Relationships Between Nitrogen and Water Concentration in Shoot Tissue of Molinia caerulea During Shoot Development
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1 Annals of Botany 83: 3 3, 999 Article No. anbo , available online at http: on Relationships Between Nitrogen and Water Concentration in Shoot Tissue of Molinia caerulea During Shoot Development B. THORNTON*, G. LEMAIRE, P. MILLARD* and E. I. DUFF * Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen, AB5 8QH, UK, Station d Ecophysiologie, INRA, 80 Lusignan, France and Biomathematics and Statistics Scotland, Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen, AB5 8QH, UK Received: November 998 Returned for revision: 0 January 999 Accepted: 5 February 999 Plants of Molinia caerulea were supplied with either a low (0 mol m ) or high (0 mol m ) supply of nitrogen over two growing seasons. A total of destructive plant harvests were made: when plants were in an over-wintering state prior to the second season; immediately following bud burst; and on further occasions throughout the second season. The relationships between shoot nitrogen concentration on a dry mass basis, shoot water content and plant developmental stage were investigated. Shoot nitrogen concentration on a dry mass basis fell as the growing season progressed. In contrast, the concentration of nitrogen in tissue water after bud burst showed only a slight reduction. The concentration of nitrogen both on a dry mass basis and in tissue water was greater for plants receiving the higher supply of nitrogen. Shoot water content was highest immediately following bud burst then declined as the season progressed, with plants receiving the low nitrogen supply having slightly greater shoot water contents. It was concluded that the decline in shoot nitrogen concentration of M. caerulea on a dry mass basis as the mass increased was mainly explained by changes in shoot water content. The observed increase in the rate of decline of both shoot nitrogen concentration and water content with increased shoot mass coincided with the cessation of leaf tissue production and was therefore due to a switch from the production of leaves to other tissues. 999 Annals of Botany Company Key words: Molinia caerulea (L.), purple moor grass, nitrogen, water content, shoot development. INTRODUCTION In many plant species the shoot concentration of nitrogen, expressed on a dry mass basis, declines as shoot dry mass increases (Caloin and Yu, 98; Leigh and Johnston, 985; Greenwood et al., 990, 99; Justes et al., 99). One generally accepted explanation for this decline is that, as the shoot grows and the amount of photosynthetic tissue increases, proportionally more structural tissue is required to support it. As structural tissue contains a lower nitrogen concentration than photosynthetic tissue, this results in an overall reduction in the nitrogen concentration of the shoot (Lemaire et al., 99; Lemaire and Gastal, 997). In barley (Hordeum ulgare L.) the nitrogen concentration of the shoot, expressed both on a dry mass and tissue water basis, was found to decline as the season progressed (Leigh and Johnston, 985). The decline in nitrogen concentration on a dry mass basis was greater than that in tissue water; in fact, the nitrogen concentration of tissue water increased after anthesis (Leigh and Johnston, 985). This suggests that while some of the decline in shoot nitrogen concentration on a dry mass basis is due to the change in nitrogen concentration of tissue water, changes in shoot water content may also have been partly responsible. Different relationships between shoot nitrogen concen- For correspondence. Fax (0) 355, b.thornton mluri.sari.ac.uk $ tration on a dry mass basis and shoot mass exist for isolated plants and those growing in dense canopies (Lemaire and Gastal, 997). A linear relationship, with a negative gradient, between ln(shoot nitrogen concentration) and ln(shoot mass) was found for isolated plants of sweet sorghum during vegetative growth. Individual plants growing in a dense canopy also gave the same relationship during the early period of growth, but when the leaf area index of the crop approached one, a more negative relationship than that for equivalent isolated plants was observed (Lemaire and Gastal, 997). The difference between isolated and individual plants in a dense