Storage of foliar-absorbed nitrogen and remobilization for spring growth in young nectarine (Prunus persica var. nectarina) trees
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1 Tree Physiology 18, Heron Publishing----Victoria, Canada Storage of foliar-absorbed nitrogen and remobilization for spring growth in young nectarine (Prunus persica var. nectarina) trees M. TAGLIAVINI, 1 P. MILLARD 2 and M. QUARTIERI 1 1 Dipartimento di Colture Arboree, Università di Bologna, Via F. Re 6, Bologna, Italy 2 Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, U.K. Received June 23, 1997 Summary The effectiveness of spraying foliage with urea to provide nitrogen (N) to augment the seasonal internal cycling of N in young nectarine trees (Prunus persica (L.) Batsch var. nectarina (Ait. f. Maxim.), cv. Stark Red Gold) was studied. One-year-old trees were grown with contrasting N supplies during the summer and foliage was sprayed with a 2% urea solution labeled with 15 N just before leaf senescence started. After leaf abscission had finished, the trees were repotted in sand and given no further N. Remobilization of both labeled and unlabeled N for leaf growth the following spring was quantified. Leaves absorbed between 58 and 69% of the 15 N intercepted by the canopy irrespective of tree N status. During leaf senescence, the majority of 15 N was withdrawn from the leaves into the shoot and roots. Remobilization of 15 N the following spring was also unaffected by tree N status. About % of 15 N in the trees was recovered in the new growth. More unlabeled N (derived from root uptake) was remobilized for leaf growth in the spring than was withdrawn from leaves during canopy senescence the previous autumn. Therefore, soil-applied N augmented N storage pools directly, and contributed more to N remobilization the following spring than did foliar-absorbed 15 N. Keywords: foliar urea sprays, internal cycling, leaf growth, peach, root uptake. Introduction In fruit trees, spring growth, including flowering, depends on the remobilization of stored nitrogen in perennial organs (Muñoz et al. 1993, Millard 1995). Because the contribution that internal cycling of N makes to overall N metabolism each growing season depends mainly on the amount of N stored in perennial organs during the previous winter (Millard and Proe 1991, Neilsen et al. 1997) and is unaffected by the current N supply in the spring (Millard 1996), adopting fertilization strategies that ensure the proper formation of storage pools should enhance fruit production. Applying N in the late summer, after primary shoot development has stopped, may increase the N storage pools that will be remobilized the following year. Although fertilization of orchards by application of N to the soil in the late summer or autumn can potentially increase the amount of N remobilized during spring (Millard 1995), it may also give rise to environmental concerns, because it enhances the potential risk of nitrate leaching during the following winter and spring, when rainfall is much greater than evaporative demand. In addition, experiments with 15 N-labeled fertilizer have shown that N taken up by roots in autumn is preferentially partitioned to the root system compared to N taken up earlier (Sanchez et al. 1990, 1991, Muñoz et al. 1993). Foliar application of nitrogen has been suggested as an alternative to supplying nitrogen to the soil late in the season, because it minimizes nitrate leaching and enhances the storage of N in aboveground organs (Khemira 1995). The effectiveness of such applications, however, has not been fully investigated in peach. The only attempts to quantify leaf absorption of N have been based on either an increase in leaf N concentration (Leece and Kenworthy 1971) or on budget studies, but both techniques are relatively imprecise (Millard 1996). An alternative approach is to apply foliar sprays enriched with 15 N (Reickenberg and Pritts 1996) and then measure directly the increase in N storage pools attributable to 15 N (Millard 1996). We tested the hypothesis that spraying foliage with urea before leaf senescence is an effective means of augmenting the N used for internal cycling in nectarine trees. Our specific objectives were to: (i) quantify leaf absorption of 15 N from foliar sprays and withdrawal of 15 N during