Effects of shading on morphology, physiology and grain yield of winter wheat

Europ. J. Agronomy 33 (2010) 267–275

Contents lists available at ScienceDirect

European Journal of Agronomy journal homepage: www.elsevier.com/locate/eja

Effects of shading on morphology, physiology and grain yield of winter wheat Huawei Li a , Dong Jiang a,∗ , Bernd Wollenweber b , Tingbo Dai a , Weixing Cao a a Key Laboratory of Crop Physiology and Ecology in Southern China, MOA/Hi-Tech Key Laboratory of Information Agriculture, Jiangsu Province, Nanjing Agricultural University, Nanjing 210095, China b Aarhus University, Department of Genetics and Biotechnology, Research Centre Flakkebjerg, DK 4200 Slagelse, Denmark

a r t i c l e

i n f o

Article history: Received 15 February 2010 Received in revised form 16 July 2010 Accepted 19 July 2010 Keywords: Dry matter redistribution Pigment Photosynthesis Shading Winter wheat Light-use efficiency

a b s t r a c t In a field experiment, winter wheat (Triticum aestivum L.) cultivars Yangmai 158 (YM 158, shading tolerant) and Yangmai 11 (YM 11, shading-sensitive) were subjected to shading between jointing and maturity. Three shading treatments were applied, i.e. 92% (S1), 85% (S2) and 77% (S3) of full radiation (S0, control). Compared with S0, the observed grain yield increased in the S1 and S2 treatments of YM 158 but not in S1 of YM 11. The yield loss of YM 11 was 2.3% and 6.7% in S2 and S3, respectively, and 5.9% in S3 of YM 158, which was much less than the corresponding reduction in radiation. Under the shading treatments applied, leaf area index, length of the peduncle internode, area of the upper leaves and content of pigments increased, which favoured efficient light capture. Shading modified light quality in the canopy as indicated by increases of diffuse- and blue light fractions and a reduction of the red light fraction. Shading also altered light-use efficiency as exemplified by reductions in the chlorophyll a/b ratio and the rate of non-photochemical quenching (NPQ), and by increases in the electron transport rate between PSII and PSI (ETR) and of the quantum yield of PSII (PSII), concomitant with no significant change in the maximum photochemical efficiency of photosystem II under dark-adapted conditions (Fv/Fm). By contrast, photosynthetic carbon-use (Pn) in the flag leaf of both cultivars was reduced in the S3 treatment only. The lower leaves were found to be more tolerant to low radiation than the flag leaf, as in most cases Pn of the third and the penultimate leaves were found to increase under shading treatments. Shading increased the redistribution of dry matter from vegetative organs into grains. The responses of the morphological and physiological traits to shading are discussed in relation to the variations of the resulting grain yield in the contrasting wheat cultivars. © 2010 Elsevier B.V. All rights reserved.

1. Introduction As a consequence of increases in aerosols, air pollutants and population density, dimming or shading (decrease in global radiation, i.e. the sum of the direct solar radiation and the diffuse radiation scattered by the atmosphere) have become major challenges to crop production in many areas of the world (Mu et al., 2010). Studies have shown that between 25◦ N and 45◦ N, global radiation has been reduced by as much as 1.4–2.7% per decade (Stanhill and Cohen, 2001; Forster et al., 2007; Ramanathan and Feng, 2009). The downstream plain of the Yangtze River (15% of the total wheat growing area in China) is a region with large-scale industries and thus high-potential risks of heavy air pollution. It is also one of the most severely dimming affected regions as reductions of more than 6% of radiation per decade have been observed (Chen et al., 2005; Qian et al., 2007).

∗ Corresponding author. Tel.: +86 25 84386575; fax: +86 25 84386575. E-mail address: [email protected] (D. Jiang). 1161-0301/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.eja.2010.07.002

