Growth Analysis of Solution Culture-grown Winter Rye, Wheat and Triticale at Different Relative Rates of Nitrogen Supply

Annals of Botany 84 : 467–473, 1999 Article No. anbo.1999.0935, available online at http :\\www.idealibrary.com on

Growth Analysis of Solution Culture-grown Winter Rye, Wheat and Triticale at Different Relative Rates of Nitrogen Supply I. A. P A P O N O V*†, S. L E B E D I N S K AI‡ and E. I. K O S H K IN‡ * Institut fuW r PflanzenernaW hrung (330), UniŠersitaW t Hohenheim, 70593 Stuttgart, Germany and ‡ Department of Plant Physiology, TimiryazeŠ Agricultural Academy, Moscow, Russia Received : 16 April 1999

Returned for revision : 21 May 1999

Accepted : 18 June 1999

At low nitrogen (N) supply, it is well known that rye has a higher biomass production than wheat. This study investigates whether these species differences can be explained by differences in dry matter and nitrogen partitioning, specific leaf area, specific root length and net assimilation rate, which determine both N acquisition and carbon assimilation during vegetative growth. Winter rye (Secale cereale L.), wheat (Triticum aestiŠum L.) and triticale (X Triticosecale) were grown in solution culture at relative addition rates (RN) of nitrate-N supply ranging from 0n03–0n18 d−" and at non-limiting N supply under controlled conditions. The relative growth rate (RW) was closely equal to RN in the range 0n03–0n15 d−". The maximal RW at non-limiting nitrate nutrition was approx. 0n18 d−". The biomass allocation to the roots showed a considerable plasticity but did not differ between species. There were no interspecific differences in either net assimilation rate or specific leaf area. Higher accumulation of N in the plant, despite the same relative growth rate at non-limiting N supplies, suggests that rye has a greater ability to accumulate reserves of nitrogen. Rye had a higher specific root length over a wide range of sub-optimal N rates than wheat, especially at extreme N deficiency (RN l 0n03–0n06 d−"). Triticale had a similar specific root length as that of wheat but had the ability to accumulate N to the same amount as rye under conditions of free N access. It is concluded that the better adaptation of rye to low N availability compared to wheat is related to higher specific root length in rye. Additionally, the greater ability to accumulate nitrogen under conditions of free N access for rye and triticale compared to wheat may be useful for subsequent N utilization during plant growth. In general, species differences are explained by growth components responsible for nitrogen acquisition rather than carbon assimilation. # 1999 Annals of Botany Company Key words : Growth analysis, nitrogen, nitrogen productivity, partitioning, specific root length, Secale cereale L., Triticum aestiŠum L., X Triticosecale, winter rye, winter wheat, winter triticale.

INTRODUCTION The growth of plants during the vegetative stage may be described as a combination of both functional and structural components responsible for carbon assimilation and nutrient acquisition. The functional components are net assimilation rate (AA, the dry matter productivity per unit leaf area per unit time) and specific absorption rate (σ, amount of nitrogen (N) per unit root length per unit time). The structural components are dry matter partitioning to roots ( fr), specific leaf area (Sla, leaf area per unit leaf weight) and specific root length (Srl, root length per unit root weight). Relative growth rate (RW, plant dry matter increment per unit plant dry matter per unit time) may be presented as a function of components responsible for carbon assimilation eqn (1) and nitrogen acquisition eqn (2) : (1) RW l AA(1kfr) Sla RW l σfr Srl\cp

(2)

The AA is a balance between photosynthesis and respiration ; both of which depend on N status of the plant (Lambers and Dijkstra, 1987). fr decreases at high N availability † For correspondence. Fax j49 711 459 3295. E-mail paponov! uni-hohenheim.de

