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CROP PHYSIOLOGY & METABOLISM

Influence of Nitrogen Availability on Seed Nitrogen Accumulation in Pea

^a Laboratoire d'Agronomie, INRA INAP-G, F-78850 Thiverval-Grignon, France

munierjo{at}dijon.inra.fr

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion REFERENCES

 
The final seed nitrogen concentration (the ratio of seed N and dry matter content) is highly variable in pea (Pisum sativum L.) and N remobilization during seed filling may limit yield by restricting the seed filling period. This study was conducted to determine how seed N accumulation is regulated in pea. The effect of N availability and distribution on individual seed N accumulation rate at different nodes was investigated in three genotypes grown in the field and glasshouse under various levels of N fertilizer, depodding, and defoliation. The N content of vegetative plants parts (stems, leaves, podwalls) and seeds from three mainstem nodes were regularly recorded. Plant N available to the seeds at a given time was assessed as the sum of the amount of N still available for remobilization in vegetative parts and the amount of N accumulated by the plant. The results indicate that the N available in a plant at a given time can be considered as one common pool accessible to all seeds and equitably divided among them. Thus, the rate of individual seed N accumulation was unaffected by intra-plant position of seeds. This rate increased with the amount of N available per seed until a maximum rate of individual seed N accumulation (43 µg seed^-1 degree-day^-1) was reached. The relationship established between the rate of individual seed N accumulation and the plant N available per seed will be useful to improve models simulating yield and final seed N concentration in legumes.

Abbreviations: BSL, beginning of seed filling at the last reproductive node • DW, dry weight • NA, amount of nitrogen available to seeds • NAS, nitrogen available per seed • Nremob • amount of remobilizable nitrogen • Nveg, nitrogen content in vegetative parts • SNR, individual seed nitrogen accumulation rate

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion REFERENCES

 
THE SEED NITROGEN CONCENTRATION of pea varies greatly with environment (Karjalainen and Kortet, 1987). Several studies on different species have shown that changes in assimilate availability during the filling period lead to changes in the seed N concentration. Nitrogen stresses during seed filling caused a decrease in seed N concentration (Streeter, 1978 with soybean [Glycine max (L.) Merrill]; Holl and Vose, 1980 with pea); enhancing assimilate availability after the beginning of the filling period by seed removal led to an increase in seed N concentration [Jones and Simmons, 1983 with maize (Zea mays L.)]. This variability in seed N concentration may play an important role in the determination of seed yield because legume plants are characterized by massive nitrogen remobilization from vegetative parts to provide N to the growing seed (Sinclair and de Wit, 1975, 1976; Pate, 1985). Since the loss of N from vegetative parts causes a decrease in plant photosynthetic capacity (Sinclair and Horie, 1989), the plant senesces and the premature termination of seed filling can limit yield.

At each nodal position, the changes in seed N concentration during seed filling can be analyzed as the ratio of the seed N accumulation rate and the seed growth rate. Changes in the assimilate availability at the time when seed number cannot be altered have no effect on seed growth rate [Jones and Simmons, 1983 with maize; Munier-Jolain et al., 1998 with pea, lupin (Lupinus albus L.), and soybean]. The seed growth rate is related to the cotyledon cell number which is fixed before the beginning of seed filling (Egli et al., 1989; Guldan and Brun, 1985 with soybean; Munier-Jolain and Ney, 1998 with pea and soybean). In contrast, N accumulation of in vitro cultured seed was positively correlated with the medium N concentration (soybean: Hayati et al., 1996; maize: Singletary and Below, 1989). Thus, the variations in seed N concentration during the filling period could be mainly due to changes in the seed N accumulation rate which seems to depend on N assimilate availability.

Pea is an indeterminate plant whose pods and seeds are set on successive reproductive nodes at different heights of the plant. The development of pods from various positions is asynchronous and the seeds from higher pods begin to fill later than seeds from lower pods (Ney and Turc, 1993). This characteristic may lead to variations in the seed N accumulation rate between nodes. As N concentration in vegetative parts increases from the base to the top of the shoot (Lemaire et al., 1991), the amount of N available to the seeds may increase with their nodal position. Thus, the rate of seed N accumulation at a given time may be higher in the upper seeds than in the lower seeds of the plant. Moreover, in legumes, the amount of N available in the vegetative organs decreases during the filling period because plant N₂ fixation decreases after the onset of seed filling (Sparrow et al., 1995), and because remobilization leads to a decrease in the N content in vegetative parts of the plant over time (Warembourg and Fernandez, 1985; Pate, 1985; Peoples and Dalling, 1988). This reduction in N availability is likely to affect the rate of seed N accumulation during the filling period. However, the pattern of N partitioning to seeds growing in pods from various intra-plant positions has not been extensively studied in planta for legume species.