Dimming or shading not only reduce radiation but also increase the fraction of diffuse light (Sinclair et al., 1992; Rochette et al., 1996; Gu et al., 1999; Greenwald et al., 2006) and alter the spectral quality (Grant et al., 1996; Bell et al., 2000). Diffuse light is more efficiently utilized by plants (Sinclair et al., 1992; Rochette et al., 1996; Gu et al., 1999, 2002), and can offset small decreases in direct radiation and actually enhance leaf CO2 uptake, photosynthesis and plant growth (Healey et al., 1998; Gu et al., 1999, 2002; Cohan et al., 2002). Meanwhile, with increasing intensity of shading, the fraction of blue light (400–500 nm) increases while of that of red light (600–700 nm) decreases (Bell et al., 2000), which might affect both physiological parameters (e.g. photosynthesis and chlorophyll synthesis (Blackwell, 1966)) as well as plant morphology (e.g. main culm development (Barnes and Bugbee, 1992), tillers appearance (Casal, 1988) and stomatal conductance (Munzner and Voigt, 1992; Zandomeni and Schopfer, 1993; Furuya et al., 1997)). Changes in radiation influence both photosynthetic light- and carbon-use efficiency, and will ultimately affect total grain yield (Bell et al., 2000; Jiang et al., 2002; Greenwald et al., 2006; Zhang et al., 2007). Shading applied during any developmental stage significantly impairs net photosynthesis in wheat leaves (Wang et al.,

268

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

2003; Mitchell et al., 2006; Acreche et al., 2009; Mu et al., 2010) via changes in the functioning of chloroplasts (Burkey and Wells, 1991) and inhibition of the activity of photosystem II (PSII) (Mu et al., 2010). It has been found that leaf chlorophyll content increases and chlorophyll a/b ratios decrease under these conditions (Zhang et al., 1995; Hikosaka, 1996; Evans and Poorter, 2001; Dai et al., 2009). Thus the proportion of antenna pigments in the light-harvesting complex is increased in order to improve the light-use efficiency of the PSII reaction centres (Dai et al., 2009). However, this strategy is not universal as decreases in chlorophyll content (Mu et al., 2010) and increases in chlorophyll a/b ratios have been found in other varieties (Jiang et al., 2004). It should be noted that canopy photosynthetic rate is considered to be more important than single leaf photosynthesis (Pn) in determining constraints to crop production (Zelitch, 1982). It is interesting that decrease of photosynthetic rate due to shading at the canopy level is less than at the single leaf level (Mu et al., 2010). This could be related to efficient acclimation- and adaptation capacities to different light regimes (Boardman, 1977; Schulze and Caldwell, 1994). For example, longer and thinner plants, increased area of leaf blades, and increased shoot to root ratios have been observed under shading (Pearcy, 2007). In addition, light fractions distribute differently within the plant canopy as the upper sunlit leaves usually receive both diffuse and direct radiation while the lower shaded leaves receive more diffuse light (Spitters et al., 1986). Thus, low light level is common for lower leaves, which are more shade tolerant (Stanhill and Cohen, 2001) and can use diffuse more efficiently than direct irradiance (Gu et al., 1999). For instance, Pn of the lower leaves increased to partially compensate the Pn reductions of the flag leaf, which could account for the slight decrease in canopy photosynthesis in wheat (Mu et al., 2010). In that study, however, no evidences were given to indicate the spatial variations in fractions of diffuse light and light quality in wheat canopy under shading. In our previous experiment (Mu et al., 2010), in which relative heavy shading treatments were applied (22% or 33% of the total radiation), the decrease in grain yield was lower than the reduction in radiation. We then presume that low shading might not reduce or even increase wheat grain yield due to high efficient light capture brought about by the morphological modifications and changes of light fractions. This hypothesis was then tested in a field experiment with much lower shading density treatments than in the previous study (Mu et al., 2010), and with two contrasting winter wheat (Triticum aestivum L.) cultivars differing in shading tolerance. Therefore, the objectives of the present study were: (1) to test the performances of wheat grain yield to different densities of shading, (2) to explore responses of the morphological and physiological traits to shading, and (3) to reveal relationship between grain yield performance and responses of the morphological and physiological traits under low shading density. 2. Materials and methods 2.1. Experimental design The experiment was conducted at the Jiangpu Experimental Station of Nanjing Agricultural University in 2007–2008, Nanjing (32◦ 07 N and 118◦ 62 E), Jiangsu Province, PR China, in a humid, semi-tropical climate. The mean annual temperature is 15 ◦ C with rainfall of about 1000 mm and solar radiation of 4540 MJ m−2 y−1 . The soil contained 1.67 g kg−1 organic matter, 126.8 g kg−1 available N, 119.8 g kg−1 Olsen-P and 108.6 g kg−1 K2 O. Shading tolerant wheat cultivar Yangmai 158 (YM 158) and sensitive cultivar Yangmai 11 (YM 11) were selected (Mu et al., 2010). Yangmai 158 is one of the cross-parents of Yangmai 11 and also the recurrent parent of Yangmai 11. The sowing date was on the 6th of November 2007,