canopy was thought to be due to differing proportions of structural tissue in the plant shoot. Lemaire and Gastal (997) considered that, as competition for light increased, individual plants within dense canopies developed a greater proportion of structural tissue, and consequently lower nitrogen concentrations, than isolated plants of equivalent shoot mass. However, care should be taken in comparing plants of the same mass subjected to differing treatments as they may be at different stages of development. Molinia caerulea (L.) Moench (purple moor grass) is a deciduous, perennial grass (Jefferies, 9; Salim et al., 988) which is widespread and dominant in many areas throughout upland Britain (Rodwell, 99). During winter the plants have swollen basal internodes with attached buds and an extensive root system. In spring these buds develop into new shoot material (Jefferies, 9). Leaf growth in 999 Annals of Botany Company
2 3 Thornton et al. Nitrogen and Water in De eloping Molinia caerulea Shoots spring is concomitant with mobilization of nitrogen from basal internodes and roots, but later in the season nitrogen is withdrawn from leaves and directed towards developing flowers and storage in basal internodes and roots over winter (Thornton and Millard, 993). The relationship between nitrogen concentration and mass, observed in crop plants subject to selective breeding, may not be applicable for unimproved species adapted to less fertile environments. The relationships between nitrogen concentration (on both a dry mass and tissue water basis), dry mass and water content of M. caerulea shoots were examined over a growing season with two contrasting supplies of nitrogen. The following hypotheses were tested: () the decline in nitrogen concentration of shoots of M. caerulea, on a dry mass basis, as their mass increases is partly explained by changes in shoot water content; () the more rapid decline in shoot nitrogen concentration previously observed with plants in dense canopies, compared with isolated plants of equivalent mass, is due in part to differences in the developmental stage of the plants. MATERIALS AND METHODS Full details of plant collection, conditions of growth, plant harvesting and sample analysis are given in Thornton and Millard (993), and only a summary of relevant details is presented here. Tussocks of Molinia caerulea in their overwintering state were collected on 9 Apr. 989, from a fieldsite in the Fife Forest District, Cleish Hills, Scotland, UK. Tillers were separated and three basal internodes with attached roots were planted in 8 cm diameter pots containing expanded mica. The pots were placed, for two growing seasons, within an open-sided greenhouse, which protected the plants from rain, but exposed them to natural variations in environmental conditions. A total of pots were arranged in a randomized block structure and, at each subsequent harvest, four replicates of each treatment were removed. Each pot received cm of a complete nutrient solution three times each week throughout the growing seasons, containing either 0 mol m or 5 mol m ammonium nitrate (0 or 0 mol m N), and deionized water when the expanded mica appeared visibly dry. Destructive harvests were taken when the plants were in an overwintering state between growing seasons (Julian day 3), immediately following bud burst (Julian day 9), and on twelve further occasions throughout the second season (Julian days 0, 7, 9,, 57, 77, 8, 98,,, 0 and 55). At harvest, plants were washed free of the expanded mica and separated into roots, the original basal internode planted, basal internodes produced in the first season, basal internodes produced in the second season, laminae plus sheaths produced in the second season (live and dead material) and flowers plus stems. All material was weighed fresh and after drying at 70 C, and dried samples were milled prior to determination of nitrogen concentration using an ANA-SIRA mass spectrometer (VG Isogas, Middlewich, UK). Bacon (988) commented that plants allocate very little nitrogen to cell walls. The mean nitrogen concentration of internodes in Lolium species, a tissue in which the cell wall was estimated to account for 0% of the dry matter, was found to be 0 8% (Wilman and Altimimi, 98). Presumably the nitrogen concentration of the isolated cell wall would have been less than 0 