydroponic culture Xue Wen Tan, Hideo Ikeda *, Masayuki Oda Laboratory of Vegetable Crops, College of Agriculture, Osaka Prefecture University, Sakai, Osaka , Japan Accepted 13 August 1999 Abstract The absorption, translocation, and assimilation of urea, nitrate, and ammonium in tomato plants within 24 h after 15 N labeled compounds were applied at four different growth stages: seedling, owering, fruiting, and harvesting. The absorption of urea-n was only 25% of NO 3 -N at seedling stage, but it was up to about 80% of NO 3 -N at the subsequent growth stages. The translocation of urea-n was limited at seedling stage, but it was as fast as that of NO 3 -N at the subsequent growth stages. 15 N was found higher in the lamina of urea- or nitrate-fed plant, but higher in the stems and fruits of ammonium-fed plant. The assimilation of urea-n at seedling stage was less than half of that at the subsequent growth stages. The poor absorption, limited translocation, and slow assimilation of hydroponically applied urea may be the cause of growth reduction at seedling stage. Because as much as 94% of total- 15 N in the leaves of urea-fed plant at seedling stage and about 84% of that at the subsequent growth stages were found in the form of urea- 15 N, urea is not only absorbed but also translocated by the plant in the form of urea itself. At reproductive growth stage, the absorption, translocation, and assimilation of hydroponically applied urea were greatly improved, and urea should be a suitable hydroponic N source for tomato plants. # 2000 Elsevier Science B.V. All rights reserved. Keywords: Tomato; Urea; Growth stage; Absorption; Translocation; Assimilation * Corresponding author. Tel: ; fax: address: ikeda@plant.osakafu-u.ac.jp (H. Ikeda) /00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved. PII: S (99)
2 276 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275± Introduction The absorption or translocation of nitrate or ammonium has been investigated extensively in hydroponic culture at either seedling stage or reproductive stage of vegetable crops (Shelp, 1987; Liu and Shelp, 1993; Kosola and Bloom, 1996). The utilization of nitrate or ammonium was in uenced by plant genotype (Gabelman et al., 1986), solution ph (Yokota and Ojima, 1995), and solution temperature (Ikeda and Osawa, 1984). Moreover, the utilization of nitrate or ammonium was also affected by the growth stage in lima beans (McElhannon and Mills, 1978) and sweet corn (Mills and McElhannon, 1982). Urea is one of the most important nitrogen (N) fertilizers used for vegetable production in the eld (Vavrina and Obreza, 1993). Urea as an organic N source is, however, seldom used in hydroponic culture for vegetable production, although a few successes have been reported in reducing nitrate accumulation in leafy vegetables by partial replacement of nitrate with urea in the feed (Gunes et al., 1994). In recent years much attention has been focused on whether urea should be used as the sole hydroponic N source for vegetables, especially for the leafy vegetables (Luo et al., 1993; Khan et al., 1997; Zhu et al., 1997). Up to date studies of the utilization of hydroponically applied urea by fruit vegetables have been limited at seedling stage (Kirkby and Mengel, 1967; Gerendas and Sattelmacher, 1997). According to their ndings, urea was not a suitable hydroponic N source when it was compared with nitrate. Similar results were also obtained in our previous experiment with tomatoes at seedling stage (Ikeda and Tan, 1998). The response of fruit vegetables at different growth stages to the utilization of urea in hydroponic culture has received much less attention. In this study, we want to know whether urea is always not a suitable hydroponic N source at all the growth stages of tomato plants. To assess the possibility of using urea in hydroponic solution for tomato plants at reproductive growth stage, the absorption, translocation, and assimilation of urea, nitrate, and ammonium were compared at four different growth stages. 2. Materials and methods 2.1. Plant materials, growth conditions, and treatments Seeds of tomato (Lycopersicon esculentum Mill., cv. Momotaro) were sown in well-sterilized sand. Seedlings at the two leaf stage were cultured hydroponically in a 15 l container in a greenhouse during autumn (328C/208C day/night). Seedlings at the 6±7 leaf stage were transplanted into a deep water culture system with Hoagland's solution. Plants were pruned to one basal stem and were pinched
3 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275± at two leaves above the third cluster. Plants were treated with 15 N tracers at four growth stages for 24 h: when the fourth or fth leaf was fully expanded (seedling stage), when 2±3 owers on the rst cluster were owering ( owering stage), when 2±3 fruits on the rst cluster were about 3 cm in diameter (fruiting stage), and when 2±3 fruits on the rst cluster were red (harvesting stage). The basic solution was formulated as (in mm) K 2 SO 4 : 2, CaCl 2 2H 2 O: 1.5, MgSO 4 7H 2 O: 1, NaH 2 PO 4 2H 2 O: 2/3, and micronutrients. Plants were treated with three N sources: urea- 15 N (30.21% 15 N atom excess), NO 3-15 N as NaNO 3 (30.12% 15 N atom excess), and NH 4-15 N as (NH 4 ) 2 SO 4 (30.02% 15 N atom excess) at 200 mg Nl 1. Treatments were arranged in a randomized block design with three replicates, made in a growth chamber (258C-12 h/158c-12 h day/night) at seedling stage, and were made in the greenhouse as described above at other growth stages Sampling procedures and chemical analyses Plants were harvested 24 h after treatment and were divided into shoots and roots. The roots were washed with deionized water. Apart from the basal zero section, each section of the shoot comprised with two leaves above cluster and one leaf below that cluster as depicted in Fig. 1. From the base to top, the shoot was divided into zero, rst, second, and third sections. Each section was divided Fig. 1. The arrangement of shoot section of a tomato plant for sampling.