and the emergence took place 1 week later. The seedling density was 160 m−2 with a row space of 25 cm. A dose of 120 kg N ha−1 , 60 kg P2 O5 ha−1 and 120 kg K2 O ha−1 was applied before sowing, and another 120 kg N ha−1 was top-dressed at jointing (26th of March, 2008) following the local wheat management practices. The anthesis and maturity dates were observed on 25th of April and 30th of May 2008, respectively. Different layers of white polyethylene screens were covered on the top of wheat canopy from jointing to maturity to provide three shading treatments, i.e. shading with one, two and three layers of the screen, which blocked about 8% (S1), 15% (S2) and 23% (S3) of the full radiation above the canopy, respectively. No shading was set as the control (S0). The screens were more than 180 cm above the ground to ensure good ventilation and were large enough to fully cover the corresponding shaded plots. The daily maximum, minimum and mean temperature, rainfall and sunshine hours in our experimental location are shown in Fig. 2. The meteorological data was recorded by an automatic weather station (CM10, Campbell Scientific, USA). The experiment was a split-plot design with shading as the main plot and wheat cultivar as subplot and three replicates for each. The size of each plot was 3 m × 4 m. 2.2. Measurements and methods The diurnal temperature in the wheat canopy was recorded hourly at two-thirds of the average canopy height using thermo sensors attached to a HOBO H8 data-logger (Onset Computer Corp., Bourne, USA). The effective accumulated temperature (EAT ≥10 ◦ C) was calculated as the weighted sum of the difference between daily mean temperature and 10 ◦ C from joining to anthesis and from anthesis to maturity stage. In case the daily mean temperature was lower than 10 ◦ C, the EAT was logged as 0 ◦ C day. The ratio of diffuse to total radiation (D/T) was recorded using a Sunscan canopy analysis system (Delta-T Devices Ltd., Cambridge, UK). Light spectra were measured with a four-channel hand-held spectroradiometer (SpectroSense2, Skye Instruments Ltd., Powys, UK), using the standard sensors for blue (B, 400–500 nm), green (G, 500–600 nm) and red light (R, 600–700 nm). Photosynthetic active radiation (PAR, 400–700 nm) was also recorded. The proportions of blue (B/PAR), red (R/PAR) and green light (G/PAR) were calculated. All measurements of D/T and the light spectra were taken between 10 and 20 DAA and between 9:30 and 11:00 am on a clear day. Each plot was divided into two blocks, one for sampling and major measurements while another for grain yield determination. Uniform tillers flowering on the same day were tagged for sampling and measurements of single leaf Pn and chlorophyll fluorescence parameters (CFP). Net photosynthetic rate (Pn) and leaf chlorophyll (Chl) fluorescence parameters (CFP) of the top three leaves were measured at 9:30–11:00 with a 10 day interval from anthesis according to Mu et al. (2010). Twenty tagged stems were harvested and separated into flag leaves, penultimate leaves and the rest of the leaves fraction, and the corresponding internodes. The length of each internode and area of each leaf were measured. Half of the samples were then dried at 80 ◦ C until constant weight in order to get dry masses of leaves and of internodes. The top three leaves from another batch of stems were detached and frozen in liquid N for at least 2 h and then stored at −40 ◦ C until analysis of chlorophyll concentration. Thirty spikes were harvested at maturity to record kernel-numbers per spike and 1000-kernel weight. At harvest, numbers of spikes of 4 m2 in the centre of the block for final yield recording in each plot were counted to record spike number per hectare and then harvested to get final grain yield. Any shrivelled grains were ignored. Half gram of fresh cut leaf was weighted, and then incubated in 25 ml of extraction solution containing an equal volume of ace-