The aim of this study was to investigate how N availability and distribution in a pea plant influence the rate of seed N accumulation by analyzing N accumulation in seeds of different reproductive nodes during the seed filling period.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion REFERENCES

 
Plant Culture and Experimental Treatments
A field experiment was sown on 5 March 1996 on a clayey calcic brown soil (clayey eutric Cambisol). Pea plants were grown in a randomized complete block design with four replications. Each block consisted of six plots of six rows for each experimental treatment. The rows were 11.25 m long and 0.20 m apart. The field received 47 kg P ha^-1, 94 kg K ha^-1, and 17 kg Mg ha^-1 during the autumn preceding the experiments. The field experiment was well irrigated in order to avoid moisture stress. Rhizobium leguminosarum was naturally present in the soil. Different experimental treatments were used in order to manipulate the amount of N available per seed. Three genotypes (`P2', `Frisson', and `Solara') were used. The genotype P2 was sown at 120 plants m^-2 and genotypes Frisson and Solara were sown at 100 plants m^-2. P2 is a non-nodulating mutant isogenic of the cultivar Frisson obtained after chemical mutagenesis (Duc and Messager, 1989). At sowing, either 0 or 25 g N m^-2 as ammonium nitrate were applied to plants of the genotype Frisson. Thus, four experimental treatments were obtained, the genotypes P2, Frisson, and Solara not fertilized with N (treatments P_ON, F_ON, and S_ON respectively) and the genotype Frisson fertilized with N (treatment F_25N).

A glasshouse experiment was sown with the genotype Solara on 24 Dec. 1996 and 260 7-L pots filled with a siliceous sand (particle size of 1- to 2-mm) were used. Eight seeds were sown in each pot and inoculated with Rhizobium leguminosarum. When the fifth leaf was fully expanded, the pots were thinned to four plants per pot and all branches were removed from each plant. The glasshouse temperature was maintained above 5°C during winter and the roof of the glasshouse opened automatically when temperature exceeded 20°C to avoid temperature stress. Nutrient solution (P, K, and micronutrients—B, Co, Cu, Fe, Mn, Mo and Zn) was provided by regular watering of pots. Three depodding and two defoliation treatments were applied to manipulate the seed location, the amount of N available per seed, and the N distribution within plants. In the three depodding treatments, pods were removed from all but two nodes: the first and the second nodes (depodding_1-2, 42 pots), the third and the fourth nodes (depodding_3-4, 38 pots), and the fifth and the sixth nodes (depodding_5-6, 34 pots). For each depodding treatment, pod removal occurred when the seeds at the selected nodes had reached the beginning of seed filling. Two different defoliation treatments were applied on non-depodded plants: the first one (defoliation_veg, 34 pots) consisted of removing the leaves from the first vegetative node to the second reproductive node and the second one (defoliation_rep, 34 pots) consisted of removing the leaves from the third to the last reproductive node. Plants were defoliated when all seeds had begun to fill. Remaining pots were left untreated as control plants. Pots were randomly allocated to depodded, defoliated, or control plants and were arranged in a completely randomized design with four replications (where one pot was a replication).

Measurements
From the middle of the flowering period until maturity, samples were taken three times a week for each treatment by randomly choosing 10 plants per replicate in the field and four pots in the glasshouse. All measurements were applied separately to each replicate of each treatment in the field and glasshouse experiments.

At Each Sampling Date
Seeds at three nodal positions of the mainstem (when they were left on the plant) were collected separately: the first, the third, and the fifth reproductive nodes for genotypes Solara and P2; the first, the fourth, and the seventh for genotype Frisson.