4 278 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275±283 into lamina, petiole, stem, and fruit. Samples were dried immediately in a forcedair oven at 1008C for the rst 30 min and at 608C thereafter, and were ground to a ne powder in a Wiley mill. The concentrations of total-n and total- 15 N were determined using a modi ed Kjeldahl method and an emission spectrometer (Yoneyama and Kumazawa, 1974), respectively. To determine the concentrations of leaf urea-n and NH 4 -N in urea-fed plant, the samples were extracted with hot water. The concentrations of urea-n and NH 4 -N were determined using the method of Cline and Fink (1956) and ion exchange chromatography (Dionex DX-AQ), respectively. NH 4-15 Nin the extract was collected by microdiffusion and was determined by the method of Yoneyama and Kumazawa (1974). Statistical analysis was made using analysis of variance, and the means were separated by Duncan's multiple range test (DMRT) at the 5% level. 3. Results Compared with the absorption of NO 3 -N or NH 4 -N within 24 h, the absorption of urea-n was most affected by growth stages (Table 1). From seedling to harvesting stage, absorption of N increased: 64 times for urea-n and only times for NO 3 -N or NH 4 -N. The absorption of urea-n was only 25% of NO 3 -N at seedling stage, whereas it was up to 66%, 82%, and 80% of NO 3 -N at owering, fruiting, and harvesting stage, respectively. The % distribution of 15 N in the shoot increased in the third section but decreased in the zero section from seedling to harvesting stage for all the N sources (Table 2). The % distribution of 15 N in the root of urea-fed plant was higher than that of nitrate-fed plant at seedling stage, but urea- and nitrate-fed plant showed a similar % distribution of 15 N in each plant section at the subsequent growth stages. At all growth stages, ammonium-fed plant had a higher Table 1 The absorption of urea, nitrate, and ammonium by tomato plants at seedling, owering, fruiting, and harvesting stage within 24 h after 15 N application Nitrogen source Absorption of 15 N (mg plant 1 ) a Plant growth stage Seedling Flowering Fruiting Harvesting Urea 0.84 (1) c 9.84 (12) c (43) b (64) b Nitrate 3.32 (1) a (4) a (13) a (20) a Ammonium 1.79 (1) b (7) b (20) b (31) b a Relative value when absorption of 15 N at seedling stage is represented as 1. Means in each column followed by different letters are signi cantly different at the 5% level by DMRT.