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

269

tone and anhydrous ethanol. After complete extraction in the dark, leaf pigments (Chl a/b) were colorimetrically analyzed according to Arnon (1949). Remobilization of dry matter was calculated according to Tan et al. (2008). Here, the amount of dry matter stored in vegetative material before anthesis of which redistributed into grains during grain filling (RAP, mg stem−1 ) was given as the difference in dry matter weight at anthesis and maturity. Correspondingly, the amount of dry matter stored in vegetative organs after anthesis and then redistributed into grains (APA, mg stem−1 ) was calculated as the difference in maximum dry matter weight after anthesis and that at anthesis. Contribution of RAP to grain dry matter (CRAP, %) was computed as the percentage of RAP to final grain mass at maturity, while contribution of APA to grain dry matter (CAPA, %) was calculated as the percentage of APA to final grain mass. 2.3. Statistics All data were subjected to the one-way analysis of variance (ANOVA), and the Duncan’s Multiple Range Test was used to determine the significance of differences between treatments or between cultivars using the SPSS statistical software (SPSS 10.0). 3. Results 3.1. Changes in temperature and light distribution in wheat canopy under shading Canopy Effective Accumulated Temperature (EAT ≥10 ◦ C) decreased with increasing shading level (Fig. 1D). Compared with the control (S0), EAT from joining to anthesis was 3.88, 6.56 and 9.32 ◦ C day lower, while EAT from anthesis to maturity was 6.19, 18.04 and 28.83 ◦ C day lower under S1, S2 and S3, respectively. However, the temperature variation between treatments in the daytime was more significantly than EAT, especially between 6:00 am and 18:00 pm (Fig. 1E). The maximum difference in canopy temperature between the shading and the control treatments during grain filling occurred at 14:00 pm and reached 2.49, 2.73 and 3.30 ◦ C under S1, S2 and S3 at 10 days after anthesis (DAA), respectively (Fig. 1E). PAR above and in the canopy decreased while the ratio of diffusion to total radiation (D/T) increased under shading, as compared to the control (Table 1). Compared with S0, the D/T ratio above the canopy increased by 1.0%, 3.0% and 4.5%, increased by 1.2%, 3.1% and 4.9% at 40 cm from the top of the canopy, and increased by 1.9%, 3.6% and 5.4% at the bottom level, in the shading treatments (S1, S2, S3).

Fig. 1. Climate data during the experimental period.

The fraction of the visible light changed in the shading treatments. Generally, the blue light fraction increased and the red fraction decreased (Table 1), while the green fraction did not change significantly. UV-A and UV-B intensity above the canopy were not affected by shading. However, shading reduced UV-A intensities at the bottom of the canopy and UV-B within the canopy. Together with decreasing PAR from the top to the bottom of the canopy, the D/T ratio and the fraction of blue light (B/PAR) increased while the fractions of red light (R/PAR) decreased.

Table 1 Light quantity and quality under each treatment. Leaf layer

Treatment

D/T (%)

PAR

B/PAR (%)

R/PAR (%)

G/PAR (%)

UV-A (watt)

UV-B (watt)

Surface layer

S0 S1 S2 S3

41.1 d 42.1 c 44.1 b 45.6 a

1431 a 1312 b 1226 c 1104 d

24.4 b 24.6 a 24.8 a 24.9 a

34.3 a 34.2 a 34.1 b 34.0 b

36.8 a 36.8 a 36.6 a 36.7 a

16.6 a 16.7 a 16.2 a 16.1 a

1.31 a 1.30 a 1.25 a 1.31 a

40 cm from surface

S0 S1 S2 S3

42.3 d 43.5 c 45.4 b 47.2 a

911 a 828 b 759 c 682 d

25.0 d 25.4 c 26.0 b 26.8 a

33.5 a 33.4 a 32.8 b 32.1 c

35.8 a 35.7 a 35.7 a 35.7 a

8.1 a 8.1 a 8.0 a 8.0 a

0.62 a 0.59 a 0.52 b 0.44 c

Bottom layer

S0 S1 S2 S3

43.4 d 45.3 c 47.1 b 48.8 a

511 a 455 b 420 c 346 d

27.0 c 27.5 b 28.2 a 28.6 a

31.6 a 31.5 a 30.8 b 30.2 c

34.2 a 34.2 a 34.2 a 34.3 a

5.5 a 4.2 b 3.5 c 3.0 c

0.31 a 0.24 b 0.22 b 0.19 b

Note: S0 refers to the ‘no shading’ treatment (control), S1, S2 and S3 refer to shading of 8%, 15% and 23% of the incident solar radiation, respectively. D/T – the radio of diffuse to total radiation (%); PAR – photosynthetically active radiation; B – blue light (␮mol m−2 s−1 ); R – red light (␮mol m−2 s−1 ); UV-A and UV-B refer to UV-A and UV-B light (watt), respectively. The data were recorded at 10 days after anthesis of the 2007–2008 growing season. Data are means of three replicates. Different letters in each row for each layer indicate significant differences at P < 0.05 analyzed by Duncan’s multiple range test.

