Sensitivity of yield and grain nitrogen concentration of wheat, lupin and pea to source reduction during grain filling. A comparative survey under high yielding conditions

Field Crops Research 114 (2009) 233–243

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Sensitivity of yield and grain nitrogen concentration of wheat, lupin and pea to source reduction during grain filling. A comparative survey under high yielding conditions ˜ a a,b, Claudia I. Harcha a,b, Daniel F. Calderini b,* Patricio A. Sandan a b

Graduate School, Faculty of Agricultural Sciences, Universidad Austral de Chile, Chile Institute of Plant Production and Protection, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile

A R T I C L E I N F O

A B S T R A C T

Article history: Received 14 April 2008 Received in revised form 2 August 2009 Accepted 8 August 2009

Several studies have been conducted to evaluate the response of crops, especially temperate cereals, to different source–sink ratios during grain filling. However, there is much less information about temperate legumes and even less work comparing the two. The objective of this study was to evaluate the response of both grain yield and grain nitrogen concentration of wheat (Triticum aestivum L.), narrow-leafed lupin (Lupinus angustifolius L.) and pea (Pisum sativum L.) to similar source reduction during grain filling. Two field experiments were conducted in a high yielding environment of Southern Chile. In experiment 1 wheat and narrow-leafed lupin were grown for two consecutive years. Experiment 2 evaluated wheat and pea on two sowing dates. In both experiments a reduction in the source–sink ratio was imposed by using black nets that intercepted 90% of the incident solar radiation from the commencement of the linear dry matter accumulation to physiological maturity. Grain yield was differentially (p < 0.01) decreased by the source reduction in lupin (98%), wheat (63%) and pea (26%). Given that these experiments were carried out in a high yielding environment, the higher response of wheat relative to previous studies supports the hypothesis that the higher the yield potential, the higher the source sensitivity of this crops during the grain filling period. On the other hand, source reduction positively affected (p < 0.05) grain nitrogen concentration in wheat (66%) and pea (18%) but negatively affected lupin (40%). The higher sensitivity of grain yield compared to that of grain nitrogen yield was the cause of the positive effect of the lower source–sink ratio recorded in wheat and pea. In contrast, source shortage in lupin decreased grain nitrogen concentration probably as result of the quick response of grain growth to source limitation. The contrasting sensitivities of lupin, wheat and pea to source reduction during grain filling prevent us to see grain yield and quality response of these crops as separate groups, i.e. temperate cereals vs. temperate legumes. ß 2009 Elsevier B.V. All rights reserved.

Keywords: Wheat Lupin Pea Grain number Grain weight Grain nitrogen concentration Source–sink ratio

1. Introduction Sensitivity of crops to source–sink manipulations has been investigated to assess clue phenophases for grain number determination (e.g., Fischer, 1975, 1985; Kiniry and Ritchie, 1985; Jiang and Egli, 1993; Cantagallo et al., 2004; Arisnabarreta and Miralles, 2008; Estrada-Campuzano et al., 2008) and to evaluate whether the yield is either source or sink limited after grain setting (Fischer and HilleRisLambers, 1978; Slafer and Savin, 1994; Egli and Bruening, 2001; Cartelle et al., 2006; Calderini et al., 2006; Gambı´n and Borra´s, 2007; Beed et al., 2007). These studies have provided the information necessary to develop conceptual and mathematical models of grain yield

* Corresponding author. Tel.: +56 63 221723; fax: +56 63 221233. E-mail address: [email protected] (D.F. Calderini). 0378-4290/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2009.08.003

determination for different crops, which in turn, created useful tools for increasing both potential and actual yields (see Sadras and Calderini, 2009). Despite the huge gains in scientific knowledge about grain yield determination, the degree of understanding reached among crops is clearly different. Temperate cereals, mainly wheat, have been much more investigated than temperate grain legumes like lupin and pea. This makes it hard to compare yield responses between these crops and to estimate their behaviour in different environments. In the agricultural systems of Southern Chile it is essential to make these types of comparisons considering that wheat is the most sown grain crop and narrow leaf lupin has become increasingly important in the last decade due to its potential as a source of proteins for the salmon industry (ODEPA, 2009). In addition to lupin, pea could also be considered as an alternative crop for plant protein production taking into account its high yield potential in Southern Chile (higher than 7 Mg ha1).

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In determinate crops such as temperate cereals it is generally assumed that grain number and grain weight determination are little overlapped after flowering (see Hay and Kirby, 1991; Slafer and Rawson, 1994), while in semi-determinate and indeterminate species like legumes grain setting is extended beyond flowering (see Slafer et al., 2009). In the last group, basal nodes are already at the pod setting when upper nodes are reaching flowering (lupin: Dracup and Kirby, 1996; pea: Ney and Turc, 1993; Dumoulin et al., 1994; soybean: Munier-Jolain et al., 1993). The corollary of these differences is that grain yield and grain number of legumes could be more sensitive to assimilate availability during the grain filling period than cereals. Despite the importance of this assumption there are no studies comparatively evaluating grain yield responses of wheat, lupin and pea to source–sink reduction in the same experiment. In addition to grain number, the sensitivity of grain weight to the source–sink ratio during the grain filling period is essential for a complete understanding of grain yield constraints. The knowledge of grain weight response to source or sink manipulation during grain filling of both temperate cereals and legumes is still under discussion. Although there is a general agreement that grain wheight of wheat is scarcely limited by the source (Slafer and Savin, 1994; Borra´s et al., 2004; Calderini et al., 2006; Cartelle et al., 2006), the magnitude of the grain weight response to source reduction has shown a wide range, i.e. between 0 and 35% when assimilates were reduced by 70% (Borra´s et al., 2004). On the other hand, grain legumes have been much less investigated than cereals and controversial results have been reported. Munier-Jolain et al. (1998) showed that increases of air CO2 concentration during the grain growth of white lupin (Lupinus albus L.) did not modify grain weight, while Palta and Ludwig (1998) found a grain weight reduction (ca. 38%) when pod number was raised from 20 to 40 pods per plant by applying N6-benzylaminopurine to flowers to ensure pod setting in narrow-leafed lupin. Additional experiments in this crop showed a grain weight response to increased air CO2 concentration during grain filling supporting the hypothesis of source limitation (Palta and Ludwig, 2000). As in lupin, studies carried out in pea have not had conclusive results. Munier-Jolain et al. (1998), found that grain weight was not affected when solar radiation was reduced 70% during grain filling at field conditions, but Lhuillier-Sounde´le´ et al. (1999), reported that grain weight of defoliated plants at the beginning of grain filling was significantly (p < 0.05), though slightly, lower than controls under controlled conditions. Although differences in methodologies used by the authors for reducing the source could be involved in the results, no final conclusions on the response of pea to lower source–sink ratio could be reached from these experiments. In addition to the controversial results found for these crops, little is know about the dynamics of grain weight in response to source reductions. Considering the studies presented above, there are still important gaps in the knowledge necessary to accurately compare the yield responses of temperate cereals and legumes to changes in assimilate availability during grain filling. Moreover, it is important to highlight that most of the studies investigating crop responses to source–sink manipulation were carried out under controlled conditions for lupin (see Palta and Ludwig, 1998, 2000; Munier-Jolain et al., 1998) or at field conditions for wheat and pea but in environments of intermediate yield potential, i.e. wheat yields 8 Mg ha1 (see references in Borra´s et al., 2004) and pea yields ca. 4.5 Mg ha1 (see Munier-Jolain et al., 1998). Consequently, conclusions from these studies cannot be easily extrapolated to the high yielding environments of Southern Chile where grain yield of wheat, lupin and pea can over-yield 10, 9 and 7 Mg ha1, respectively, considering that there is evidence