5 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275± Table 2 The % distribution of 15 N in the root and shoot section of tomato plants at seedling, owering, fruiting, and harvesting stage 24 h after 15 N application Plant section 15 N distribution (%) from three N sources a Urea Nitrate Ammonium Seedling stage b a b Root a b a Flowering stage a 2.51 b 1.08 c b a b a a b a a a Root b b a Fruiting stage a a b a a c a a b b b a Root b b a Harvesting stage a a b a a b a a a a a a Root b b a a Means among the N sources followed by different letters are signi cantly different at the 5% level by DMRT. % distribution of 15 N in the root but a lower distribution of 15 N in the third or second shoot section than the nitrate-fed plant. The % distribution of 15 N in the lamina, petiole, and stem of zero shoot section decreased from seedling to fruiting stage for all the N sources, and the % distribution of 15 N in each organ of the third section increased generally from seedling to harvesting stage (Fig. 2). 15 N was distributed more in the lamina of urea- or nitrate-fed plant, while even more in the stems and fruits of ammonium-fed plant throughout plant growth. The % distribution of 15 N in the lamina of top shoot section was the highest in the urea-fed plant regardless of growth stages. The assimilation of urea in the lamina of urea-fed plant at seedling stage was less than half of that at reproductive growth stages (Table 3). The assimilation of urea in the lamina of top shoot section was much higher than that of basal section. Among the total- 15 N in the lamina, as much as 94% at seedling stage and about
6 280 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275±283 Fig. 2. The % distribution of 15 N in the shoot organs of tomato plants at seedling, owering, fruiting, and harvesting stages 24 h after 15 N application. Each value is the means SE of three replicates. Values in the bars are % 15 N in different shoot organs at different shoot sections. Values in the bracket are the total- 15 N distribution in each shoot organ. 84% (average) at the subsequent growth stages remained unassimilated, and 3± 5% was changed from urea- 15 NtoNH 4-15 N at all the growth stages. 4. Discussion What form of N is absorbed by the plant when urea is applied as the sole hydroponic N source? This topic has been investigated in recent years. Our investigation showed that urea is not only absorbed but also translocated by the
7 Table 3 The concentration and assimilation of 15 N in the lamina of tomato plants fed with urea at seedling, owering, fruiting, and harvesting stage 24 h after 15 N application Growth stage X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275± Shoot section 15 N concentration (mg g 1 DW) a 15 N assimilation Urea- 15 N NH 4-15 N Total- 15 (%) b N Seedling (94.0) 10.8 (2.9) c Flowering (82.0) 13.8 (5.2) a (87.2) 6.2 (5.3) b Fruiting (80.7) 24.6 (4.9) a (87.7) 11.9 (5.2) b Harvesting (81.4) 15.1 (4.8) a (87.0) 9.5 (5.1) b a The percentage of the total- 15 N. b 15 N assimilation: (total- 15 N urea- 15 N) 100/total- 15 N, according to Bowman and Paul (1992). Means in the column followed by different letters are signi cantly different at the 5% level by DMRT. plant as urea, not as NH 4 -N which is the by-product of the hydrolyzed urea. The evidences are: (1) as much as 94% of total- 15 N in the leaves of urea-fed plant at seedling stage and about 84% of that at the subsequent growth stages were detected in the form of urea- 15 N and (2) no ammonium was detected in the urea feed 24 h after treatment. At seedling stage, the absorption of urea was only 25% of nitrate, and the translocation of urea was also less than nitrate. Urea was accumulated more in the root and was not translocated to the shoot as fast as nitrate at seedling stage. Furthermore, the assimilation of urea at seedling stage was much slower than that at the subsequent growth stages. The poor absorption, limited translocation, and slow assimilation of urea may be the cause of growth reduction when urea is applied at seedling stage as the sole hydroponic N source for tomato plants. This nding is consistent with the earlier ndings with tomato in which the relatively low concentrations of total-n in the tissues of urea-fed plant at seedling stage were contributed to the insuf cient absorption of urea in comparison with that of nitrate or ammonium (Kirkby and Mengel, 1967). On the other hand, the chlorotic and developed necroses at the leaf edges of urea-fed zucchinis plant at seedling stage (Gerendas and Sattelmacher, 1997) may be the symptom of urea excess due to insuf cient assimilation. 15 N was distributed more in the lamina of nitrate-fed plant, but more in the stems and fruits of ammonium-fed plant. This nding is in agreement with our previous ndings (Ikeda, 1991). There are evidences to support the notion that urea is transported by transpiration stream: (1) urea is transported as such; (2) a high distribution of 15 N in the lamina of the top shoot section was detected in