8%. Consequently, in order to calculate the concentration of nitrogen in tissue water in the present experiment it was assumed that all the nitrogen was present in the aqueous phase. This concentration represents the weighted mean of cytoplasm and vacuole. All statistical procedures were performed using Genstat 5 Release 3. (Lawes Agricultural Trust, IACR-Rothamsted, UK). The data presented in Figs to were subject to analysis of variance (ANOVA) with harvest date and nitrogen supply as treatment factors. To stabilize the variance, some variables required transformation (shoot and leaf dry mass, log (n ); nitrogen concentration on a dry mass basis, angular arcsine). As transformation did not affect the interpretation of results, untransformed data are presented for clarity. The broken stick models (Figs 5 and ) were fitted by minimizing the residual variance on the y-axis. Comparison of these models with simple linear regression models was carried out to assess the improvement gained by fitting the broken stick models. Using the estimated slopes and standard errors from the broken stick models, t-tests were carried out to assess differences between gradients within models and between gradients in different models. Similarly, the x-values at which the break points occurred in different models were compared using t-tests. RESULTS At the start of the second growing season, leaf material was the major component of shoot dry mass, irrespective of the nitrogen supply (Fig. ). Leaf growth was complete by Julian day 77 as no further increase in leaf dry mass occurred after this date (P 0 05). Shoot growth did continue beyond Julian day 77 (P 0 00). The contribution of leaf material to the total shoot mass, therefore, decreased as the season progressed (Fig. ). The shoot nitrogen concentration on a dry mass basis (shoot % N) of M. caerulea fell throughout most of the season. However towards the end of the season (Julian day 55), the values remained constant (P 0 00, Fig. ). At any given time, shoot % N of plants receiving the high nitrogen supply was greater than that of plants receiving the low nitrogen supply (P 0 00, Fig. ). From before bud burst (Julian day 3) to the last sampling date (Julian day 55), shoot % N declined by a similar proportion irrespective of nitrogen supply (7% for low, compared with 73% for the high supply of nitrogen, Fig. ). The concentration of nitrogen in the shoot tissue water was greatest in the overwintering buds (Fig. 3), but fell rapidly after bud burst to values which showed only slight but significant reduction (P 0 00) over the rest of the season. Plants receiving the higher nitrogen supply had greater concentrations of nitrogen in tissue water (P 0 00, Fig. 3). The shoot water content of M. caerulea increased from that in the overwintering buds to the highest observed values immediately after bud burst, but then declined as the season progressed
3 Thornton et al. Nitrogen and Water in De eloping Molinia caerulea Shoots A leaf shoot [N] (percent dry mass) Dry mass (g) 0 0 B leaf shoot FIG.. Relationships between shoot nitrogen concentration on a dry mass basis (% dry mass) and time (Julian days) for M. caerulea plants receiving either a low or high supply of nitrogen. The values are means of four replicates s.d. except for plants on Julian day 3 where the value represents one analysis on material pooled from four replicates. Bud burst occurred immediately before the harvest on Julian day FIG.. Relationships between dry mass of shoot and leaves and time (Julian days), for M. caerulea plants receiving either a low (A) or a high (B) supply of nitrogen. Values are means of four replicates s.d. Bud burst occurred immediately before the harvest on Julian day 9. (Fig., P 0 00). Beyond Julian day 98, no further reduction in water content of the shoot per unit dry mass occurred (Fig. ). Considered over all harvest dates, plants receiving the low nitrogen supply had slightly greater shoot water contents compared with plants receiving the high nitrogen supply (P 0 0, Fig. ). Because of the observed differences in the concentration of nitrogen in tissue water and of shoot water content between the over-wintering buds and the shoot tissue at other times of the season (Figs 3 and ), the following analyses were restricted to shoot growth after bud burst. When shoot % N was plotted against