showing the higher the environmental yield potential the higher the sensitivity of grain yield to source–sink manipulation (Calderini et al., 2006; Beed et al., 2007). The impact of source or sink manipulation during grain filling on grain nitrogen concentration is, in addition to grain yield, essential to attain a clear understanding of crop sensitivity during the grain filling period. A high proportion of nitrogen for growing grains is stored in vegetative tissues before grain filling (Barbottin et al., 2005; Triboı¨ and Triboı¨-Blondel, 2002; Schiltz et al., 2005). Therefore, a higher or lower source–sink ratio during grain filling often has a positive or negative effect on grain nitrogen concentration in both wheat (Ma et al., 1995; Martre et al., 2003) and pea (Lhuillier-Sounde´le´ et al., 1999). The response of grain nitrogen concentration to a similar source or sink manipulation seems to be different for these crops because increases of grain nitrogen concentration between 26 and 65% were recorded when 75% of spikelets were removed in wheat (Ma et al., 1996), while under similar sink reduction (75%), grain nitrogen concentration was increased 17% in pea (Lhuillier-Sounde´le´ et al., 1999). This difference could be intrinsic to the crops regarding that grain nitrogen concentration is crop dependent (Lemaire and Gastal, 2009) or due to the methodological procedures used to evaluate the response of wheat and pea. Source reduction through defoliation often has a negative impact on grain nitrogen concentration because the availability of nitrogen stored in vegetative organs is decreased (Lhuillier-Sounde´le´ et al., 1999). On the other hand, source reduction avoiding organ removal (e.g., by shading) could increase the nitrogen concentration of grains considering that starch and protein deposition in growing grains are independent events (Jenner et al., 1991). To the best of our knowledge, there are no studies comparing the sensitivity of grain nitrogen concentration of wheat and pea to source reduction. In addition, there is no information about lupin in regards to this trait in response to source reduction. Therefore, it is necessary to comparatively assess the response of grain nitrogen concentration among these crops. The aim of this study was to evaluate the sensitivity of grain yield, numerical components and grain nitrogen concentration of wheat, narrow-leafed lupin and pea to source reduction during grain filling in the high yielding environments of Southern Chile. 2. Materials and methods 2.1. Site, experimental design and management Two field experiments were conducted on a Typic Hapludand soil at the Universidad Austral de Chile, Valdivia (398470 S, 738140 W, 19 m a.s.l.), Chile. In both experiments, treatments consisted of (i) two crops and (ii) two source–sink ratios (control and shaded plots during grain filling). Crops in experiment 1 were bread wheat (cv. Otto) and narrow-leafed lupin (cv. Quilinock), while in experiment 2 the crops were bread wheat (the same cultivar as in experiment 1: Otto) and pea (semi-leafless cv. Nitouche). Experiment 1 was carried out during 2 growing seasons, 2004–2005 (Y1) and 2005– 2006 (Y2) and experiment 2 was done on 2 sowing dates (S1 and S2) in 2005–2006. In experiment 1, sowing dates were July 27th and August 25th in Y1 for lupin and wheat, respectively. Sowing dates in Y2, were August 24th for lupin and September 26th for wheat. The differences in sowing dates for the two crops were aimed at overlapping the grain filling periods of lupin and wheat to avoid contrasting environmental conditions during the source–sink treatments considering differences in their cycle lengths. In experiment 2 both wheat and pea were sown on August 24th (S1) and September 29th (S2) during the 2005–2006 growing season. It is important to highlight that the second growing season