0305-7364\99\100467j07 $30.00\0

(Hirose, 1986 ; Hirose and Kitajima, 1986 ; Hirose, Freijsen and Lambers, 1988). Sla usually decreases under conditions of extreme N limitation (Hirose, 1986). It is obvious that specific nitrogen absorption rate (σ) increases with increased N availability. There are different data concerning the reaction of Srl to N limitation, which are obviously strongly genotype specific (Robinson and Rorison, 1988 ; Bernston, Farnsworth and Bazzaz, 1995 ; Ryser and Lambers, 1995). The N concentration in the plant (cp) is linearly related to RW at limiting N supply (A/ gren, 1985 ; A/ gren and Bosatta, 1996). Thus, all these components of RW are dependent on N availability. Moreover, these components may affect nitrogen acquisition and carbon assimilation in different ways. If higher biomass allocation to the roots increases nitrogen acquisition, carbon assimilation is decreased. It is well known that rye is more efficient under poor soil conditions, even though the yield potential under nonlimiting conditions is lower compared to wheat (e.g. Bland, 1971 ; Stoskopf, 1985). We suggest that the better adaptation of rye to low levels of available N compared to wheat might be caused by differences in plasticity of functional and structural components of growth. The aim of the present work was to investigate whether interspecific differences between rye and wheat exist in structural and functional components of growth responsible for carbon assimilation # 1999 Annals of Botany Company

PaponoŠ et al.—Growth Analysis of Winter Cereals

and nitrogen acquisition at different N nutritional status of the plants. We used the relative addition rate technique (RN, nitrogen increment per unit nitrogen per unit time) that allows the N availability to plants to be controlled. Plants grown with this technique attain a stable internal nitrogen concentration, where the RW is equal to the applied RN if the RN does not exceed the maximum RW (Ingestad, 1982 ; Ingestad and Lund, 1986). Triticale as a hybrid species, which combines many of the better qualities of both parents, e.g. high yield potential for wheat and effective growth of rye at low soil fertility, was also included in this study.

MATERIALS AND METHODS Seeds of winter rye (Secale cereale L., ‘ Voskhod 1 ’), winter wheat (Triticum aestiŠum L., ‘ Mironovskaja 808 ’) and winter triticale (X Triticosecale, gen 35) were imbibed in 0n01 m CaSO solution for 4 d. On the fourth day, the % seeds were removed from the seedlings. For the following 6 d, the seedlings were grown in a solution containing all necessary mineral nutrients except N in order to dilute the initially high plant N content. The plants were kept in a growth chamber with a 16 h photoperiod and photon flux density (PFD) of 200 µmol m−# s−" in the spectral range 400–700 nm. The pH of the solution was adjusted daily and kept in the range 5n5–6n5. The average nitrogen content of seedlings was about 0n5 mg N. From 10 d after sowing, a limiting amount of nitrate in the form of KNO was added daily at the rates $ calculated using the following equation (Ingestad and Lund, 1979) (3) NtkNt− l Nt− (eRNk1) " " where Nt and Nt− are amounts of nitrogen in the plant at " time t and tk1, respectively. The nitrate was added at the RN 0n03 ; 0n06 ; 0n09 ; 0n15 ; and 0n18 d−". It was assumed that all added N was taken up by plants on a daily basis. The period of steady-state growth was ascertained in separate experiments. The lag phase (13 d for RN 0n18 d−" to 17 d for RN 0n03 d−") preceded the time at which constant nitrogen concentration and relative growth rate were attained. In the subsequent experimental period (7–8 d) nutrition and growth were controlled by the addition treatments. The non-limited cultures started with a concentration of 1 m nitrate in solution. There were five harvests between 20 d after sowing (DAS) and 28 DAS with an interval of 2 d between each harvest. The final dry weight with nonlimiting N supply was about 0n6 g per plant.

Growth parameters Growth was measured as the increasing dry weight obtained after drying for 48 h at 70 mC. The RW was determined as the slope of the natural logarithm of total plant dry weight Šs. time using least-squares linear regression. Net assimilation rate per unit shoot weight (AW) was calculated from RW divided by the shoot weight ratio (1kfr). Leaf area was measured in a photometric area

counter (Leaf Area Meter, Li-Cor, model 3100, Lincoln, Nebraska, USA). Specific leaf area (Sla) was obtained by division of leaf area by shoot dry weight. Senescent leaves which were observed at RN of 0n03 d−" were excluded from measurements of leaf area. Root length was measured using the grid intercept method (Tennant, 1975).

Determination of N Reduced N of shoots and roots was analysed using the ‘ classical ’ Kjeldahl method with concentrated sulphuric acid, K SO , and Se as a catalyst. This Kjeldahl procedure # % reduced a very small proportion of the nitrate (Greenwood et al., 1990), which is included in the ‘ Reduced-N ’. The N content was subsequently determined colorimetrically using indophenol blue. For measurements of nitrate concentration in plant material, the method of Cataldo et al. (1975) was used.