leaf senescence in low-n and high-n trees to determine if absorption and remobilization of N are affected by tree N status; (ii) identify the perennial organs that store foliar-absorbed N, and supply N for new growth in spring; and (iii) quantify the spring remobilization of both foliar-absorbed 15 N and unlabeled N from root uptake, and compare the amounts of N remobilized with the amounts of N withdrawn from senescing leaves in autumn. Material and methods Growth conditions and soil N supply In winter , 24, one-year-old nectarine trees (Prunus persica (L.) Batsch var. nectarina (Ait. f.) Maxim.), cv. Stark Red Gold on GF 305 rootstock (P. persica), were planted in
2 204 TAGLIAVINI, MILLARD AND QUARTIERI 40-l plastic pots, filled with a 3:2 (v/v) mix of sandy loam soil and sand. The trees were each pruned back to two shoots that were trained to grow in a V system. At planting, all trees received 5 g of N as calcium nitrate, as well as 0.02 g phosphorus, potassium and Fe-chelates. Trees were grown outdoors with pots inserted in a trench and protected against direct sunlight. To obtain trees differing in N status, trees were randomly allocated to either a low-n (LN) or a high-n (HN) treatment from the beginning of May until the end of August. The HN trees received 10 applications of N in the irrigation water. Each application comprised 3.5 g of N as a combination of calcium nitrate and potassium nitrate. The LN trees received 1.5 g of N as potassium nitrate at each of the first two applications and 0.5 g of N at each of the remaining eight applications. Both sets of trees also received 0.02 g of phosphorus in the irrigation water and two foliar fertilizations with micronutrients every 2 weeks. The effect of N supply on tree nitrogen status was assessed by determining the concentration of N in mid-shoot leaves of all trees in July 1995 when primary growth of the main and adventitious shoots had finished. Foliar application of labeled urea Early in September 1995, before leaf abscission started, trees were moved to a tunnel covered with transparent film. One of the two shoots per tree was randomly chosen and sprayed with a 2% (w/v) urea solution enriched with atom % 15 N. Sprays were applied three times (September 4, 6 and 8, between 0630 and 0730 h). To quantify precisely the amount of urea-n intercepted by the canopy of each tree, the selected shoot (treated shoot) was surrounded by a cone of absorbant paper, which was removed and weighed immediately after each spraying. Foliar N uptake, N withdrawal and N remobilization Three days after the last foliar spray, the two shoots of each tree (one treated shoot and one untreated shoot) were separately covered by a net and abscised leaves were collected three times a week (from September 13) until all the leaves had fallen (November 17). The area and mass of abscised leaves were recorded, and the samples bulked, milled and analyzed for total N concentration and 15 N abundance. In January 1996, four randomly chosen HN and LN trees were harvested and divided into the following organs: fine roots (less than 2 mm in diameter), coarse roots (including the aboveground part of the rootstock), stem, foliage from the treated shoot and foliage from the untreated shoot. After carefully washing the root systems of the remaining trees, they were transplanted to 40-l pots filled with pure sand that had been washed to eliminate residual nitrogen. The trees were grown outdoors and received no nitrogen during To assess the remobilization of foliar-absorbed 15 N and unlabeled N taken up by the roots for spring growth, trees were harvested on April 9, 1996, at the start of petal fall, and on May 3, 1996, at the beginning of fruit pit hardening. At each spring harvest, trees were divided into the same organs selected for the January harvest: in addition, flowers, fruits, shoots and white roots were separated. All tree organs from the January, April and May harvests were dried, milled and analyzed for total N and 15 N abundance by ANA-SIRA mass spectrometry (VG Isogas, Middlewich, Cheshire, U.K.). The 15 N enrichment was calculated by subtracting the background 15 N abundance measured in untreated control trees. The amount of 15 N and unlabeled N in each organ was calculated as described by Millard and Neilsen (1989). The amount of 15 N