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of experiment 1 and the second sowing date of experiment 2 were sown side by side in the experimental field. In addition, sowing dates of wheat in Y2 (experiment 1) and S2 (experiment 2) differed by only 3 days (see above). Treatments were arranged in a split–split–plot design in both experiments, where years or sowing dates were assigned to the main plots, crops to the sub-plots and source–sink treatments to the sub-sub-plots randomised in three blocks. Plots in experiment 1 consisted of six rows, 2 m long and 0.2 m apart for wheat. Similar plots were used for lupin, but the rows were 0.3 m apart. Seed rates were 250 seeds m2 and 50 seeds m2 for wheat and lupin, respectively. Wheat plots were fertilized with 140 kg N ha1, 220 kg P2O5 ha1 and 125 kg K2O ha1 at sowing. At tillering 110 kg N ha1 and 95 kg K2O ha1 were added. Lupin plots were fertilized with 150 kg N ha1, 100 kg P2O5 ha1 and 130 kg K2O ha1 at sowing. At flowering 100 kg N ha1 and 90 kg K2O ha1 were added. In experiment 2, plots consisted of seven rows, 2 m long and 0.2 m apart for both wheat and pea. In this experiment, seed rates were 300 seeds m2 and 120 seeds m2 for wheat and pea, respectively, in S1. In S2, seed rates were 400 seeds m2 and 120 seed m2 for wheat and pea, respectively. Wheat plots were fertilized with 50 kg N ha1, 300 kg P2O5 ha1, and 150 kg K2O ha1 at sowing plus 200 kg N ha1 at tillering. Pea plots were fertilized with phosphorus and potassium at the same rate and time as wheat. In addition, 50 kg N ha1 and 250 kg N ha1 were applied at sowing and at stage 104 (Knott, 1987), respectively. In both experiments legumes were fertilized with nitrogen in order to prevent any negative impact of shading treatments on biological N fixation. Both experiments were surface-irrigated as required depending on rainfall to avoid water shortage until physiological maturity. The experiments were maintained free of biotic stresses. Thus, weeds were periodically removed by hand, while diseases and insects were prevented with the use of fungicides and insecticides at the rates recommended by their manufacturers. 2.2. Shading treatments In both experiments, shading treatments were imposed using black nylon nets intercepting 90% of the incident solar radiation. Nets were suspended 20 cm above the top of the canopy by wooden frames covering the whole plot. Nets have little effect on air temperature as average temperature was less than 1 8C lower in shadow plots than in controls. Shading treatments began 10 days after flowering in wheat and at the beginning of the lineal grain growth of pods 3 and 4 of the main stem inflorescence in lupin and pods of reproductive nodes 3 and 4 in pea. In all crops shading treatments were imposed until harvest. The timing for the beginning of shading treatments was chosen to affect the linear growth phase of wheat grains (Fischer, 1985; Savin and Slafer, 1991), lupin and pea (Munier-Jolain et al., 1998). The start of grain filling in lupin and pea was estimated when water concentration of grains reached values lower than 85%, i.e. when grains start the linear growth phase (see Munier-Jolain et al., 1998). To calculate the relative change of the source due to the shading treatments the methodology proposed by Slafer and Savin (1994) and later by Borra´s et al. (2004) was used. Briefly, this study considered both the fraction of solar radiation intercepted by nets and the proportion of the whole filling period when plants were not shaded. For example, in wheat, if the shading treatment reduced 90% of the incident solar radiation starting this treatment at 19% of the whole grain filling period (measured in thermal time) a real assimilate reduction of 71% (relative change = 90–19) was assumed relative to the control treatment. In the present experiments source reductions across treatments were 71, 71 and 68% for wheat, lupin and pea, respectively.

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2.3. Measurements In both experiments, phenological observations were done weekly. The date of anthesis of wheat was recorded using the decimal code scale proposed by Zadoks et al. (1974). In lupin and pea, flowering dates were recorded according to the scales proposed by Dracup and Kirby (1996) and Knott (1987), respectively. In these crops, anthesis and flowering dates were registered when 50% of the plants reached this stage at each plot. At maturity, grain yield was measured in a 1 m long sample from the central row of plots in both experiments. Spikes and pods were threshed to record the grain yield. All grains were weighed after oven drying for 48 h at 65 8C with an electronic balance (Mettler Toledo XP205DR, Greifensee, Switzerland). In addition, 10 spikes and 10 pods per plot from each pod and node position in lupin and pea, respectively) were harvested at maturity in order to record the final grain weight of wheat at individual positions or average grain weight of each category of pod in lupin and pea. Grains from positions 1, 2, 3, and 4 in wheat, pods 3 and 4 in lupin and nodes 3 and 4 in pea were pooled together to measure grain nitrogen concentration using the Kjeldhal methodology (Humphries, 1956). From anthesis onward in wheat and from the beginning of grain filling in lupin and pea (see Munier-Jolain et al., 1998), grains were sampled twice weekly until final harvest to evaluate the growth of grains. In wheat, grains from each position within the two central spikelets of three spikes were sampled per plot. In lupin, all grains of two pods 3 and 4 were measured, while in pea, all grains of two pods from node 3 and 4 were measured. Grain weight data from anthesis/beginning of grain filling to harvest were used to calculate grain growth rate and grain filling duration using a routine of TBL curve (Jandel Scientific, 1991) to fit bi-linear functions (r2 > 0.80) subject to boundary conditions (Eqs. (1) and (2) with one unknown break point ‘c’). The model consists on the following equations: GW ¼ a þ bx

if ðx  cÞ; and

(1)

GW ¼ a þ bc

if ðx > cÞ

(2)

where GW is grain weight in units of mg, a is the intercept (mg), b is the rate of grain filling (mg grain1 8Cd1), and c is the thermal time from anthesis (8Cd) to physiological maturity (wheat stage 95, Zadoks et al., 1974; lupin stage 57, Dracup and Kirby, 1996; pea stage 209, Knott, 1987). The duration of this phase, in thermal time units, was calculated as the sum of the daily average temperature [(Tmax + Tmin)/2] with a base of 0 8C for all three crops (wheat: Calderini and Reynolds, 2000; lupin: Dracup and Kirby, 1996; pea: Ney et al., 1993). 2.4. Statistical analyses Data were subjected to analysis of variance for split-split-plot designs. Therefore, three sources of error were estimated. Whenever comparisons were made between years or sowing dates in experiments 1 and 2, respectively, Error A (main plot) was used; while when comparisons between crops or between shading treatments, the magnitude of Error B (sub-plot) and C (sub-subplot) were taken into account, respectively. To assess the relationship between traits linear regression analysis was used. 3. Results 3.1. Crop phenology and environmental conditions during the crop cycle in experiments 1 and 2 In experiment 1, lupin showed a longer crop cycle than wheat, both in Y1 and Y2 (Fig. 1), however, the delayed sowing date of

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Fig. 1. Crop phenology of control treatments of wheat, lupin and pea after the 27th of July (the earliest sowing date of the experiments) during years 1 (Y1) and 2 (Y2) in experiment 1 and sowing dates 1 (S1) and 2 (S2) in experiment 2. Bars show the length of each developmental phase: sowing-emergence (dashed bars), emergenceflowering (open bars), flowering-beginning of linear grain filling (dotted bars) and starting of linear grain filling-physiological maturity (closed bars).