Replicates Growth data were obtained from four replicate plants at each harvest. Averages from the first and last, or all five harvests were used at limiting or non-limiting N supply, respectively. RESULTS Growth and tissue N concentration Figure 1 shows the experimentally determined values of RW at RN and at non-limiting N nutrition. The RW closely approached the RN up to 0n15 d−". The maximum RW determined at non-limiting N nutrition was close to 0n18 d−" (Fig. 1). The RW was linearly related to plant N concentration in the range of 0n06 d−" to free access of N for wheat and to 0n18 d−" RN for rye and triticale (Fig. 2). At non-limiting N supply, rye and triticale accumulated a higher N concentration in the plant than wheat with no corresponding

0·25 0·20 RW (d–1)

468

0·15 0·10 0·05

0

0·05

0·15 0·10 RN (d–1)

Free access

F. 1. Relative growth rate (RW) plotted as a function of relative addition rate (RN) for winter rye ($), wheat (#) and triticale (X). Bars represent s.e.

PaponoŠ et al.—Growth Analysis of Winter Cereals

469

T     1. List of symbols used Symbol AA AW cp cr cs fr Lar NO p $ NO r $ NO s $ Nt RN RW Sla Srl σ

Parameter

Dimension g DW m−# d−" g DW (g DW)−" d−" mmol N (g DW)−" mmol N (g DW)−" mmol N (g DW)−" g DW (g DW)−" m# (kg DW)−" mmol N (g DW)−" mmol N (g DW)−" mmol N (g DW)−" mmol N mmol N (mmol N)−" d−" g DW (g DW)−" d−" m# (kg DW)−" m (g DW)−" mmol N m−" d−"

Net assimilation rate per unit leaf area Net assimilation rate per unit shoot weight Nitrogen concentration in plant Nitrogen concentration in root Nitrogen concentration in shoot Root weight ratio Leaf area ratio Nitrate concentration in plant Nitrate concentration in root Nitrate concentration in shoot Amount of nitrogen in plant at time t Relative uptake rate of nitrogen Relative growth rate of plant Specific leaf area Specific root length Specific absorption rate

0·7

0·20

0·6

0·15

0·5

(A)

fr

RW (d–1)

0·25

0·10

0·4

0·05

0·3

0

1

2 3 cp (mmol N g–1 DW)

0·2

4

F. 2. Relationship between total plant relative growth rate (RW) and total plant nitrogen concentration in winter rye ($), wheat (#) and triticale (X). Bars represent s.e.

1

4

2 3 cp (mmol N g–1 DW)

4

cs (mmol N g–1 DW)

increase in growth (Fig. 2). A decrease in RN to 0n03 d−" did not decrease the N concentration of the plants compared with 0n06 d−" RN (Fig. 2).

0

(B)

3

2

1

Dry matter and nitrogen partitioning Fractions of plant dry weight in the root ( fr) were plotted against reduced nitrogen concentration in the plant for rye, wheat and triticale (Fig. 3 A). The cereal species demonstrated a high tendency to allocate dry matter to the root under nitrogen limiting stress. With non-limiting nitrogen nutrition, the root weight ratio ( fr) was about 25 %, whereas at minimal nitrogen supply (0n03 d−" RN) the cereals allocated about 60 % of the total plant dry matter to roots. No significant differences between the three species were observed. Reduced N concentrations in the shoot (cs) were plotted against reduced N concentration in the root (cr) for rye, wheat and triticale (Fig. 3 B). Under conditions of free access, rye had a higher ratio of N concentration in the shoot

0

1

2 3 cr (mmol N g–1 DW)

4

F. 3. (A) Relationship between root contribution to total plant dry weight ( fr) and total plant nitrogen concentration (cp) and (B) relationship between nitrogen concentration in shoot (cs) and nitrogen concentration in root (cr) in winter rye ($), wheat (#) and triticale (X). Bars represent s.e.

to N concentration in the root than wheat. Triticale occupied an intermediate position. In the range of N supplies from 0n03–0n18 d−" RN, no species differences were found. Rye also accumulated more nitrate in the shoot at the

470

PaponoŠ et al.—Growth Analysis of Winter Cereals

16 Sla (m2 kg–1)

0·6

0·4

0·2

NO3p (mmol N g–1 DW)