recovered in the new growth during 1996 was foliar-applied 15 N that had been stored during the winter and remobilized in the spring. The unlabeled N recovered in new growth was N taken up by the roots and internally cycled for spring growth. Foliar N absorption was calculated as the amount of 15 N in the harvested trees plus that recovered in abscised leaves. The amount of 15 N recovered in the organs of the trees harvested represented the amount of foliar-absorbed 15 N withdrawn from the sprayed leaves during senescence. Withdrawal of unlabeled N from senescing leaves To estimate the amount of unlabeled N withdrawn from senescing leaves, a sample of 10 leaves per treated shoot were collected before abscission started (September 11). This subsample represented between 5 and 10% of the leaves on the tree. After measuring leaf area, samples were washed, dried, milled and analyzed for N concentration. The unlabeled N content of the canopy was calculated and the amount withdrawn from senescing leaves was estimated as the difference between the amount of unlabeled N in the leaves before abscission and the amount retained in the abscised leaves. Statistical analysis and presentation of data The experimental design was completely randomized. Twelve replicates per N treatment were considered for assessing foliar N uptake and N withdrawal, and at each destructive harvest four replicates of each treatment were taken. The effects of N status were assessed by the Student s t-test. Comparison between original N and fertilizer N were performed by a paired t-test. Results Foliar uptake of urea- 15 N The soil N supply in 1995 did not affect total biomass of the trees during that year (data not given), but it affected the N status of the trees. In summer 1995, mean leaf N concentrations (% of dry matter) were 4.1 ± 0.01% in HN trees and 3.1 ± 0.1% in LN trees. Canopies of HN and LN trees had similar leaf areas at the beginning of September when foliar sprays were applied, because primary growth of main and auxiliary shoots had ceased by September and total leaf area did not change subsequently. On average, less than 40% of the N supplied in foliar sprays (data not shown) was intercepted by the shoots, regardless of tree N status. Table 1 shows that tree N status had no significant TREE PHYSIOLOGY VOLUME 18, 1998
3 STORAGE AND REMOBILIZATION OF N IN PRUNUS 205 Table 1. Amounts of nitrogen (mg N tree 1 ) intercepted by the canopy from foliar sprays, absorbed by the leaves, retained by leaves after abscission and withdrawn to perennial organs during leaf senescence in low-n (LN) and high-n (HN) trees. Each value is a mean ± standard error of 12 replicates. (P < 0.05) effect on the amount of 15 N absorbed by the leaves, which ranged from 58 to 69% of the amount intercepted by shoots. Regardless of tree N status, some (40--46%) of the 15 N was retained in the abscised leaves but most (54--60%) of the 15 N was withdrawn during leaf senescence and recovered in the harvested trees (Table 1). Nitrogen storage Intercepted Absorbed Retained Withdrawn N N N N LN Trees 332 ± ± ± ± 14 HN Trees 365 ± ± ± ± 27 In winter, % of the total 15 N per tree was stored in the root system (Table 2). Another significant portion of 15 N remained within the treated shoot (Table 2), whereas only a few mg of 15 N were translocated to the untreated shoot during leaf senescence. The nitrogen status of the trees did not significantly (P < 0.05) affect the within-tree distribution of foliarabsorbed 15 N in winter. The within-tree distribution of foliar-absorbed 15 N in winter did not differ significantly from the distribution of unlabeled N (Table 3), except that a higher percentage of unlabeled N (about 10% of total) than 15 N (5% of total) was recovered in the untreated shoot. Although the distribution of unlabeled N in winter was unaffected by tree N status, unlabeled N content per tree was 47% higher (P < 0.01) in HN trees than in LN trees (Table 3). Nitrogen remobilization in spring Because the trees that were harvested in spring 1996 had been transplanted in January 1996 to sand and were not supplied with N in 1996, we were able to assess the remobilization of both unlabeled N and 15 N for spring growth. The validity of this approach was demonstrated by the finding that the whole-tree contents of 15 N (Table 