wheat allowed the grain filling period of both crops to almost completely overlap in both years facilitating the comparison of their responses to source reduction. In experiment 2, wheat showed the longest crop cycle for both sowing dates (Fig. 1) mainly due to the shorter grain filling period of pea. Despite this difference, the grain filling period in pea and wheat began at similar times (Fig. 1). Climatic conditions in experiment 1 showed that average temperature and solar radiation were higher for wheat than for lupin during the emergence-flowering period in Y1 and Y2 (Table 1); but similar data were recorded for both crops from flowering to physiological maturity (Table 1). In experiment 2, growing conditions at pre- and post-flowering were similar for wheat and pea in S1 and S2. As is shown in Table 1, environmental conditions experienced by the three crops were very similar during the grain filling phase, i.e. when the shading treatments were carried out. 3.2. Grain yield and its components in experiments 1 and 2 As expected, control treatments of wheat and lupin reached high grain yield values in experiment 1 in accordance with the growing conditions referred to in Table 1. Controls of these crops showed similar (p > 0.05) grain yield in Y1 and Y2. Averaged across seasons, grain yield of wheat and lupin were 1134 and 1044 g m2, respectively (Table 2). In both years shading treatments had a notorious impact (p < 0.01) on grain yield of these crops, however,

the sensitivity of wheat and lupin to the source reduction was clearly different as is shown by the interaction (p < 0.05) between crop and shading treatments (Table 2). Under source reduction grain yield of wheat and lupin decreased 64 and 98%, respectively (Table 2). Even though shading treatments were initiated at the beginning of the linear accumulation of grain dry matter, the response of grain yield to source reduction was the consequence of both grain number and grain weight decreases. Grain number was significantly (p < 0.01) reduced in both crops but wheat was much less affected than lupin. Grain number of the former decreased 41% in Y1 while no change (p > 0.10) was found in Y2. On the other hand, grain number of lupin showed the highest sensitivity and similar decreases in both growing seasons (90 and 92% in Y1 and Y2, respectively) (Table 2). In addition to grain number, thousand grain weight (TGW) of wheat and lupin were also sensitive (p < 0.01) to the source manipulation. Similar to grain number, TGW of wheat was less affected (59 and 56% in Y1 and Y2, respectively) than that of lupin (93 and 60% in Y1 and Y2, respectively) (Table 2). In agreement with experiment 1, controls of wheat and pea showed high grain yields in experiment 2. However, across sowing dates grain yield of wheat (1018 g m2) was higher (p < 0.05) than that of pea (782 g m2) (Table 2). As expected, the delay in sowing date decreased (p < 0.05) the grain yield of control treatments of wheat and pea by 10 and 15%, respectively. In addition, no interaction (p > 0.05) was found between crop and sowing date (Table 2). Regarding source–sink treatments, the source reduction affected grain yield of both crops at different magnitudes. Shading treatments reduced grain yield of wheat and pea by 61 and 26%, respectively (Table 2). Consistently, wheat showed similar grain yield reduction in this experiment as that of experiment 1 (64%). The negative effect of source reduction on grain yield found in experiment 2 was also the outcome of lower GN (p < 0.01) and TGW (p < 0.01) showed by the crops (Table 2). In this experiment grain number of wheat decreased 16 and 10% in S1 and S2, respectively, while in pea this trait diminished 21% in S1 but no effect was found in S2. Regarding TGW, this yield component was reduced in wheat by 58 and 54% in S1 and S2, respectively, which are highly consistent with the results recorded in experiment 1. On the other hand, TGW of pea was less sensitive, showing a 13 and 26% reduction in S1 and S2, respectively (Table 2). 3.3. Individual grain weight in experiments 1 and 2 For a better picture of grain weight response to the source–sink treatments grain weight was evaluated at individual positions within the spike of wheat or the canopy of legumes to avoid masked results due to compensations between components. In addition, grain growth dynamics were also assessed.

Table 1 Average maximum (Tmax), minimum (Tmin) and mean (Tmean) temperatures, and photosynthetically active radiation (PAR) during the emergence-flowering and floweringphysiological maturity periods of wheat, lupin and pea during years 1 (Y1) and 2 (Y2) in experiment 1, and sowing dates 1 (S1) and 2 (S2) in experiment 2. Experiment

Year or sowing date

Crop

Phenological period Emergence-flowering

1

2

Flowering-physiological maturity

Tmax (8C)

Tmin (8C)

Tmean (8C)

PAR (MJ m2 d1)

Tmax (8C)

Tmin (8C)

Tmean (8C)

PAR (MJ m2 d1)

Y1

Wheat Lupin

17.3 15.6

7.4 6.4

12.3 11.0

7.3 5.9

21.7 18.7

11.2 13.3

16.5 16.0

11.4 11.1

Y2

Wheat Lupin

18.7 17.3

8.4 6.8

13.6 12.1

8.8 7.1

23.7 23.0

11.1 10.6

17.4 16.8

12.0 11.7

S1

Wheat Pea

17.6 17.3

7.0 6.7

12.3 12.0

7.7 7.4

22.7 21.7

10.6 10.9

16.7 16.3

11.7 11.3

S2

Wheat Pea

18.9 18.9

8.6 8.5

13.8 13.7

9.4 9.3

23.8 22.8

11.1 11.0

17.5 16.9

11.9 12.0

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Table 2 Grain yield (Yield), grain number (GN) and thousand grain weight (TGW) of wheat, lupin and pea in control and shading treatments during years 1 (Y1) and 2 (Y2) in experiment 1, and sowing dates 1 (S1) and 2 (S2) in experiment 2. Year or sowing date

Y1/S1

Y2/S2

Crop

Source–sink treatment

Experiment 1 (wheat and lupin) Yield (g m2)

GN (m2)

Yield (g m2)

GN (m2)

TGW (g)

Wheat

Control Shading

1025 249

22731 13301

45.2 18.6

1071 380

24521 20628

43.6 18.4

Lupin/pea

Control Shading

1146 9

7010 707

162.9 12.2

846 587

3263 2582

260.0 227.0

Wheat

Control Shading

1243 582

31928 33935

39.3 17.1

965 402

27485 24681

35.3 16.2

Lupin/pea

Control Shading S.E.M.a

942 28 54

5772 439 1703

162.6 65.5 5.8

718 570 25

2708 2895 455

265.0 197.0 3.7

Year or sowing (Y) Crop (C) Source–sink (S) YC YS CS YCS a

Experiment 2 (wheat and pea) TGW (g)

n.s. ** ** ** n.s. * n.s.