12 8 4

0·2 0·4 0·6 –1 NO3r (mmol N g DW)

0

0·8

(A)

20

(A)

0

0·8

1

4

2 3 cs (mmol N g–1 DW)

200

(B)

(B) 160

0·6 Srl (m g–1)

NO3s (mmol N g–1 DW)

0·8

0·4

0·2

0

120 80 40

1

2 3 cp (mmol N g–1 DW)

0

4

F. 4. (A) Relationship between nitrate concentration in shoot (NO s) $ and nitrate concentration in root (NO r) and (B) relationship between $ nitrate concentration in plant (NO p) and nitrogen concentration in $ plant (cp) in winter rye ($), wheat (#) and triticale (X). Bars represent s.e.

0·05

0·15 0·10 RN (day–1)

Free access

F. 5. (A) Relationship between specific leaf area (Sla) and nitrogen concentration in shoot (cs) and (B) specific root length (Srl) at different relative addition nitrogen rates (RN) for winter rye ($), wheat (#) and triticale (X). Bars represent s.e.

Specific leaf area and specific root length No significant differences between species were found in specific leaf area (Sla) at equal cs (Fig. 5 A). The lowest values of Sla were observed at the lowest values of cs. With subsequent increases in cs, the Sla increased rapidly at first and then more slowly. In the N-limited range of 0n03–0n15 d−" RN, rye had a higher Srl than wheat and triticale (Fig. 5 B). Rye adapted to extreme low N availability (0n03–0n06 d−" RN) with a significant increase in Srl to about 180 m g−". Net assimilation rate The net assimilation rate per unit shoot weight increased with increasing shoot N concentration in the range of low cs, but further increases in cs did not result in great increases in

AW (g g–1 day–1)

0·24

expense of nitrate accumulation in the root compared to wheat (Fig. 4 A). Triticale occupied an intermediate position. Rye and triticale both accumulated more reduced N and nitrate in the plant under free access conditions (Fig. 4 B).

0·20 0·16 0·12

AW = (cs – 0·437)/(1·751 + 3·767(cs – 0·437)) r2 = 0.88

0·08 0·04

0

1

2 3 cs (mmol N g–1 DW)

4

F. 6. The dependence of the net assimilation rate (AW) on the shoot nitrogen concentration (cs) in winter rye ($), wheat (#) and triticale (X).

AW (Fig. 6). The relationship between AW and cs could be fitted, by least squares, to a hyperbolic function : AW l (csk0n437)\(1n751j3n767(csk0n437)) r# l 0n88

(4)

No significant interspecific differences were found (Fig. 6).

PaponoŠ et al.—Growth Analysis of Winter Cereals DISCUSSION RelatiŠe growth rate and plant N concentration A/ gren (1985) and A/ gren and Bosatta (1996) related RW to the plant nitrogen concentration by a proportional factor ‘ nitrogen productivity ’ (the slope of the line) and a constant identified by extrapolation to RW l 0. A linear relationship between RW and cp was found in the N-limiting range for several perennial species (Ingestad, 1979, 1981 ; Ericsson, 1981 ; Jia and Ingestad, 1984 ; Ingestad and Ka$ hr, 1985 ; Coleman, Dickson and Isebrands, 1998) and in Pisum and Lemna (Oscarson, Ingemarsson and Larsson, 1989 a). However, calculating plant carbon balances from photosynthesis minus respiration and accounting for leaf maturation, A/ gren and Bosatta (1996) demonstrated that a linear relationship between RW and cp was valid for a wide range of limiting N supply. However, at extreme N deficiency (RW 0n06 d−"), the RW decreased relatively more rapidly per unit decrease of plant nitrogen concentration. Hirose et al. (1988) studied the growth of Plantago species at different RN and also suggested that there was a rapid decrease in RW with relatively small decreases in plant nitrogen concentration at extreme N deficiency, although within a wide range of N-limitation, the linear relationship between RW and cp was still observed. Applying relative N addition rate methods to barley cultivars, Mattsson et al. (1991) also observed hyperbolic curves between RW and cp rather than straight lines. In agreement with this observation, in our study, a hyperbolic relationship was observed between RW and cp for wheat, triticale and rye (Fig. 2). Possibly, a marked senescence of lower leaves, which was observed in our experiment at RN 0n03 d−", was an important factor in determining the decrease in RW with relatively small decreases of cp. At free access to N, the cereal species had similar RW (Fig. 1). However, rye accumulated more N in the plant than wheat under this condition (Fig. 2). This can be explained mainly by the higher accumulation of reduced N in the shoot by rye (Fig. 3 B) and a high shoot weight ratio at high levels of N supply (Fig. 3 A). Moreover, the higher nitrate accumulation in the shoot at the expense of the root in rye compared to wheat (Fig. 4 A), together with a high shoot weight ratio at high N supply (Fig. 3 A), also resulted in a higher nitrate accumulation in the whole rye plant compared to wheat (Fig. 4 B). Triticale accumulated reduced N and nitrate under free access conditions in similar amounts to rye (Fig. 4 B). Since a decrease in N availability during crop growth can result in N being limiting for the plant, the N storage of both reduced N and nitrate may be of significance for subsequent remobilization of nitrogen during a later stage of crop growth.