For each seed group, fresh weight and dry weight after oven drying at 85°C for 48 h were measured in order to calculate the seed water concentration. At each of the three nodal positions, the beginning of seed filling and the physiological maturity were determined as times when the water concentration were 850 and 550 g kg^-1 by linear regression between the seed water concentration and the cumulative degree-days during the linear decline of seed water concentration (Ney et al., 1993). The progressions of these reproductive stages along the mainstem were described by linear functions based on cumulative degree-days (Ney and Turc, 1993) to define the dates when depodding and defoliation treatments should be applied. The date of the beginning of seed filling at the last reproductive node was determined for each treatment in the field experiment and for the control in the glasshouse experiment.

Seeds of each node group (Nodes 1, 3, and 5 for P2 and Solara; Nodes 1, 4, and 7 for Frisson) were ground and N concentrations were determined by Kjeldahl procedure (Lepo and Ferrenbach, 1987). Individual seed N content at each node was calculated as the multiplication of the seed N concentration and the individual seed dry weight.

The mean rate of individual seed N accumulation at Node 1 was assessed as (i) in the field experiment and for the control in the glasshouse experiment, the amount of N accumulated in a seed during seed filling divided by the degree-days cumulated during the same period, and (ii) for the depodding and defoliation treatments in the glasshouse experiment, the amount of N accumulated in a seed from the treatment date until maturity divided by the degree-days cumulated during the same period.

During the seed filling, the rate of individual seed N accumulation at a given node between two sampling dates (SNR_{n(t to t+1)}) was calculated by dividing the individual seed N accumulation during this period by the cumulative degree-days between the two sampling dates; the data were smoothed by a moving average of three between-sampling date rates of individual seed N accumulation.

Remaining seeds and vegetative tissues—leaves, stems, and podwalls—were collected, weighed after oven drying at 85°C for 48 h, ground, and N concentrations were determined by Kjeldahl procedure (Lepo and Ferrenbach, 1987). Total plant N content was calculated as the sum of all seed N content and vegetative parts N content in order to calculate total plant N accumulation between two sampling dates.

At Maturity
Seeds of each reproductive node of the mainstem and seeds of branches (only in the field experiment) were collected separately and counted. Vegetative tissues—leaves, stems, and podwalls—were collected separately and N concentrations were determined by Kjeldahl procedure (Lepo and Ferrenbach, 1987).

Time was expressed as degree-days cumulated from the beginning of seed filling at the last reproductive node with a 0°C base temperature (Ney and Turc, 1993). Statistical analyses were performed by the GLM and the NLIN procedures of SAS (SAS Institute, 1987). Means were compared by the least significant difference (LSD) at the 0.05 probability level.

Assessment of the Amount of N Available to Seeds
The changes in the amount of N available to seeds were estimated during the seed filling for each treatment in both experiments. The N accumulated in seeds comes from the remobilization of N already in vegetative parts at the beginning of seed filling and from the N currently accumulated by the plant during seed filling (Pate, 1985; Jensen, 1987). According to Caloin and Yu (1984) a proportion of the N in vegetative parts is not available for the remobilization to the seeds because it is associated with structural components. Minimal values of N concentrations of each vegetative organ (leaves, stems, podwalls, and roots) at maturity, similar in different conditions of N starvation, were considered in soybean as the concentrations of non-remobilizable N (Hanway and Weber, 1971; Streeter, 1978; Munier-Jolain et al., 1996). Because roots were shown to provide very little N to seeds (Peoples and Dalling, 1988), root N was neglected in this study. Minimal values of N concentration of leaves, stems, and podwalls in pea at maturity were obtained for the P_ON and S_ON treatments (field experiment). These values were not significantly different between treatments, consequently mean values of non-remobilizable N concentrations were calculated for each vegetative organ analyzed and they were 8.6 g kg^-1 dry matter for leaves, 6.6 g kg^-1 for stems, and 6.2 g kg^-1 for podwalls. These values were consistent with concentrations of non-remobilizable nitrogen observed in soybean for each vegetative organ (Streeter, 1978; Munier-Jolain, 1994) and were consequently used to estimate the amount of shoot N available for remobilization to filling seeds at a Sampling Date t (Nremob_(t)):

where Nveg is the amount of N in the vegetative parts; DW_l, DW_s, and DW_pw are the dry weights of leaves, stems, and podwalls (Munier-Jolain et al., 1996).