8 282 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275±283 urea-fed plant at all the growth stages; (3) urea- and nitrate-fed plant showed a similar distribution of 15 N in each plant section at reproductive growth stages; and (4) nitrate is transported from root to top in tomato plant through transpiration stream (Kirkby and Mengel, 1967). Although the absorption of urea was only 25% of nitrate at seedling stage, it was up to about 80% of nitrate at the subsequent growth stages. The translocation of urea was as fast as that of nitrate at reproductive growth stages, and the assimilation of urea at these stages was more than twice that at seedling stage. The absorption, translocation, and assimilation of hydroponically applied urea were greatly improved after seedling stage. Therefore, it is feasible to use urea as the sole hydroponic N source for tomato plants at reproductive growth stages. Acknowledgements We thank H. Furukawa for his several helpful discussions on the experiment, and all the students in our laboratory for their assistance during the experiment. This study was supported by Grants-in-Aid for Scienti c Research (H. Ikeda: no ) from the Ministry of Education, Science, Sports, and Culture of Japan. References Bowman, D.C., Paul, J.L., Foliar absorption of urea, ammonium, and nitrate by perennial ryegrass turf. J. Amer. Soc. Hort. Sci. 117(1), 75±79. Cline, R.E., Fink, R.M., Investigation of color reaction between p-dimethyl aminobenzaldehyde and urea or ureide acids. Anal. Chem. 28(1), 47±52. Gabelman, W.H., Gerloft, G.C., Schettini, T., Coltman, R., Genetic variability in root systems associated with nutrient acquisition and use. Hort. Sci. 21(4), 971±973. Gerendas, J., Sattelmacher, B., Signi cance of N source (urea vs. NH 4 NO 3 ) and Ni supply for growth, urease activity and nitrogen metabolism of zucchini (Cucurbita pepo convar. giromontiina). Plant and Soil 196(1), 217±222. Gunes, A., Post, W.N.K., Kirkby, E.A., Aktas, M., In uence of partial replacement of nitrate by amino acid nitrogen or urea in the nutrient medium on nitrate accumulation in NFT grown winter lettuce. J. Plant Nutr. 17(11), 1929±1938. Ikeda, H., Utilization of nitrogen by vegetable crops. Jpn. Agric. Res. Quart. 25(2), 117±124. Ikeda, H., Osawa, T., Lettuce growth as in uenced by N source and temperature of the nutrient solution. In: Proceedings of the Sixth International Congress On Soilless Culture, pp. 273±284. Ikeda, H., Tan, X.W., Urea as an organic nitrogen source for hydroponically grown tomatoes in comparison to inorganic nitrogen sources. Jpn. Soil Sci. Plant Nutr. 44(4), 609±615. Khan, N.K., Watanabe, M., Watanabe, Y., Effect of different concentrations of urea with or without nickel on spinach (Spinacia oleracea L.) under hydroponic culture. In: Ando, T., Fujita, K., Matsumoto, H., Mori, S., Sekiya, J. (Eds.), Plant Nutrition for Sustainable Food Production and Environment. Kluwer Academic Publishers, Tokyo, pp. 85±86.
9 X.W. Tan et al. / Scientia Horticulturae 84 (2000) 275± Kirkby, E.A., Mengel, K., Ionic balance in different tissues of the tomato plant in relation to nitrate, urea, or ammonium nutrition. Plant Physiol. 42(1), 6±14. Kosola, K.R., Bloom, A.J., Chlorate as a transport analog for nitrate absorption by roots of tomato. Plant Physiol. 110(4), 1293±1299. Liu, L., Shelp, B.J., Nitrogen partitioning in greenhouse-grown broccoli in response to varying NH 4 : NO 3 ratios. Commun. Soil Sci. Plant Anal. 24(1), 45±60. Luo, L., Lian, Z.H., Yan, X.L., Urea transformation and the adaptability of three leafy vegetables to urea as a source of nitrogen in hydroponic culture. J. Plant Nutr. 16(3), 797±812. McElhannon, W.S., Mills, H.A., In uence of percent NO 3 =NH 4 on growth, N absorption, and assimilation by lima beans in solution culture. Agron. J. 70(4), 1027±1032. Mills, H.A., McElhannon, W.S., Nitrogen uptake by sweet corn. Hort. Sci. 17(5), 743±744. Shelp, B.J., Plant characteristics and nutrient composition and mobility of broccoli (Brassica oleracea var. italica) supplied with NH 4,NO 3 or NH 4NO 3. J. Exp. Bot. 38(195), 1603±1618. Vavrina, C.S., Obreza, T.A., Response of Chinese cabbage to nitrogen rate and source in sequential plantings. Hort. Sci. 28(12), 1164±1165. Yokota, S., Ojima, K., Physiological response of root tip of alfalfa to low ph and aluminum stress in water culture. Plant and Soil 171(1), 163±165. Yoneyama, T., Kumazawa, K., A kinetic study of the assimilation of 15 N-labeled ammonium in rice seedling roots. Plant Cell Physiol. 15(4), 655±661. Zhu, Z.J., Gerendas, J., Sattelmacher, B., Effects of replacing of nitrogen with urea or chloride on the growth and nitrate accumulation in pak-choi in the hydroponics. In: Ando, T., Fujita, K., Matsumoto, H., Mori, S., Sekiya, J. (Eds.), Plant Nutrition for Sustainable Food Production and Environment. Kluwer Academic Publishers, Tokyo, pp. 963±964.
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