471

cerning interspecific differences in allocation pattern and plasticity. Chapin (1980, 1988) hypothesized that the adaptation of species from infertile soils was due to high inflexible fr. In contrast, Reynolds and D’Antonio (1996) found no evidence to support this hypothesis in their detailed review. Mattsson et al. (1991) compared old and modern barley varieties but did not find any consistent differences in the plasticity of dry matter allocation. Our data (Fig. 3 A) are consistent with data of Mattsson et al. (1991), i.e. dry matter allocation pattern cannot explain interspecific differences in adaptation to low N levels. Specific root length. Nutrient uptake is related to root length rather than to root weight (Nye and Tinker, 1977 ; Chapin, 1980). If a fixed proportion of assimilate is used for root growth, a much greater root length can be achieved by increasing specific root length (Fitter, 1985). Considering that dry matter allocation to roots is constrained by intrinsic limits and only rarely does fr increase above 0n67 (Reynolds and D’Antonio, 1996), increasing specific root length may be important for nutrient acquisition. Indeed, wide genetic variation in Srl has been reported (Fitter, 1991). Analysis of Srl in fast- and slow-growing species demonstrated that the latter possessed greater plasticity than fast-growing species (Robinson and Rorison, 1988 ; Bernston et al., 1995). According to our study, rye as a species with high adaptive potential to poor soil conditions, has a higher Srl in a wide range of N supply with especially high values of Srl at extreme N deficiency (0n03–0n06 d−" RN). Root systems grown in hydroponics are not representative of soil-grown roots because of differences in soil resistance encountered and the availability of nutrients at the root surface (Taylor, 1974 ; Nye and Tinker, 1977). However, Mian et al. (1994) worked with different wheat genotypes and found that seedling growth in hydroponics predicted subsoil root length growth in the field. The absolute values of specific root length for cereals in our study is comparable to that found for wheat grown in the soil (Robinson, Linehan and Gordon, 1994). Robinson et al. (1994) observed Srl values in the range of 144–211 m g−". N uptake. During the transition from sub-optimal to non-limiting N nutrition, the plants will likely absorb nitrate at maximal rates in order to fill storage pools, after which the uptake rate will decrease to rates in phase with consumption. The observed lower uptake rates under these conditions could be explained either by a decreased number of nitrate transporters or by down regulation of transporter activity (Clarkson, 1986 ; Ingemarsson et al., 1987 ; Oscarson et al., 1989 b ; Mattsson et al., 1991). The fact that rye and triticale accumulated more nitrogen under the non-limited N condition (Fig. 2) suggested that nitrate uptake by these species was not so strongly down-regulated as in wheat.

Contribution of the growth components to nitrogen acquisition

Contribution of the growth component to carbon assimilation

Dry matter allocation to root. Increased dry matter allocation to the roots with decreasing nitrogen supply is a well known phenomenon (Chapin, 1980 ; Lambers and Poorter, 1992). However, contradicting reports exist con-

Leaf area. The amount of leaf area per total plant weight, i.e. the leaf area ratio, is a major factor determining the potential relative growth rate of the plants (e.g. Lambers and Poorter, 1992). Comparison of a wide range of plant