270

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

Fig. 3. Effect of shading on photosynthesis of the top three leaves of wheat. Fig. 2. Ratios of chlorophyll a, b and chlorophyll a/b under the shading treatments to the control in the top three leaves of wheat cultivars at 10 days after anthesis.

3.2. Pigment content Shading enhanced the pigment content in the uppermost three leaves by increasing the contents of chlorophyll a (Chl a) and Chl b, especially in the S3 treatment (Fig. 2). However, the ratio of Chl a/b under the shading treatments to that under the control was lower than 1, and decreased with increasing shading intensity. This indicated that shading reduced Chl a/b, and that the increase of Chl b content due to shading was higher than the Chl a content. The pigment content and Chl a/b in the penultimate and the third leaves showed similar patterns to the flag leaf and the increases in Chl b contents there were even higher than in the flag leaf (Fig. 2). 3.3. Net photosynthetic rate (Pn) The responses of Pn to shading differed between leaf positions and between cultivars (Fig. 3). Before 20 DAA, Pn in the flag leaf of YM 158 of the control was lower than in S1 and S2, and higher than in S3. In the flag leaf of YM 11, Pn of S0 was lower than S1 and higher than in the S3 treatment. At 10 DAA, Pn of the flag leaf under S1 and S2 was about 1.37 and 1.79 ␮mol CO2 m−2 s−1 higher than in S0 of YM 158, and 1.11 ␮mol CO2 m−2 s−1 higher under S1 than S0 in Y11. In addition, Pn in flag leaves in both YM 158 and Y11 decreased in S3 compared to S0. At 10 DAA, Pn in the penultimate leaf in S1 and S2 treatments were higher than the control and in S3, and was lowest in S0 at 20 DAA. Pn of the third leaf was increased by the shading treatments.

During the last 10 functional days (20–30 DAA for flag leaf, and 10–20 DAA for penultimate and the third leaf), Pn of the top three leaves dropped rapidly. However, the decline was much slower under shading conditions than in the control. As a result, Pn was the highest in S3, compared to S2 and S1, and was lowest in S0, indicating that shading potentially prolonged the functional duration of the uppermost three leaves. 3.4. Chlorophyll fluorescence parameters of the top three leaves In both cultivars, no significant differences in the maximum quantum yield of the PSII (Fv/Fm) between the shading and the non-shading treatments were found (Table 2). In YM 158, Fv/Fm of the penultimate and the third leaves was much higher in S3 than in the other treatments, while in YM 11 Fv/Fm was much higher in S2 and S3 than in S1 and S0. Thus, shading did not affect Fv/Fm in the flag leaf, and even improved Fv/Fm in the penultimate and third leaves in order to keep higher photochemical turnover efficiency and to make full use of the absorbed irradiance. In both cultivars, the actual photochemical efficiency (PSII) of the top three leaves increased along with increasing shading intensity. The electron transport rate (ETR) between PSII and PSI in the uppermost three leaves increased with shading, indicating a more efficient use of the limited excited light energy under these conditions. In the flag leaf of YM 158, non-photochemical quenching of Chl fluorescence (NPQ) was much lower in S3 than in the other treatments, and decreased with increasing shading intensity in YM 11. In both cultivars, NPQ of the penultimate and of the third leaves decreased with increasing shading intensities. Thus, less absorbed light energy

Table 2 Effects of shading on chlorophyll fluorescence parameters of the top three leaves. Leaf position