The total amount of N available to the seeds between two sampling dates (NA_{(t to t+1)}), presumed to be the sum of the amount of N accumulated by the plant between the two dates and the amount of remobilizable N at the Sampling Date t (Nremob_(t)), was calculated as:

where Ntot is the total amount of N in the plant.

	Results and discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion REFERENCES

 
Variation in N Availability and Mean Rate of Individual Seed N Accumulation
In both field and glasshouse experiments, the seed number per plant and the N content of vegetative plant parts at the beginning of seed filling at the last reproductive node varied widely for the different genotypes (Solara, Frisson, and P2) and treatments (N supply, depodding, and defoliation) (Table 1) . These variations led to a large range of vegetative parts N content per seed (Table 1). The vegetative parts N content per seed varied from 3 mg N seed^-1 for the treatment P_ON (non-nodulating) in the field experiment to 30 mg N seed^-1 for the treatment depodding_5-6 in the glasshouse experiment (Table 1). Moreover, in the glasshouse experiment, the vegetative parts N content per seed was increased and decreased in depodded and defoliated plants compared with the control plants (Table 1). In both field and glasshouse experiments, the mean rate of individual seed N accumulation at the first reproductive node increased with vegetative parts N content per seed, regardless of genotype. This rate varied from 11 µg seed^-1 degree-day^-1 in the lowest vegetative parts N content per seed situation (P_ON) to 38 µg seed^-1 degree-day^-1 in the highest vegetative parts N content per seed situation (depodding_1-2).

Seed N Accumulation at Different Nodes during Seed Filling
For the genotypes Solara and Frisson (F_ON and F_25N treatments) sown in field, the patterns of individual seed N accumulation from the beginning of seed filling at the last reproductive node were similar at the three different nodal positions (Nodes 1, 3, and 5 for Solara and Nodes 1, 4, and 7 for Frisson) (Fig. 1) . Seeds at Node 1 reached maturity earlier than for the other nodes. Consequently, at the maturity date of Node 1, seed N accumulation stopped at Node 1, whereas N was still accumulated at similar rates in the seeds at the two other nodes (Fig. 1).

View larger version (21K): [in this window] [in a new window]   Fig. 1 Individual seed N accumulation at different reproductive nodes from the beginning of seed filling at the last reproductive node (BSL) in the field. FON: Frisson not fertilized with N. F25N: Frisson fertilized with 25 g N m-2. SON: Solara not fertilized with N. Vertical bars are LSD (0.05)

View larger version (24K): [in this window] [in a new window]   Fig. 2 Effect of plant N availability on the individual seed N accumulation at different reproductive nodes from the beginning of seed filling at the last reproductive node (BSL) in glasshouse experiment. Control, control plants; Depodding 1-2, all nodes were depodded except Nodes 1 and 2; Defoliation veg, leaves were removed from the first vegetative node to the second reproductive node. Vertical bars are LSD (0.05)

View larger version (22K): [in this window] [in a new window]   Fig. 3 Effect of plant N distribution on the individual seed N accumulation at different reproductive nodes from the beginning of seed filling at the last reproductive node (BSL) in glasshouse experiment. Defoliation veg, leaves were removed from the first vegetative node to the second reproductive node; Defoliation rep, leaves were removed from the third to the last reproductive node. Vertical bars are LSD (0.05)

Increasing or decreasing N available per seed in the glasshouse experiment enhanced and reduced the rate of individual seed N accumulation at the three different nodal positions analyzed (Fig. 2). However, decreasing N available per seed did not change the relative distribution of N assimilates among seeds of the different nodes. Thus, there could be no clear-cut priority of filling seeds at one nodal position over others regarding N accumulation. Whatever the amount of N available at a given time, it seems to be equitably divided among all filling seeds.