472

PaponoŠ et al.—Growth Analysis of Winter Cereals

species demonstrated that higher leaf area ratio was related mainly to higher specific leaf area, while dry matter allocation pattern is less important (Poorter and Remkes, 1990 ; Poorter, Remkes and Lambers, 1990 ; Garnier, 1992 ; Van der Werf et al., 1993 a, b). However, no interspecific differences in specific leaf area were found using the winter cereals in the study (Fig. 5 A). A strong decrease in Sla at extremely low N availability (0n03 d−" RN) was obviously related to the increased contribution of senescent leaf tissue dry matter to total leaf weight rather than to leaf thickness. Net assimilation rate. The curvilinear relationship between photosynthesis and leaf N concentration (Field, 1983 ; Hirose and Werger, 1987) and increasing respiratory loss with increasing N concentration (Lambers et al., 1981 a, b ; Hirose and Kitajima, 1986) results in a curvilinear relationship between AW and cs (Fig. 6), despite increasing biomass allocation to the shoot (Fig. 3 A). The comparison of many slow- and fast-growing species demonstrated that AA was not responsible for differences in RW between species (Poorter and Remkes, 1990 ; Poorter, Remkes and Lambers, 1990 ; Garnier, 1992 ; Van der Werf et al., 1993 a, b ; Hunt and Cornelissen, 1997). These data are in agreement with our observations since no differences in net assimilation rate were found between winter cereals.

Strategy of adaptation to N deficiency Model calculations indicate that a very low root density, defined as root length per unit soil volume, was sufficient to utilize almost all nitrate in soil (Barraclough, 1986, 1989). In field-grown plants, however, nitrate uptake may be restricted to certain root zones because of lack of root-soil contact (Veen et al., 1992), low accessibility of nitrate in compacted soil clods, cortical senescence in older parts of the root system (Lascaris and Deacon, 1991) or drying of the top soil. Furthermore, nitrate uptake of field-grown plants may often occur at suboptimal temperature (Engels and Marschner, 1995). Therefore, it is possible that under certain conditions, the size and morphology of root systems may be significant for the nitrate uptake of field-grown plants. Low levels of available N in the soil are often related to low levels of other nutrients. Apparently, the longer roots will be significantly more useful for uptake of nutrients supplied mainly by diffusion. In this case, increased root length under N-limiting conditions may be important not only for nitrogen uptake but also for uptake of other nutrients. Thus, the greater root length of rye could be an advantage compared to wheat under poor soil conditions. Considering that nitrate content fluctuates in the soil and usually decreases during crop growth, the higher accumulation of storage N, both reduced N and nitrate, by rye compared to wheat may also be significant. Apparently, storage of N during the vegetative growth stage may be important for later use during generative growth. Triticale also accumulated high amounts of storage N under nonlimiting N conditions, but was unable to modify root morphology in response to low N supply to the extent observed for rye. The higher yield potential under nonlimiting conditions for wheat compared to rye cannot be

explained by N use efficiency during the vegetative stage. To understand the reason for yield differences between species under optimal conditions we need to study N uptake and its utilization during the generative stage.

A C K N O W L E D G E M E N TS We thank G. I. A/ gren, C. Engels, D. J. Greenwood and H.-J. Hawkins for detailed revisions of the manuscript.