Treatment

Yangmai 158

Yangmai 11

Fv/Fm

PSII

ERT

NPQ

Fv/Fm

PSII

ERT

NPQ

Flag leaf

S0 S1 S2 S3

0.832 a 0.834 a 0.833 a 0.830 a

0.57 c 0.59 b 0.59 b 0.61 a

1.16 d 1.33 c 1.77 b 2.94 a

0.23 a 0.22 a 0.22 a 0.15 b

0.832 a 0.832 a 0.835 a 0.832 a

0.57 b 0.57 b 0.58 a 0.59 a

1.51 d 1.86 c 2.45 b 2.52 a

0.24 a 0.22 b 0.22 b 0.16 c

Penult leaf

S0 S1 S2 S3

0.819 b 0.819 b 0.817 b 0.827 a

0.50 c 0.52 b 0.52 b 0.54 a

1.18 d 1.36 c 2.24 b 2.74 a

0.38 a 0.27 b 0.26 b 0.29 b

0.817 b 0.820 b 0.827 a 0.824 a

0.47 d 0.49 c 0.51 b 0.54 a

1.49 d 1.68 c 2.05 b 2.76 a

0.49 a 0.33 b 0.23 c 0.22 c

The third leaf

S0 S1 S2 S3

0.720 b 0.714 b 0.710 b 0.746 a

0.17 b 0.17 b 0.18 b 0.23 a

1.25 d 1.62 c 2.00 b 2.31 a

0.84 a 0.53 b 0.47 c 0.34 d

0.710 b 0.715 b 0.728 a 0.748 a

0.17 b 0.17 b 0.18 b 0.19 a

1.05 d 1.87 c 1.94 b 2.35 a

0.80 a 0.70 b 0.49 c 0.35 d

Note: S0 refers to the ‘no shading’ treatment; S1, S2 and S3 refer to shading of 8%, 15% and 23% of the incident solar radiation, respectively. Fv/Fm, PSII indicate the maximum quantum yield of PSII and the actual photochemical efficiency, ETR and NPQ indicate the electron transport rate and non-photochemical quenching of chlorophyll fluorescence. Data are means of three replicates. Different letters in each row for each leaf indicate significant differences at P < 0.05 as analyzed by the Duncan’s multiple range test.

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

271

158 could contribute to effective interception of the limited light available as compared to the YM 11 cultivar. Single leaf weight (SLW) of the flag and penultimate leaves of YM 158 and of the flag leaf of YM 11 was higher in S1 than in S0, S2 and S3, while SLW of all leaves was higher in S0 than in S2 and S3. This could indicate that shading increased single leaf areas and that shading intensities higher than 15% (S2 and S3) could reduce leaf thickness, while a low shading intensity of 8% (S3) could thicken the flag leaf of both cultivars and the penultimate leaf of YM 158. 3.7. Internode length and specific weight

Fig. 4. Effect of shading on leaf area index of wheat at 10 and 30 DAA.

was transferred to the non-photochemical processes in the shading treatments as compared to the control. 3.5. Leaf area index (LAI) LAI increased with increasing shading intensity at both 10 and 30 DAA (Fig. 4). It should be noted that LAI of both the upper and lower leaf layers increased under the shading treatments, as compared to the control. From 10 to 30 DAA, the LAI in all treatments decreased rapidly, and the rate of decline was slower in the shading treatments than in the control. 3.6. Single leaf area and specific leaf weight (SLW) Single leaf areas of the top three leaves increased in the shading treatments (Fig. 5), which was consistent with the response of LAI to shading. Thus, the leaf area increase was highest in the flag leaf, followed by the penultimate leaf and the third leaf (the increase of the flag leaf area in YM 158 was 1.82, 0.54 and 0.43 cm2 in S3, S2 and S1, respectively, while in YM 11 it was only 1.48, 0.30 and 0.05 cm2 , respectively). The enlarged leaf area could allow the wheat canopy to better catch the limited light resources under shading conditions. The larger leaf area increase in the shading tolerant cultivar YM

Internode weight reached the maximum at 20 DAA (data not shown). Shading reduced the maximum weight of all internodes of YM 11, while S1 and S2 increased the maximum weight of the first and penultimate internodes and in YM 158 only S3 reduced the weight of all the internodes (Fig. 5). Compared with the control, the weight of the peduncle and penultimate internode of YM 158 increased in S1 and S2. In S3, the maximum weight of the peduncle and of the penultimate internodes was reduced. Shading significantly lengthened the peduncle internode but did not affect length of the penultimate and the third internode (Fig. 5). Compared with the control, the length of the peduncle internode in YM 158 and in YM 11 increased in S1, S2 and S3. In addition, only S3 resulted in a notable decline in SLW of the first and penultimate internode. Both S2 and S3 reduced SLW of the third internode, while S1 did not affect SLW of the internodes. Overall, severe shading decreased dry mass per unit internode. 3.8. Redistribution of dry matter from leaves and stems into grains Substantial redistribution of dry matter from stems into grains was found in both cultivars (Table 3). The amount of redistributed dry matter from stems into grains increased in S1 and S2 of YM 158 and in S1 of YM 11. This increase was mainly originating from the penultimate internodes under the relative low shading intensities of S1 and S2 (in YM 158) or of S1 (in YM 11). The amount of redistributed dry matter from stems into grain decreased in S3 of YM 158, and in S2 and S3 of YM 11. The contribution of remobilized dry matter to grain mass was found to be higher in S3 in both cultivars. The increment of remobilized dry matter from stems into grains was much higher before anthesis than after anthesis (the contribution of before anthesis increased 4.62% in YM 158 and 1.39% in YM 11), and this increase mainly originated from the lower internodes. This indicated that severe shading promoted the redistribution of stored dry matter from the lower internodes into the grains. S1 and S2 had no significant effects on the amount of redistributed dry matter in leaves, with limited contributions to grain filling. Under the severe shading conditions of S3, the amount of redistributed stored reserves from leaves was reduced. 3.9. Grain yield and harvest index