2) and unlabeled N (Table 3) were not significantly different (P < 0.05) between January and May. At the beginning of petal fall (April harvest), trees had remobilized around 18% of their 15 N for new growth, regardless of the amount of fertilizer N applied to the trees the previous year (Table 2). By the end of the experiment in May, remobilization had increased to around 42% of tree 15 N. By the time of the April harvest, remobilization of 15 N for shoot and flower growth was predominantly from the treated shoot, and from the coarse roots of LN trees as well. Remobilization of 15 N between the April and May harvests was mainly from coarse roots and treated shoots and also from the fine roots of LN trees (Table 2). The shoots, flowers and eventually fruits growing on the treated shoots had a higher content of 15 N than those on the untreated shoots (Table 2). Unlabeled N absorbed by the roots was also remobilized for shoot growth. In contrast to the foliar-applied 15 N, significantly more (P = 0.001) unlabeled N was remobilized in HN trees than in LN trees (Table 3). By the April harvest, about 19 and 10% of unlabeled N had been remobilized by HN and LN trees, respectively. At the final harvest in May, these values had risen to 36 and 26%. In LN trees, the unlabeled N was initially remobilized from the treated shoot, but by May it was being remobilized mainly from roots but also from the untreated shoot and stem (Table 3). In HN trees, the majority of unlabeled N was initially remobilized from the coarse roots and the untreated shoot. Between the April and May harvests, remobilization of unlabeled N was from both roots and shoots (Table 3). The importance of leaf senescence as a mechanism for providing N for storage during the winter is shown in Table 4. Leaf senescence enabled about 51 and 92% of the N subsequently remobilized for spring growth to be withdrawn from the canopy of HN and LN trees, respectively. Table 4 shows that, especially in HN trees, more unlabeled N was remobilized in the spring than was withdrawn from leaves during their Table 2. Effects of tree N status on the distribution of labeled nitrogen (mg 15 N tree 1 ) in different tree organs in January, April and May Values are the mean ± standard error of four replicates. Abbreviations: LN = low-n status; and HN = high-n status. Tree organs LN Trees HN Trees January April May January April May Fine roots 37.5 ± ± ± ± ± ± 8.5 Coarse roots 56.6 ± ± ± ± ± ± 4.8 Stem 5.6 ± ± ± ± ± ± 0.9 Treated shoot 28.0 ± ± ± ± ± ± 4.3 Flowers ± ± Shoots ± ± ± ± 11.0 Fruits ± ± 2.5 Untreated shoot 4.0 ± ± ± ± ± ± 0.3 Flowers ± ± Shoots ± ± ± ± 0.4 Fruits ± ± 0.4 Whole tree ± ± ± ± ± ± 30.4 TREE PHYSIOLOY ON-LINE at
4 206 TAGLIAVINI, MILLARD AND QUARTIERI Table 3. Effects of tree N status on the distribution of unlabeled nitrogen (mg N tree 1 ) in different tree organs in January, April and May Values are the mean ± standard error of four replicates. Abbreviations: LN = low-n status; and HN = high-n status. Tree organs LN Trees HN Trees January April May January April May Fine roots 866 ± ± ± ± ± ± 153 Coarse roots 1188 ± ± ± ± ± ± 149 Stem 126 ± ± ± ± 2 86 ± ± 18 Treated shoot 291 ± ± ± ± ± ± 78 Flowers ± ± Shoots ± ± ± ± 195 Fruits ± ± 42 Untreated shoot 230 ± ± ± ± ± ± 49 Flowers ± ± Shoots ± ± ± ± 66 Fruits ± ± 42 Whole tree 2701 ± ± ± ± ± ± 451 Table 4. Effects of tree N status on the amounts of N withdrawn from senescent leaves and the amounts of N remobilized for growth by May of the following year. All values are mg N tree 1 and represent the mean ± standard error of four replicates. Abbreviations: LN = low-n status; and HN = high-n status. senescence, the balance representing N taken up by the roots directly into storage. In the case of the foliar-applied 15 N, only 38 and 46% of the 15 N withdrawn during leaf senescence was subsequently remobilized by the LN and HN trees, respectively. Discussion LN Trees HN Trees Unlabeled N Withdrawn 594 ± ± 170 Remobilized 723 ± ± 151 Labeled N Withdrawn 112 ± ± 30 Remobilized 43 ± 5 58 ± 13 We used 15 N-labeled urea to demonstrate that nectarine trees can take up from 58 to 69% of the urea-n intercepted by the canopy, regardless of their N status. Because the tree canopies were washed 3 days after the final foliar spray (1 week after the first spray), all of the 