LITERATURE CITED A/ gren GI. 1985. Theory of growth of plants derived from the nitrogen productivity concept. Physiologia Plantarum 64 : 17–28. A/ gren GI, Bosatta E. 1996. Theory for plant growth. In : Theoretical ecosystem ecology. Cambridge : Cambridge University Press, 113–138. Barraclough PB. 1986. The growth and activity of winter wheat roots in the field : Nutrient inflows of high yielding crops. Journal of Agricultural Science, Cambridge 106 : 53–59. Barraclough PB. 1989. Root growth, macro-nutrient uptake dynamics and soil fertility requirements of a high-yielding winter oilseed rape crop. Plant and Soil 119 : 59–70. Bernston GM, Farnsworth EJ, Bazzaz FA. 1995. Allocation, within and between organs, and the dynamics of root length changes in two birch species. Oecologia 101 : 439–447. Bland BF. 1971. Crop production : cereals and legumes. London, New York : Academic Press. Cataldo DH, Haroon M, Schrader LE, Youngs VL. 1975. Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communication of Soil Science and Plant Analysis 6 : 71–81. Chapin FS III. 1980. The mineral nutrition of wild plants. Annual ReŠiew of Ecology and Systematics 11 : 233–260. Chapin FS III. 1988. Ecological aspects of plant mineral nutrition. AdŠances in Plant Nutrition 3 : 161–190. Clarkson DT. 1986. Regulation of the absorption and release of nitrate by plant cells : A review of current ideas and methodology. In : Lambers H, Stulen I, eds. Fundamental, ecological and agricultural aspects of nitrogen metabolism in higher plants. Dordrecht, The Netherlands : Martinus Nijhoff Publishers, 3–27. Coleman MD, Dickson RE, Isebrands JG. 1998. Growth and physiology of aspen supplied with different fertilizer addition rates. Physiologia Plantarum 103 : 513–526. Engels C, Marschner H. 1995. Plant uptake and utilization of nitrogen. In : Bacon PE, ed. Nitrogen fertilization in the enŠironment. New York, Basel, Hong Kong : Marcel Dekker, 41–81. Ericsson T. 1981. Effects of varied nitrogen stress on growth and nutrition in three Salix clones. Physiologia Plantarum 51 : 423–429. Field C. 1983. Allocating leaf nitrogen for the maximization of carbon gain : Leaf age as a control on the allocation program. Oecologia 56 : 341–347. Fitter AH. 1985. Functional significance of root morphology and root system architecture. In : Fitter AH, Atkinson DJ, Read DJ, Usher MB, eds. Ecological interactions in soil. Special Publication of British Ecological Society, No. 4. Oxford : Blackwell Scientific, 87–106. Fitter AH. 1991. Characteristics and functions of root systems. In : Waisel Y, Eshel A, Kafkafi U, eds. Plant roots the hidden half. New York, Basel, Hong Kong : Marcel Dekker, Inc, 3–25. Garnier E. 1992. Growth analyses of congeneric annual and perennial grass species. Journal of Ecology 80 : 665–675. Greenwood DJ, Lemaire G, Gosse G, Cruz P, Draycott A, Neeteson JJ. 1990. Decline in percentage N of C and C crops with increasing $ % plant mass. Annals of Botany 66 : 425–436. Hirose T. 1986. Nitrogen uptake and plant growth. II. An empirical model of vegetative growth and partitioning. Annals of Botany 58 : 487–496.

PaponoŠ et al.—Growth Analysis of Winter Cereals Hirose T, Kitajima K. 1986. Nitrogen uptake and plant growth. I. Effect of nitrogen removal on growth of Polygonum cuspidatum. Annals of Botany 58 : 479–486. Hirose T, Werger MJA. 1987. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiologia Plantarum 70 : 215–222. Hirose T, Freijsen AHJ, Lambers H. 1988. Modelling of the responses to nitrogen availability of two Plantago species grown at a range of exponential nutrient addition rates. Plant, Cell and EnŠironment 11 : 827–834. Hunt R, Cornelissen JHC. 1997. Components of relative growth rate and their interrelations in 59 temperate plant species. New Phytologist 135 : 395–417. Ingemarsson B, Oscarson P, af Ugglas M, Larsson CM. 1987. Nitrogen utilization in Lemna. II. Studies of nitrate uptake using "$NO −. $ Plant Physiology 85 : 860–864. Ingestad T. 1979. Nitrogen stress in birch seedlings. II. N, K, P, Ca, and Mg nutrition. Physiologia Plantarum 45 : 149–157. Ingestad T. 1981. Nutrition and growth of birch and grey alder seedlings in low conductivity solutions and varied relative rates of nutrient additions. Physiologia Plantarum 52 : 454–466. Ingestad T. 1982. Relative addition rate and external concentration. Driving variables used in plant nutrition research. Plant, Cell and EnŠironment 5 : 443–453. Ingestad T, Ka$ hr M. 1985. Nutrition and growth of coniferous seedlings at varied relative nitrogen addition rate. Physiologia Plantarum 65 : 109–116. Ingestad T, Lund AB. 1979. Nitrogen stress in birch seedlings. I. Growth technique and growth. Physiologia Plantarum 45 : 137–148. Ingestad T, Lund AB. 1986. Theory and techniques for steady state mineral nutrition and growth of plants. ScandinaŠian Journal of Forest Research 1 : 439–453. Jia H, Ingestad T. 1984. Nutrient requirements and stress response of Populus simonii and Paulownia tomentosa. Physiologia Plantarum 62 : 117–124. Lambers H, Dijkstra P. 1987. A physiological analysis of genotypical variation in relative growth rate : can growth rate confer ecological advantage ? In : van Andel J, Bakker JP, Snaydon RW, eds. Disturbance in glasslands. Dordrecht, The Netherlands : Junk Publishers, 237–252. Lambers H, Poorter H. 1992. Inherent variation in growth rate between higher plants : a search for physiological causes and ecological consequences. AdŠances in Ecological Research 23 : 187–261. Lambers H, Posthumus F, Stulen I, Lanting L, van de Dijk SJ, Hofstra R. 1981 a. Energy metabolism of Plantago lanceolata as dependent on the supply of mineral nutrients. Physiologia Plantarum 51 : 85–92. Lambers H, Posthumus F, Stulen I, Lanting L, van de Dijk SJ, Hofstra R. 1981 b. Energy metabolism of Plantago major ssp. major as dependent on the supply of mineral nutrients. Physiologia Plantarum 51 : 245–252. Lascaris D, Deacon JW. 1991. Comparison of methods to assess senescence of the cortex of wheat and tomato roots. Soil Biology and Biochemistry 23 : 979–986.