** ** * ** n.s. * n.s.

n.s. ** ** * * ** n.s.

* n.s. ** n.s. * ** n.s.

** ** ** ** n.s. ** n.s.

* ** ** n.s. n.s. ** *

S.E.M.: standard error of the means; n.s.: not significant; *p < 0.05; **p < 0.01.

were found between these crops. Grains of wheat were more sensitive (58% decrease) than pea grains (15% decrease) under source reduction (Fig. 2 and Table 3). Interestingly, wheat results mimic those found in experiment 1 (Table 2), showing a similar grain weight response across positions for both experiments (62 and 57% decreases in experiments 1 and 2, respectively). Moreover, high consistency between experiments was also found when the impact of the source reduction was assessed for grain position in experiments 2 (decreases by 53, 55, 63 and 62% in G1, G2, G3 and G4, respectively) and 1 (55, 59, 67 and 71% decreases, respectively). In pea, similar responses of grain weight were found between node 3 and 4 (Table 3). As in experiment 1, grain weight of wheat was associated (p < 0.01) with both grain growth rate and grain filling duration (Fig. 3). On the other hand, grain weight determinants were not affected (p > 0.10) by source reduction in pea (Figs. 2 and 3).

In experiment 1, shading treatments significantly (p < 0.01) reduced individual grain weight of wheat and lupin in all evaluated grain positions (Table 3, Fig. 2). In wheat, grain weight across positions decreased 62% (Table 3), which agrees with TGW reduction (58%); while in lupin the effect of shading on individual grains (91% reduction) was similar to the observed values of TGW in Y1 (93%) but higher than in Y2 (60%). Considering grain positions, distal grains of wheat were more sensitive than proximal ones considering that G1, G2, G3 and G4 showed 55, 59, 67 and 71% decreases, respectively (Table 3). In lupin, similar responses were found in grains from pods 3 and 4 (Table 3). The negative effect of shading on the grain weight of wheat and lupin was due to both a lower grain filling rate and a shorter grain filling duration compared to the controls as it is shown in Fig. 2. A similar association was found between final grain weight and: (i) grain filling rate, and (ii) grain filling duration (Fig. 3). These similarities confirm that the source reduction affected both grain weight determinants at similar magnitudes. It is important to emphasize that grain growth of lupin was extremely sensitivity to source reduction considering that the dry matter accumulation of grains ended early after the shading treatment was set (Fig. 2). In experiment 2, the individual grain weight of wheat and pea were significantly (p < 0.01) decreased by the source shortage and individual grain weight responses agreed with TGW decreases in both crops (Tables 2 and 3). On the other hand, clear differences

3.4. Effect of source reduction on grain nitrogen concentration As expected, the crops in both experiments showed contrasting grain nitrogen concentrations (GNC) (Table 4). In experiment 1, GNC of control treatments averaged 2.3 and 5.6% for wheat and lupin, respectively. GNC of these crops was not affected (p > 0.10) by year or year  source–sink interaction. Surprisingly, shading treatments affected (p < 0.01) this quality trait but in opposite

Table 3 Individual grain weight (mg grain1) of wheat, lupin and pea in control and shading treatments during years 1 (Y1) and 2 (Y2) in experiment 1, and sowing dates 1 (S1) and 2 (S2) in experiment 2. Year or sowing date

Source–sink treatment

Experiment 1

Experiment 2

Wheat

Lupin

Wheat

Pea

G1

G2

G3

G4

Pod 3

Pod 4

G1

G2

G3

G4

Node 3

Node 4

Y1/S1

Control Shading

52.4 23.7

55.2 21.7

49.0 14.3

33.0 7.4

154.5 13.2

156.9 12.5

53.6 23.8

56.7 24.4

50.7 18.6

36.9 13.8

265.1 236.9

263.1 225.5

Y2/S2

Control Shading S.E.M.a

48.4 22.1 1.2

52.1 22.4 1.2

44.0 16.3 1.0

32.5 11.8 1.9

187.9 16.6 4.2

182.8 18.3 4.9

47.1 23.6 1.1

51.3 23.8 1.4

44.3 16.9 1.3

35.1 13.4 1.1

283.9 229.7 7.8

275.9 232.2 5.6

n.s. ** n.s.

n.s. ** n.s.

* ** n.s.

n.s. ** n.s.

** ** *

n.s. ** n.s.

n.s. ** n.s.

n.s. ** n.s.

n.s. ** n.s.

n.s. ** n.s.

n.s. ** n.s.

n.s. ** n.s.

Year or sowing (Y) Source–sink (S) YS a

S.E.M.: standard error of the means; n.s.: not significant; *p < 0.05; **p < 0.01.

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Fig. 2. Time course of grain weight after flowering for grain position 2 of wheat, pod 3 of lupin and node 3 of pea in control (open circles) and shading (closed circles) treatments during years 1 (Y1) and 2 (Y2) in experiment 1 and sowing dates 1 (S1) and 2 (S2) in experiment 2. The arrows indicate the beginning of shading treatments. Segments show the standard error of the means, when they are larger than the size of the symbols.

ways for these crops since the GNC of wheat was increased 78% by the source reduction while lupin grains showed a 40% decrease relative to the controls (Table 4). The legume also showed higher (p < 0.01) GNC than the cereal in experiment 2. Control treatments of wheat and pea reached 2.4 and 3.7% GNC, respectively. The GNC of wheat resemble that found in experiment 1, while comparing legumes, lupin achieved higher values than pea (Table 4). The sowing date also affected (p < 0.01) the GNC of crops. Delayed sowing slightly increased this trait but

no interaction (p > 0.1) was found between the sowing date and the shading treatment. More importantly, shading enhanced (p < 0.01) GNC in both crops, but to a different extent (significant shading  crop interaction) in wheat (54%) and pea (18%) (Table 4). Considering that grain nitrogen concentration is the balance between dry matter and nitrogen economies of grains, a comparative analysis of both was accomplished. Shading treatments caused similar relative changes in the grain weight and the grain nitrogen concentration of both wheat and pea. For this