15 N recovered in trees and abscised leaves is assumed to have been absorbed by the canopy during the 3 to 7-day period after spraying. Urea is considered the most suitable form of N to apply as a foliar N spray (Swietlik and Faust 1984) because the cuticle penetration of urea is times higher than that of inorganic ions (Yamada et al. 1965). Our data differ from previously published values of leaf absorption of urea-n by intact peach trees, which were mainly based on budget studies. Such studies led to the suggestion that, despite high leaf urease activity (Dilley and Walker 1961a), the efficiency with which leaves absorb N is low (Leece and Kenworthy 1971). Our data on nectarine leaves are comparable with results for apple leaves that are able to absorb up to 75% of applied urea over a 24-h period (Shim et al. 1973). More than half of the foliar-absorbed 15 N was translocated from the leaves during their senescence and recovered in the perennial organs. This agrees with the results of Castagnoli et al. (1990) who studied the remobilization of N from senescing leaves of peach and nectarine trees subjected to increasing N supply. For each harvested tree, we estimated the amount of 15 N present in the leaf biomass 3 days after the last urea spray, and showed that the amount of 15 N recovered in leaves was at least 25% less than that recovered in the perennial organs and abscised leaves in winter (Table 1), indicating that a significant proportion of the absorbed 15 N was translocated out of leaves during the first week after the initial foliar application of urea. Winter storage of 15 N was unaffected by the N status of the trees and long distance translocation (to the root system) was greater than short distance translocation (to the aboveground perennial organs). Partitioning of N to the root system in autumn for storage during winter is typical of young deciduous trees of several species including Acer pseudoplatanus L. (Millard and Proe 1991), Betula pendula Roth. (Wendler and Millard 1996) and Malus domestica Borkh. (Tromp 1983). The distribution of labeled and unlabeled N in the trees was similar, suggesting that when foliar-applied urea enters the leaf it is rapidly converted to amino acids, mainly aspartic and glutamic acids (Dilley and Walker 1961b), and indicating that the metabolism of root-absorbed and leaf-absorbed N do not differ. The LN and HN trees remobilized similar amounts of 15 N and a similar proportion (25--35%) of their unlabeled N for spring growth. However, HN trees remobilized twice the amount of unlabeled N compared with LN trees, indicating that the differential soil N supply in 1995 (12 versus 40 g N tree 1 ) resulted in significantly (P = 0.001) more unlabeled N being stored and remobilized in HN trees than in LN trees. In general, a generous soil N supply was more effective in increasing winter storage of N than the application of foliar urea (see Table 4), because only a small proportion of the foliar-absorbed 15 N withdrawn during leaf senescence was sub- TREE PHYSIOLOGY VOLUME 18, 1998
5 STORAGE AND REMOBILIZATION OF N IN PRUNUS 207 sequently remobilized the following spring. These findings are unlikely to have been influenced by the fact that the trees received no N supply to their roots during Experiments on a range of young deciduous and evergreen trees have shown that the amount of N remobilized is only dependent on the amount of N supplied the previous year and is unaffected by the supply of N in the spring (Millard 1996). Because more N was remobilized for leaf growth than was withdrawn from leaves during their senescence, root uptake must have contributed directly to N storage. Similar results have been reported by Weinbaum et al. (1984) for late-summer N uptake by mature Prunus dulcis (Mill.) D.A. Webb trees, and for Malus domestica by Millard and Thomson (1989). We found that increasing the soil N supply in 1995 greatly increased the amount of N that was remobilized in spring Withdrawal of unlabeled N from canopies of HN trees averaged 700 mg (Table 4), and HN trees remobilized 840 mg of unlabeled N more than LN trees. Shifting from a low-n to a high-n regime increased the amount of root-absorbed N partitioned directly to storage by about 730 mg tree 1. We conclude that: (i) peach leaves were able to absorb a considerable