shoot dry mass using natural logarithmic axes, two-phase dynamics for the decline in nitrogen concentration were observed (Fig. 5). Similar dynamics were also observed for shoot water content (Fig. ). The data variance accounted for by the broken stick models was greater than that for simple linear regression in three out of the four models; in the remaining model the variance was equal to that accounted for by linear [N] (mg N g H O) FIG. 3. Relationships between concentration of nitrogen (mg N g water) in shoot tissue and time (Julian days) for M. caerulea plants receiving either a low or high supply of nitrogen. Values are means of four replicates s.d. Bad burst occurred immediately before the harvest on Julian day 9. regression. In Fig. 5, the variance accounted for by the broken stick models was 89 and 9% for plants receiving a low and high supply of nitrogen, respectively, compared with 87 and 93% using linear regression. In Fig., for plants receiving a low or high nitrogen supply, the variance
4 3 Thornton et al. Nitrogen and Water in De eloping Molinia caerulea Shoots Water content (g H O g dry mass) In(shoot water content) In(shoot dry mass) 3 FIG.. Relationships between shoot water content (g water g dry mass) and time for M. caerulea plants receiving either a low or high supply of nitrogen. Values are means of four replicates s.d. Bud burst occurred immediately before the harvest on Julian day 9. FIG.. Relationships between the natural logarithm of shoot water content (g water g dry mass) and the natural logarithm of shoot dry mass (g) for M. caerulea plants receiving either a low or high supply of nitrogen. Values are for individual replicates. The lines were fitted using broken stick models. For low N plants at x 7, y x whereas at x 7, y x. For high N plants at x 5, y 5 0 x whereas at x 5, y x. In(shoot %N) In(shoot dry mass) FIG. 5. Relationships between the natural logarithm of shoot nitrogen concentration (% dry mass) and the natural logarithm of shoot dry mass (g) for M. caerulea plants receiving either a low or high supply of nitrogen. Values are for individual replicates. Lines were fitted using broken stick models. For low N plants at x 9, y x whereas at x 9, y x. For high N plants at x, y 0 x whereas at x, y x. accounted for was 85 and 8% using the broken stick model compared with 85 and 83% using linear regression. The initial gradients (at lower dry mass) of ln(shoot % N) s. ln(shoot dry mass) were similar (P 0 05) irrespective of nitrogen supply (Fig. 5). After the break point, the gradients were more negative (P 0 0 low N, P 0 00 high N), but still unaffected by nitrogen supply (P 0 05; 3 Fig. 5). The relationship of ln(shoot water content) s. ln(shoot dry mass) also showed similar initial gradients irrespective of nitrogen supply (P 0 05) at lower shoot dry mass. After the break point, the gradient became significantly more negative only for plants receiving the high nitrogen supply (P 0 00; Fig. ). With the low supply of nitrogen, the x-values at which the breaks in the broken stick model occurred were similar (P 0 05) irrespective of whether ln(shoot % N) or ln(shoot water content) was plotted against ln(shoot dry mass) (Figs 5 and ). With the high supply of nitrogen, there was evidence that the values of ln(shoot dry mass) at which the breaks occurred differed (P 0 05; Figs 5 and ). For the relationship of ln(shoot % N) s. ln(shoot dry mass) the break points occurred at 9 and on the x-axis, equivalent to shoot dry masses of 0 0 and 3 g, for plants receiving low or high supplies of nitrogen, respectively. From Fig. the dates at which these dry masses were achieved can be estimated: Julian day 9 for the low nitrogen supply and between days and 57 for the high supply. For the relationship of ln(shoot water content) s. ln(shoot dry mass) the breaks occurred at 7 and 5, equivalent to shoot dry masses of 0 07 and 5 g. These shoot masses were achieved between Julian days and 57 for plants receiving the low nitrogen supply and between days 57 and 77 for plants receiving the high nitrogen supply. The similarity, at any given nitrogen supply, of the overall relationships between ln(shoot % N) an ln(shoot water content) when plotted against ln(shoot dry mass) (Figs 5 and ) is emphasized by the relationships which existed between shoot % N and shoot water content (Fig. 7).