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239

Fig. 3. Relationship between grain weight and grain growth rate (left panels) and grain filling duration (right panels) of wheat and lupin (experiment 1) and wheat and pea (experiment 2) in control (open symbols) and shading (closed symbols) treatments. Data included grain weight at different grain position of wheat, lupin and pea.

reason, the relative changes of grain weight and grain nitrogen concentration were compared in experiments 1 and 2 (Fig. 4). Results of these comparisons suggest a concentration of grain nitrogen in wheat and pea. This effect was further confirmed by analyzing the relationships between grain nitrogen yield and grain

yield of crops (Fig. 5). In experiment 1, grain yield of wheat was more sensitive than its nitrogen yield. Averaging across growing seasons, shading treatments reduced grain yield by 63% and nitrogen yield by 35%, while in lupin, these values were both greatly reduced (98 and 99%, respectively) (Fig. 5). In experiment 2,

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240

Table 4 Grain nitrogen concentration in wheat, lupin and pea in control and shading treatments during years 1 (Y1) and 2 (Y2) in experiment 1, and sowing dates 1 (S1) and 2 (S2) in experiment 2. Year or sowing date

Y1/S1

Y2/S2

a

Crop

Source–sink treatment

Grain nitrogen concentration (%) Experiment 1

Experiment 2

Wheat

Control Shading

2.37 4.04

2.21 3.61

Lupin/pea

Control Shading

5.49 3.38

3.48 3.95

Wheat

Control Shading

2.25 4.19

2.63 3.82

Lupin/pea

Control Shading S.E.M.a

5.71 3.38 0.13

3.72 4.59 0.09

Year or sowing (Y) Crop (C) Source–sink (S) YC YS CS YCS

n.s. ** * n.s. n.s. ** n.s.

** ** ** n.s. n.s. ** n.s.

S.E.M.: standard error of the means; n.s.: not significant; *p < 0.05; **p < 0.01.

the shading treatment in wheat decreased grain yield and nitrogen yield by 62 and 41%, respectively, while pea showed decreases of 26 and 12%, respectively (Fig. 5). These responses conclusively support the nitrogen concentration shown for wheat and pea in Fig. 4. 4. Discussion The present study exposed grain filling of wheat, lupin and pea to a severe reduction of incoming solar radiation (90%). However, this does not mean that assimilate availability was reduced by the same magnitude because: (i) shading treatments were imposed after rapid phase of grain growth was started and (ii) previously stored carbohydrates were available to support grain growth (Palta et al., 1994; Takahashi et al., 1994; Beed et al., 2007). According to the quantification of assimilate reduction proposed by Slafer and Savin (1994) and Borra´s et al. (2004), shading treatments assessed in the present experiments reduced assimilates availability by 71,

Fig. 4. Relative changes of grain weight (GW,) and grain nitrogen concentration (GNC) in response to shading treatments in wheat for years 1 (Y1) and 2 (Y2) in experiment 1 and wheat and pea for sowing dates 1 (S1) and 2 (S2) in experiment 2. Dry matter changes where multiplied by 1 in order to make these values positive and benefit from an easier comparison to changes in protein concentration. Segments show the standard error of the means.

71 and 68% for wheat, lupin and pea, respectively. Although these source reductions were clearly high, similar magnitudes were previously evaluated in wheat at lower yielding environments (see Fig. 2 in Borra´s et al., 2004). Equivalent restrictions were also carried out for pea (70% in Munier-Jolain et al., 1998) and soybean (up to 67%, see Fig. 4 in Borra´s et al., 2004) while no data is available for lupin. In the present study, the grain yield response to source reduction was beyond the crop species group (cereal vs. legume crops) as lupin, wheat and pea underwent higher, intermediate and lower yield reductions, respectively. Taking into account that there are no previous studies assessing grain yield sensitivity to shading in lupin, this does not allow us to make unequivocal comparisons with existing literature. However, our results are in agreement with other experiments that show grain yield reduction when pod number was increased, presumably because this crop is highly sensitive to source reduction during grain filling (Palta and Ludwig, 1996, 1998). This is also consistent with the fact that grain yield of lupin is highly sensitive to terminal drought in Mediterranean environments (Palta et al., 2004). On the other hand, in wheat, decreases of grain yield between 20 and 30% were recorded under shading treatments of 50% from anthesis to physiological maturity (Fischer, 1975; Caldiz and Sarando´n, 1988; Savin and Slafer, 1991) or even at higher shading levels: 68% for a shorter period, i.e. from 14 days after anthesis until maturity (Beed et al., 2007). These previous results showed lower responses than those found in our experiments (63% decrease). The stronger source reduction assessed and the higher yield potential environment (>10 Mg ha1) under which the present study was carried out could explain these differences. Contrary to lupin and wheat, pea showed a small yield decrease (26%) considering the source reduction (68%). This agrees with a previous study accomplished in a lower yielding environment (Munier-Jolain et al., 1998) where grain yield decreased by 20% in response to shading (70%) during grain filling. Grain yield reductions reported here were the consequences of lower grain number and/or grain weight depending on the crop. The setting of grain number of lupin was extremely sensitive to shading during grain filling (see Table 2). Previous studies have also shown that grain setting of this crop is highly sensitive to growing conditions after flowering (Palta and Ludwig, 1996, 1998; Palta et al., 2004), most likely due to the high dependence of this crop on current photosynthesis during grain filling (Pate et al., 1998); the abrupt stop of grain growth shown in Fig. 2 supports this hypothesis. In contrast with lupin, grain number of wheat was less decreased (15% averaged across experiments) as a result of source reduction (Table 2). Previous reports found grain number reduction between 8 and 18% when assimilate availability was decreased to a lower extent (shading by 50%) from anthesis to physiological maturity (Fischer, 1975; Caldiz and Sarando´n, 1988; Savin and Slafer, 1991). Even though the shading treatments were imposed 10 days after anthesis in our experiments, i.e. when grains were already in the linear phase of dry matter accumulation (see Fig. 2), results suggest that at a very high source reduction the period of grain number determination could be longer than usually accepted (Fischer, 1985; Savin and Slafer, 1991; Ortiz-Monasterio et al., 1994; Abbate et al., 1995, 1997). Pea showed a similar grain number decrease when compared to wheat in S1 (21%), however, no effect of source reduction was found in S2. Munier-Jolain et al. (1998), showed similar grain number reduction (22%) when they shaded (70%) pea during grain filling under field conditions (Munier-Jolain et al., 1998). Although evolutionary and agronomic selection of small grain cereals and legumes led to a highly plastic grain number and a narrow range of grain weight (Sadras, 2007), clear differences in grain weight responses to source–sink manipulation during grain