Fig. 5. Effect of shading on the single leaf weight, leaf area and specific weight, internode weight, length and specific weight at 10 DAA.

The main effects of shading and cultivar on grain yield were found to be highly significant, and the interactions between shading and cultivar were significant (Table 4). In YM 158 the highest grain yield was obtained in the S1 and S2 treatment. In YM 11 the highest yield was obtained in S1, followed by S0 and S2. In both cultivars the lowest yield was found in the S3 treatment. The variation in grain yield in response to shading was mainly ascribed to the changes in thousand-kernel-weight (TKW). TKW of YM 158 was increased in S1 and S2, and significantly reduced in S3. TKW of YM 11 was significantly increased in S1 and reduced in S3. In addition, both spikes per hectare and kernel number per spike were not significantly affected by the main effects of shading, cultivar

272

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

Table 3 Effect of shading on remobilization of dry matter stored in internodes and leaves and its contributions to grains yield. Cultivars

Treatments

Peduncle

Penult internode

Rest internodes

Stem

RAP

APA

Stem

CRAP

CAPA

YM158

S0 S1 S2 S3

208 a 217 a 217 a 190 b

278 b 294 a 303 a 231 c

333 b 326 b 319 c 372 a

820 b 838 a 839 a 794 c

517 b 517 b 516 b 524 a

303 b 321 a 320 a 270 c

42.8 bc 41.2 c 41.2 c 47.5 a

27.0 b 25.4 c 25.8 c 30.6 a

15.8 b 15.8 b 15.4 b 16.9 a

YM11

S0 S1 S2 S3

175 a 173 a 161 b 154 c

268 b 281 a 254 c 192 d

359 b 362 ab 362 ab 374 a

803 b 816 a 777 c 720 d

356 b 366 b 338 b 407 a

447 a 450 a 439 a 313 b

44.8 b 43.1 c 44.3 b 46.4 a

25.5 b 24.5 c 25.0 b 26.9 a

19.4 ab 18.7 b 19.3 ab 19.5 a

Cultivars

Treatments

Flag leaf

Penult leaf

Lower leaves

Leaves

RAP

APA

Leaves

CRAP

CAPA

S1 S2 S3

72 a 72 a 73 a 69 b

53 ab 54 a 54 a 51 b

36 a 35 a 34 ab 33 b

161 a 161 a 162 a 155 c

12.8 a 11.9 b 11.6 b 8.9 c

148 a 149 a 150 a 146 b

8.4 b 7.9 c 8.1 c 9.0 a

0.57 a 0.59 a 0.58 a 0.52 b

7.8 b 7.3 c 7.5 c 8.5 a

S0 S1 S2 S3

71 a 71 a 66 b 61 c

59 a 55 ab 52 b 50 c

35 a 37 a 35 a 32 b

160 a 162 a 153 b 146 c

13.5 a 10.7 b 10.7 b 7.0 d

152 a 152 a 142 b 140 b

8.9 ab 8.5 b 8.7 b 9.5 a

0.57 a 0.57 a 0.61 a 0.45 b

8.3 b 8.0 bc 8.1 bc 9.0 a

YM158

YM11

Redistribution amount of dry matter (mg/stem)

Contribution to grains (%)

Note: S0 refers to the ‘no shading’ treatment, and S1, S2 and S3 refer to shading of 8%, 15% and 23% of the incident solar radiation, respectively. APA and RAP indicate Redistribution Amount of dry matter stored at Pre-anthesis and After anthesis, respectively. CAPA and CRAP indicate contributions of APA and RAP to grains in dry matter content (%), respectively. Data are means of three replicates. For each cultivar, different letters in each row indicate significant differences at P < 0.05 as analyzed by the Duncan’s multiple range test.