5 N concentration (% dry mass) Thornton et al. Nitrogen and Water in De eloping Molinia caerulea Shoots 35 0 Water content (g H O g dry mass) FIG. 7. Relationships between shoot nitrogen concentration on a dry mass basis (% dry mass) and shoot water content (g water g dry mass) for M. caerulea plants receiving either a low or high supply of nitrogen. Values are for individual replicates. Lines were obtained by plotting back-transformations of the fitted broken stick models in Figs 5 and, against each other, for both the low and high supply of nitrogen. DISCUSSION The observed results for M. caerulea agree with those of Leigh and Johnston (983, 985) who found that, in H. ulgare, the seasonal decline in the shoot concentration of both nitrogen and potassium was greater on a dry mass than tissue water basis. In field-grown plants of M. caerulea, Aerts and de Caluwe (989) found that the percentage retranslocation of nitrogen from leaves, leaf sheaths and culms changed little with increased nutrient availability; the present results, showing that the proportional decline in shoot % N was independent of nitrogen supply, support this. Differences in the nitrogen concentration of shoots of M. caerulea on a dry mass basis resulting from differing supplies of nitrogen were attributable, in this investigation, to differences in the concentration of nitrogen in the tissue water; such differences were not observed in H. ulgare by Leigh and Johnston (985). The observed differences in the shoot nitrogen concentration on a dry mass basis, which occurred after bud burst, were mainly attributable to changes in shoot water content. Lemaire and Gastal (997) considered that the decline in shoot nitrogen concentration, on a dry mass basis, as shoot dry weight increased, was caused by an increase in the proportion of structural tissue required to support photosynthetic tissue. An accelerated decline in shoot nitrogen concentration in plants from dense canopies, compared with that of isolated plants, was thought to be due to the same phenomenon (Lemaire and Gastal, 997). The present results are consistent with the conclusions of Lemaire and Gastal (997), assuming that structural tissue contains a lower water content than photosynthetic tissue, because an increased proportion of structural tissue in the shoot would also result in an overall reduction in shoot water content (on a dry mass basis). Acceleration in the rate of decline of shoot nitrogen concentration on a dry mass basis has been observed to occur after flowering in sorghum (Greenwood et al., 990; Ple net and Cruz, 997). The causes of the accelerated decline of both shoot % N and water content of M. caerulea with increased shoot mass may be twofold: () an effect of competition for light on plants as shoot mass increases, as shown by Lemaire and Gastal (997) for plants in dense canopies; or () a developmental change leading to production of a greater proportion of structural tissue of reduced nitrogen and water concentrations. The fact that the break points in ln-ln plots of Figs 5 and occurred at very different shoot dry masses for the two nitrogen treatments, but that these different masses were all achieved around the time of cessation of leaf tissue production, indicates that only the second hypothesis needs to be considered. Shoot growth after the break point consisted of increases in flower stems, flowers and new basal internodes for storage over the following winter (Thornton and Millard, 993). In Lolium perenne and L. multiflorum, flower stems were found to have lower nitrogen concentrations than leaf blades (Wilman and Altimimi, 98); an increase in the proportion of flower stems would, therefore, result in a greater reduction in shoot nitrogen concentration than an equivalent increase in leaf material. Concomitant with flower stem production, leaf material may senesce, with the onset of nitrogen mobilization both from leaves to other tissues (Thornton and Millard, 993) and or within leaves (Hirose, Werger and van Rheenen, 989). The relationship between % N and water content of the shoot remains remarkably unaffected by the developmental changes occurring at the time of cessation of leaf growth. The concentration of nitrogen in tissue water, therefore, appears to be relatively constant, irrespective of the development of the plant, and reflects the nitrogen status of the plant independent from its development. In contrast to Leigh and Johnston (985), an increase in the nitrogen concentration of tissue water after anthesis was not observed in the present results. These authors considered that the increase they observed was due to development of ears containing high concentrations of nitrogen in the tissue water (Leigh and Johnston, 985). The