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241

Fig. 5. Relationship between grain nitrogen yield and grain yield of control (open symbols) and shading (closed symbols) treatments of wheat (squares) and lupin (circles) in experiment 1 and wheat (squares) and pea (triangles) in experiment 2. Lines represent constant grain nitrogen concentration of 2.3% and 5.6% for wheat and lupin, respectively in experiment 1, and 2.4 and 3.6%, for wheat and pea, respectively in experiment 2.

filling exist both among and within crops (Borra´s et al., 2004). The impact of source reduction on grain weight of wheat was evaluated in Fig. 6A by comparing data from experiments 1 and 2 with data from previous studies analyzed by Borra´s et al. (2004). Regarding the lack of evaluations of lupin and pea, data from experiments 1 and 2 are compared in Fig. 6B with available information of the most studied grain legume, i.e. soybean. Grain weight of lupin was greatly decreased by the source reduction when compared to wheat, pea and even soybean (Fig. 6A and B). This therefore confirms that lupin is very sensitive to large reductions of current photosynthesis; at least, at the beginning of the grain filling period. This is also supported by the fact that grain growth stopped soon after nets were set above the plots (Fig. 2) even though the grain number was reduced. The high sensitivity of lupin found in the present study agrees with the experiment carried out by Palta and Ludwig (2000) where air CO2 was raised from 350 to 700 cm3 m3 during the grain filling period of narrowleafed lupin and yield was increased between 44 and 66%. On the other hand, Munier-Jolain et al. (1998) did not find a grain weight response to CO2 increase from 350 to 850 cm3 m3 in white lupin. In addition to species differences (narrow-leafed and white lupin), two reasons could be considered for the different responses of

lupin to CO2 increase: (i) plants were exposed to higher CO2 for only one week in the Munier-Jolain et al. (1998) experiment while, Palta and Ludwig (2000) enhanced CO2 concentration for 10 weeks and (ii) the sink size of evaluated plants: ca. 43 and 130 grains per plant in the experiment by Munier-Jolain et al. (1998) and Palta and Ludwig (2000), respectively. In experiment 1, grain number of the control treatment was closer (ca. 127 grains per plant) to that reported by Palta and Ludwig (2000) than that reached in the study by Munier-Jolain et al. (1998). Thus, in accordance with both Palta and Ludwig (2000) and our results, the increase of sink size of lupin seems to be useless without a previous enlargement of the source. In wheat, both thousand grain weight and individual grain weight were similarly and consistently reduced by the shading treatment across experiments. Notably, the present study increased the range of grain weight response of wheat under equivalent source reduction (i.e. 70%) by almost doubling the highest values found previously, i.e. from 35 to 65% (see Fig. 6A). Although this does not suggest that wheat cultivars are already limited by the source of assimilates, it may indicate that grain weight of wheat could be more sensitive to source reduction than generally accepted in high yielding environments. This hypothesis is reinforced by the fact that greater responses of grain weight have

Fig. 6. Relationship between relative change of grain weight and relative change of assimilate availability during grain filling of wheat (A, closed triangles), lupin (B, closed squares) and pea (B, open triangles) in response to shading treatments recorded in the present study and previous studies reviewed by Borra´s et al. (2004). Data from previous studies correspond to wheat (A, open circles) and soybean (B, open circles). Shaded areas show the range of data explored in previous studies. Closed circles were used to fit solid lines.

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been found when the source–sink ratio was reduced during grain filling under high yield potential environments (Beed et al., 2007). Modern wheat cultivars have shown higher response to source– sink manipulation than older cultivars evaluated at different times (Fischer and HilleRisLambers, 1978; Koshkin and Tararina, 1989; Kruk et al., 1997; A´lvaro et al., 2008), which also reinforces this suggestion. However, genotypic differences in stored and remobilized carbohydrates could also be responsible for the differential sensitivity of grain weight to similar source reduction (see Fig. 6A) since large variability in water-soluble carbohydrates has been found among wheat cultivars and environments (Ruuska et al., 2006). Grain weight of pea was less affected by source reduction than lupin and wheat and similar to the lowest affected responses of soybean (Fig. 6). Thousand grain weight was decreased 19% in agreement with data from specific grain positions (15%). A previous study showed null sensitivity of pea to shading treatments (70%) (Munier-Jolain et al., 1998). In addition, although Lhuillier-Sounde´le´ et al. (1999) reported significant effect under source manipulation during grain filling, the grain weight reduction found by the authors under defoliation treatments was low (9%) in light of the magnitude of source reduction (leaves from the first vegetative node to the second reproductive node were removed). Therefore, pea has consistently shown little response to source reduction even in high yielding environments. The low sensitivity of pea could be due to (i) high photosynthesis efficiency at low irradiation and/or (ii) high ability for storing and remobilizing carbon assimilates to the growing grains. Grain nitrogen concentration of wheat and pea was increased by source reduction in our experiments due to differential effects of shading treatments on dry matter and nitrogen economies. Previous studies evaluating grain nitrogen concentration in response to source reduction by organ removal have negatively affected final GNC (wheat: Mikesell and Paulsen, 1971; pea: Lhuillier-Sounde´le´ et al., 1999). On the other hand, when the source–sink ratio was increased by diminishing sink size GNC was improved (e.g., wheat: Koshkin and Tararina, 1989; Ma et al., 1990, 1995, 1996; Martre et al., 2003; pea: Lhuillier-Sounde´le´ et al., 1999). In our experiments, the enhancement of GNC by shading was mainly due to the effect it had on carbon economy during grain filling. Moreover, the difference in the sensitivity of GNC found between wheat and pea reflects the differential susceptibility of grain dry matter accumulation to shading. These results agree with the general understanding of the negative relationship between grain nitrogen concentration and grain yield of crops (Jenner et al., 1991; Calderini et al., 1995; Triboı¨ et al., 2006; Rotundo and Westgate, 2009). In contrast to wheat and pea, GNC of lupin decreased (49%) in response to shading. It is likely that this decrease was the consequence of the time at which grain growth stopped and the differential download of carbohydrates and nitrogen into the grains, more than a lack of nitrogen availability during grain filling. This is reinforced by the fact that seed coat of lupin, which has a higher relative contribution to final grain weight under source reduction (Lenoble, 1982; Hauksdottir et al., 2002), has low nitrogen concentration: from 0.32 to 0.80% (Hauksdottir et al., 2002). In conclusion, the response of grain yield of lupin, wheat and pea to lower source–sink ratio was clearly different; lupin was the most sensitive, wheat the intermediate and pea the least affected. These yield responses were related to how susceptible grain number and grain weight of the crops were to source reduction. In lupin, grain number and weight were highly and similarly affected, while grain weight was more responsive than grain number to source reduction in wheat. Yield components of pea were less affected compared to wheat. The high reduction of grain yield found in wheat supports the hypothesis that this crop is more