As recently suggested by other reports (Jenner et al., 1991; Hayati et al., 1996), our results show that the rate of seed N accumulation is not directly correlated with individual seed growth rate. The individual seed growth rate can vary between morphological positions (Munier-Jolain and Ney, 1998), but it is not affected by changes in C and N assimilate availability during seed filling (Jones and Simmons, 1983; Munier-Jolain et al., 1998) because this rate depends mainly on the seed cell number (Guldan and Brun, 1985; Munier-Jolain and Ney, 1998). In contrast, the rate of individual seed N accumulation seems to be similar in all filling seeds of a plant at a given time and depends on the pool of N available per seed at a given time. This rate is likely to decrease during the seed filling period because the N available per seed decreases during this period (Warembourg and Fernandez, 1985). Consequently, the mean rate of individual seed N accumulation could be higher for the oldest seeds at the first reproductive nodes than for the youngest seeds at the last reproductive nodes at the top of the plant. This hypothesis could explain the decrease of seed N concentration (the ratio of the individual seed N accumulation rate and the individual seed growth rate) from the oldest reproductive node to the youngest at the top of the plant (Cousin, 1983; Monti 1983).

Relationship between the Rate of Individual Seed N Accumulation and the N Available per Seed at a Given Time
For each experiment (field and glasshouse) and for each treatment, N available per seed between two sampling dates (NAS_{(t to t+1)}) was estimated as the ratio of N available to filling seeds from vegetative parts and current plant N accumulation (NA_{(t to t+1)}) divided by the number of filling seeds at Sampling Date t.

Our results demonstrate that the rate of individual seed N accumulation is unaffected by intra-plant position of seeds. Consequently, the rates of individual seed N accumulation (SNR_{n(t to t+1)} at each analyzed node (Nodes 1, 3, and 5 for P2 and Solara; Nodes 1, 4, and 7 for Frisson) were averaged to assess the rate of individual seed N accumulation between two sampling dates in all filling seeds (SNR_{(t to t+1)}) for each treatment in both experiments.

Regardless of the experiment (field or glasshouse), the genotype (P2, Frisson, or Solara), and the treatment (N supply, depodding, and defoliation), the rate of individual seed N accumulation was related to the N available per seed (Fig. 4) : the rate of individual seed N accumulation increased sharply with N available per seed until a N available per seed of approximately 15 mg N seed^-1. Above this level, the rate of individual seed N accumulation was constant. The data were well fitted (r² = 0.94) by the following equation:

where 43 µg seed^-1 degree-day^-1 can be considered as the maximum rate of individual seed N accumulation.

View larger version (22K): [in this window] [in a new window]   Fig. 4 Relationship between the rate of seed N accumulation at a given time (SNR(t to t+1)) and the plant N availability at a given time (NAS(t to t+1)) for the three genotypes in the field and glasshouse experiments

Seed N accumulation during the filling period is a key feature of models simulating yield establishment in grain legumes (Sinclair and de Wit, 1976; Sinclair, 1986). The loss of nitrogen transferred from leaves to filling seeds has been shown to lead to a decline in leaf photosynthetic capability (Lugg and Sinclair, 1981; Sinclair and Horie, 1989). To simulate this plant "self destruction" process, Sinclair and de Wit (1976) estimated the rate of seed N accumulation by a constant proportion of the seed growth rate, corresponding to an assumed mean N concentration of seeds valid during all the filling period. Our data give evidences against this assumption. These data are consistent with the results obtained in vitro by Hayati et al. (1996), showing that the seed N accumulation rate was independent of the seed growth rate in soybean.

The relationship between the rate of individual seed N accumulation and the N available per seed presented in this study should lead to great improvements in the modeling of N partitioning during seed filling in legume plants. This relationship will be useful to determine the amount of N provided to filling seeds in pea. Thus, the decrease in N content in vegetative plant parts could be better simulated in order to determine the duration of seed filling (Munier-Jolain et al., 1996). This relationship will be also of value for predicting final seed N concentration (the ratio of the seed N accumulation rate and the seed growth rate).

However, this relationship has limitations. Some reports suggest that the processes leading to N assimilate availability to the seeds such as remobilization of N from vegetative parts can be influenced by temperature (Paulsen, 1994) or by diseases (Garry et al., 1996). Thus, the simulation of the seed N accumulation rate during the filling period presented in this study could be further improved by a better understanding of these processes.Holl Vose 1980; SAS Institute 1987

	ACKNOWLEDGMENTS

 
Our grateful thanks are due to the technical assistance of the INRA laboratory and the experimental management staff in Dijon. This work was partly funded by UNIP, Biopôle Végétal de Picardie, SIDO and Conseil Régional de Picardie.

Received for publication December 14, 1998.

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