473

Mattsson M, Johansson E, Lundborg T, Larsson M, Larsson CM. 1991. Nitrogen utilization in N-limited barley during vegetative and generative growth. I. Growth and nitrate uptake kinetics in vegetative cultures grown at different relative addition rates of nitrate-N. Journal of Experimental Botany 42 : 197–205. Mian MAR, Nafziger ED, Kolb FL, Teyker RH. 1994. Root size and distribution of field-grown wheat genotypes. Crop Science 34 : 810–812. Nye PH, Tinker PB. 1977. Solute moŠement in the soil-root system. Oxford : Blackwell Scientific Publications. Oscarson P, Ingemarsson B, Larsson CM. 1989 a. Growth and nitrate uptake properties of plants grown at different relative rates of nitrogen supply. I. Growth of Pisum and Lemna in relation to nitrogen. Plant, Cell and EnŠironment 12 : 779–785. Oscarson P, Ingemarsson B, Larsson CM. 1989 b. Growth and nitrate uptake properties of plants grown at different relative rates of nitrogen supply. II. Activity and affinity of the nitrate uptake system in Pisum and Lemma in relation to nitrogen availability and nitrogen demand. Plant, Cell and EnŠironment 12 : 787–794. Poorter H, Remkes C. 1990. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83 : 553–559. Poorter H, Remkes C, Lambers H. 1990. Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology 94 : 621–627. Reynolds HL, Antonio CD. 1996. The ecological significance of plasticity in root weight ratio in response to nitrogen : opinion. Plant and Soil 185 : 75–97. Robinson D, Linehan DJ, Gordon DC. 1994. Capture of nitrate from soil by wheat in relation to root length, nitrogen inflow and availability. New Phytologist 128 : 297–305. Robinson D, Rorison IH. 1988. Plasticity in grass species in relation to nitrogen supply. Functional Ecology 2 : 249–257. Ryser P, Lambers H. 1995. Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant and Soil 170 : 251–265. Stoskopf NC. 1985. Cereal grain crops. Reston : Reston Publishing Company Inc. Taylor HM. 1974. Root behavior as affected by soil structure and strength. In : Carson, ed. The plant root and its enŠironment. University Press of Virginia, Charlottesville, VA, 271–291. Tennant D. 1975. A test of a modified line intersection method of estimating root length. Journal of Ecology 63 : 995–1001. Van der Werf A, Visser AJ, Schieving F, Lambers H. 1993 a. Evidence for optimal partitioning of biomass and nitrogen at a range of nitrogen availabilities for a fast- and slow-growing species. Functional Ecology 7 : 63–74. Van der Werf A, Enserink T, Smith B, Booij R. 1993 b. Allocation of carbon and nitrogen as a function of the internal nitrogen status of a plant : modelling allocation under non steady-state situations. Plant and Soil 155/156 : 183–186. Veen BW, van Noordwijk M, de Willigen P, Boone FR, Kooistra MJ. 1992. Root-soil contact of maize, as measured by a thin-section technique. III. Effects on shoot growth, nitrate and water uptake efficiency. Plant and Soil 139 : 131–138.