sensitive to lower source–sink ratios under high yielding environments, at least, when the crop is exposed to high source reduction. Contrary to yield response, GNC was increased in wheat and pea because grain yield was more sensitive than grain nitrogen yield to source reduction. More importantly, similar behaviour was found between these crops when relative changes of GNC and grain yield were considered. Source shortage in lupin decreased GNC probably as a result of the high sensitivity of this crop and its quick response to source reduction and the consequent higher contribution of seed coat to the final grain weight. The contrasting responses to source reduction during grain filling showed by lupin, wheat and pea found in the present study prevent to consider the grain yield determination of these crops, as separate groups, i.e. temperate cereals vs. temperate legumes. Acknowledgments We especially thank Dr. Lucas Borra´s (Universidad Nacional de Rosario) for providing the values of wheat and soybean for Fig. 6. We also thank Dr. Jairo Palta (CSIRO Plant Industry) for his helpful comments on an earlier version of this manuscript. We also thank Dr. Mario Mera (INIA, Carillanca) for providing pea seeds and Luis Vargas for his technical assistance. The revision of English usage by Christine Harrower (Universidad Austral de Chile) is highly appreciated. This study was funded by Fundacio´n Andes, Project C-13855 (8), Fortalecimiento de la Docencia e Investigacio´n en ˜ a and C.I. Universidades Regionales competitive grant. P.A. Sandan Harcha held a postgraduate scholarship from Fundacio´n Andes. References Abbate, P.E., Andrade, F.H., Culot, J.P., 1995. The effects of radiation and nitrogen on number of grains in wheat. J. Agric. Sci. 124, 351–360. Abbate, P.E., Andrade, F.H., Culot, J.P., Bindraban, P.S., 1997. Grain yield in wheat: effects of radiation during spike growth period. Field Crops Res. 54, 245–257. A´lvaro, F., Royo, C., Garcı´a del Moral, L.F., Villegas, D., 2008. Grain filling and dry matter translocation responses to source–sink modifications in a historical series of durum wheat. Crop Sci. 48, 1523–1531. Arisnabarreta, S., Miralles, D., 2008. Critical period for grain number establishment of near isogenic lines of two- and six-rowed barley. Field Crops Res. 107, 196– 202. Barbottin, A., Lecomte, C., Bouchard, C., Jeuffroy, M., 2005. Nitrogen remobilization during grain filling in wheat: genotypic and environmental effects. Crop Sci. 45, 1141–1150. Beed, F.D., Paveley, N.D., Sylvester-Bradley, R., 2007. Predictability of wheat growth and yield in light-limited conditions. J. Agric. Sci. 145, 63–79. Borra´s, L., Slafer, G.A., Otegui, M.E., 2004. Seed dry weight response to source-sink manipulations in wheat, maize and soybean: a quantitative reappraisal. Field Crops Res. 86, 131–146. Calderini, D.F., Reynolds, M.P., 2000. Changes in grain weight as a consequence of de-graining treatments at pre- and post-anthesis in synthetic hexaploid lines of wheat. Aust. J. Plant Physiol. 27, 183–191. Calderini, D.F., Reynolds, M.P., Slafer, G.A., 2006. Source-sink effects on grain weight of bread wheat, durum wheat, and triticale at different locations. Aust. J. Agric. Res. 57, 227–233. Calderini, D., Torres-Le´on, S., Slafer, G., 1995. Consequences of wheat breeding on nitrogen and phosphorus yield, grain nitrogen and phosphorus concentration and associated traits. Ann. Bot. 76, 315–322. Caldiz, D., Sarando´n, S., 1988. Influence of shading during different periods upon ear development, grain yield and its components in two wheat cultivars. Agronomie 8, 327–332. Cantagallo, J.E., Medan, D., Hall, A.J., 2004. Grain number in sunflower as affected by shading during floret growth, anthesis and grain setting. Field Crops Res. 85, 191–202. Cartelle, J., Pedro´, A., Savin, R., Slafer, G., 2006. Grain weight responses to postanthesis spikelet-trimming in an old and a modern wheat under Mediterranean conditions. Eur. J. Agron. 25, 365–371. Dracup, M., Kirby, E.J.M., 1996. Lupin Development Guide. University of Western Australia, Australia. Dumoulin, V., Ney, B., Ete´ve´, G., 1994. Variability of seed and plant development in pea. Crop Sci. 34, 992–998. Egli, D.B., Bruening, W.P., 2001. Source-sink relationships, seed sucrose levels and seed growth rates in soybean. Ann. Bot. 88, 235–242. Estrada-Campuzano, G., Miralles, D., Slafer, G., 2008. Yield determination in triticale as affected by radiation in different development phases. Eur. J. Agron. 28, 597– 605.

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