differences between these observations could be explained by the fact that M. caerulea flowers in the present study had not reached the same maturity as the corresponding H. ulgare flowers at the end of the respective experiments. The concept of the use of the nitrogen concentration in tissue water as an indicator of plant nitrogen status has to be restricted to growth associated with volume expansion. It cannot be applied during growth of storage organs such as grain or tubers when dry mass increase is not necessarily associated with water accumulation. It will also be of limited use during water stress, as the variation in the nitrogen concentration in tissue water may not reflect nitrogen nutrition but mainly fluctuation in water content. The concentration of nitrogen in tissue water in M. caerulea after bud burst was similar to the preanthesis values of between 5 0 mg N g tissue water observed in H. ulgare (Leigh and Johnston, 985), supporting the sugges-
6 3 Thornton et al. Nitrogen and Water in De eloping Molinia caerulea Shoots tion of Greenwood et al. (99) that the nitrogen concentration of either the metabolic or structural components of plants varied little between species of the same metabolic group (C or C ). In conclusion, the decline in the nitrogen concentration of the shoots of M. caerulea on a dry mass basis, as mass increased after bud burst, is mainly explained by changes in shoot water content. The concentration of nitrogen in the tissue water of shoots showed only a small decrease beyond bud burst. A more rapid decline in shoot nitrogen concentration was due, not to an increased proportion of structural tissue required to support leaves competing for light, but to a switch in the type of tissue produced from leaves to flower stems, flowers and new basal internodes. ACKNOWLEDGEMENTS This work was funded by the Scottish Office Agriculture, Environment and Fisheries Department. We thank MR Tyler for skilled technical assistance. LITERATURE CITED Aerts R, de Caluwe H Aboveground productivity and nutrient turnover of Molinia caerulea along an experimental gradient of nutrient availability. Oikos 5: Bacon JSD Structure and chemistry. In: Ørskov ER, ed. Feed science. Amsterdam: Elsevier Science Publishers B. V., Caloin M, Yu O. 98. Analysis of the time course of change in nitrogen content in Dactylis glomerata L. using a model of plant growth. Annals of Botany 5: 9 7. Greenwood DJ, Gastal F, Lemaire G, Draycott A, Millard P, Neeteson JJ. 99. Growth rate and % N of field grown crops: theory and experiments. Annals of Botany 7: Greenwood DJ, Lemaire G, Gosse G, Cruz P, Draycott A, Neeteson JJ Decline in percentage N of C and C crops with increasing plant mass. Annals of Botany : 5 3. Hirose T, Werger MJA, van Rheenen JWA Canopy development and leaf nitrogen distribution in a stand of Carex acutiformis. Ecology 70: 0 8. Jefferies TA. 9. The vegetative anatomy of Molinia caerulea, the purple heath grass. New Phytologist 5: 9 7. Justes E, Mary B, Meynard J-M, Machet J-M, Thelier-Huche L. 99. Determination of a critical nitrogen dilution curve for winter wheat crops. Annals of Botany 7: Leigh RA, Johnston AE Concentrations of potassium in the dry matter and tissue water of field-grown spring barley and their relationships to grain yield. Journal of Agricultural Science, Cambridge 0: Leigh RA, Johnston AE Nitrogen concentrations in field-grown spring barley: an examination of the usefulness of expressing concentrations on the basis of tissue water. Journal of Agricultural Science, Cambridge 05: Lemaire G, Gastal F N uptake and distribution in plant canopies. In: Lemaire G, ed. Diagnosis of the nitrogen status in crops. Berlin, Heidelberg: Springer-Verlag, 3 3. Lemaire G, Khaity M, Onillon B, Allirand JM, Chartier M, Gosse G. 99. Dynamics of accumulation and partitioning of N in leaves, stems and roots of lucerne (Medicago sati a L.) in a dense canopy. Annals of Botany 70: Ple net D, Cruz P Maize and sorghum. In: Lemaire G, ed. Diagnosis of the nitrogen status in crops. Berlin, Heidelberg: Springer-Verlag, Rodwell JS. 99. British plant communities, olume : Mires and heaths. Cambridge: Press Syndicate of the University of Cambridge. Salim KA, Carter PL, Shaw S, Smith CA Leaf abscission zones in Molinia caerulea (L.) Moench, the purple moor grass. Annals of Botany : 9 3. Thornton B, Millard P The effects of nitrogen supply and defoliation on the seasonal internal cycling of nitrogen in Molinia caerulea. Journal of Experimental Botany : Wilman D, Altimimi MAK. 98. The digestibility and chemical composition of plant parts in Italian and perennial ryegrass during primary growth. Journal of the Science of Food and Agriculture 33:
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