fraction of the urea applied as a foliar spray; (ii) foliar-absorbed N was effectively withdrawn to perennial organs, being stored mainly in the roots during winter and contributing to the spring growth of nectarine trees; (iii) internal cycling of foliar-absorbed N was unaffected by the N status of the tree; and (iv) soil-applied N augmented N storage pools directly and contributed much more to remobilization of N the following spring than foliar-absorbed N. Acknowledgments We thank Dr. A. Midwood for the 15 N analyses and Prof. B. Marangoni for providing support and encouragement. The technical help of M. Malaguti and G. Concari during sample collection is also gratefully acknowledged. This work was funded in part by the Italian Ministry of Universities (Project MURST 60%) and by the Scottish Office Agriculture and Fisheries Department. Financial support from the British Council and the Conferenza Permanente dei Rettori delle Università Italiane is also gratefully acknowledged. References Castagnoli, S.P., T.M. Dejong, S.A. Weinbaum and R.S. Johnson Autumn foliage applications of ZnSO 4 reduced leaf nitrogen remobilization in peach and nectarine. J. Am. Soc. Hortic. Sci. 115: Dilley, D.R. and D.R. Walker 1961a. Urease activity of peach and apple leaves. Proc. Am. Soc. Hortic. Sci. 77: Dilley, D.R. and D.R. Walker. 1961b. Assimilation of C 14 and N 15 labeled urea by excised apple and peach leaves. Plant Physiol. 36: Khemira, H Nitrogen partitioning and remobilization in fieldgrown apple trees. Ph.D. Thesis, Oregon State University, Corvallis, OR, 136 p. Leece, D.R. and A.L. Kenworthy Effect of potassium nitrate foliar sprays on leaf nitrogen concentration and growth of peach leaves. Hortscience 6: Millard, P Internal cycling of nitrogen in trees. Acta Hortic. 383: Millard, P Ecophysiology of the internal cycling of nitrogen for tree growth. J. Plant Nutr. Soil Sci. 159: Millard, P. and G.H. Neilsen The influence of nitrogen supply on the uptake and remobilization of stored N for the seasonal growth of apple trees. Ann. Bot. 63: Millard, P. and M.F. Proe Leaf demography and the seasonal internal cycling of nitrogen in sycamore (Acer pseudoplatanus L.) seedlings in relation to nitrogen supply. New Phytol. 117: Millard, P. and C.M. Thomson The effect of the autumn senescence of leaves on the internal cycling of nitrogen for the spring growth of apple trees. J. Exp. Bot. 40: Muñoz, N., J. Guerri, F. Legaz and E. Primo-Millo Seasonal uptake of 15 N-nitrate and distribution of absorbed nitrogen in peach trees. Plant Soil 150: Neilsen, D., P. Millard, G.H. Neilsen and E.J. Hogue Sources of N for leaf growth in a high-density apple (Malus domestica) orchard irrigated with ammonium nitrate solution. Tree Physiol. 17: Reickenberg, R.L. and M.P. Pritts Dynamics of nutrient uptake from foliar fertilizers in red raspberry (Rubus idaeus L.). J. Am. Soc. Hortic. Sci. 121: Sanchez, E.E., T.L. Righetti, D. Sugar and P.B. Lombard Seasonal differences, soil texture and uptake off newly absorbed nitrogen in field-grown pear trees. J. Hortic. Sci. 65: Sanchez, E.E., T.L. Righetti, D. Sugar and P.B. Lombard Recycling of nitrogen in field-grown Comice pears. J. Hortic. Sci. 66: Shim, K.K., J.S. Titus and W.E. Splittstoesser The fate of carbon and nitrogen from urea applied to foliage of senescing apple trees. J. Am. Soc. Hortic. Sci. 98: Swietlik, D. and M. Faust Foliar nutrition of fruit crops. In Horticultural Reviews, Vol. 6. Ed. J. Janick. Avi Publishing Company, Inc., Westport, CT, pp Tromp, J Nutrient reserves in roots of fruit trees, in particular carbohydrates and nitrogen. Plant Soil 71: Weinbaum, S.A., I. Klein, F.E. Broadbent, W.C. Mickie and T.T. Muraoka Effects of time of nitrogen application and soil texture on the availability of isotopically labeled fertilizer nitrogen to reproductive and vegetative tissue of mature almond trees. J. Am. Soc. Hortic. Sci. 109: Wendler, R. and P. Millard Impact of water and nitrogen supplies on the physiology, leaf demography and nitrogen dynamics in Betula pendula Roth. Tree Physiol. 16: Yamada, Y., S.H. Wittwer and M.J. Bukovac Penetration of organic compounds through isolated cuticular membranes with special reference to 14 C urea. Plant Physiol. 40: TREE PHYSIOLOY ON-LINE at
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