Table 4 Shading effects on wheat grain yield and yield components. Cultivars

Treatment

Spikes/ha (104 ha−1 )

Kernels/spike

TKW (g)

Yield (kg ha−1 )

Biomass (kg ha−1 )

HI (%)

YM 158

S0 S1 S2 S3

322 a 316 a 318 a 320 a

45.6 a 44.0 a 43.0 a 43.2 a

45.8 b 46.2 a 46.3 a 42.2 c

5888 b 5997 a 5965 a 5541 c

13846 b 13934 a 13996 a 13337 c

42.6 a 43.0 a 42.6 a 41.6 b

YM 11

S0 S1 S2 S3

323 a 313 a 320 a 323 a

44.6 a 46.1 a 42.1 a 40.8 a

43.1 b 43.3 a 43.1 b 40.7 c

5844 a 5863 a 5711 b 5452 c

13856 a 13897 a 13885 a 12739 b

42.2 a 42.2 a 41.1 b 41.3 b

F value

FS FC FS × C

1.67 2.85 0.06

1.03 0.13 0.34

1.24 1.09 1.33

65.41** 77.93** 3.46*

48.10** 36.89** 0.26

85.39** 93.7** 3.49

Note: S0 refers to the ‘no shading’ treatment, S1, S2 and S3 refer to shading of 8%, 15% and 23% of the incident solar radiation, respectively. TKW – thousand-kernel-weight; HI – harvest index. Data are means of three replicates. For each cultivar, different letters in each row indicate significant differences at P < 0.05 as analyzed by the Duncan’s multiple range test. FS – F value of shading treatment, FC – F value of cultivar, FS × C – F value of interaction of shading by cultivar. * Significant at 5% probability level. ** Significant at 1% probability level.

and their interaction. Biomass and harvest index (HI) were significantly affected by the main effects of both shading and cultivar, but not affected by the interaction of shading and cultivar. In both cultivars, biomass increased significantly in S1 and S2 but decreased in the S3 treatment. In YM 158 there was no significant difference in HI between the S0, S1 and S2 treatments which were higher than in S3. In YM 11, HI was higher in S0 and S1 than in S2 and S3, and the difference in HI was not significant between S0 and S1 or between S2 and S3. In YM 11, HI decreased remarkably in S2 and in S3. 4. Discussion 4.1. Response of grain yield Many studies have shown that shading reduces grain yield (Gill et al., 2009; Mu et al., 2010). Our results indicate that the effect on grain yield is dependent on the level of shading applied and that the effect is also cultivar-dependent. Heavy shading treatments (such as S3 for YM158 or S2 and S3 for YM 11) were found to reduce grain

yield. In contrast, low-intensity shading (such as S1 and S2 for YM 158) increased grain yield. Even under heavy shading of S3, the yield loss was only 5.9% and 6.7% in YM 158 and YM 11, respectively, and under S2 in YM 11 the yield loss was only 2.3%. Thus, the yield losses were much lower than the reduction in radiation (15% in S2 and 23% in S3). This indicated that there must be physiological and morphological compensation effects at both leaf and canopy level to mitigate the adverse effect on grain yield under shading (Mu et al., 2010). In addition, yield reduction was much larger in YM 158 than in YM 11 in S3, and yield was increased in YM 158 while reduced in YM 11 by S2, and in S1 yield increased in YM 158 while was not significantly affected in YM 11. This suggests that YM 11 is more sensitive in responding to shading than YM 158. 4.2. Photosynthesis The response of photosynthesis to shading differs with leaf position, shading intensity and cultivar. Our previous experiment (minimum reduction in radiation of 22%) showed that shading

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

reduced Pn of flag leaf (Mu et al., 2010). In the present study we found that low levels of shading (S1 and S2 for the shading tolerant cultivar YM 158, and S1 for the intolerant YM 11) even increased Pn of the flag leaf, but Pn of flag leaf was decreased when shading exceeded 15% for YM 11 or 23% for YM 158. In accordance with our previous study (Mu et al., 2010), Pn of the penultimate and third leaves increased with increasing shading intensity. Thus, in both YM 158 and in YM 11 under S3, about 61.40% and 47.25% of the reduction in flag leaf Pn was compensated by the increase in Pn of the lower leaves. 4.3. Morphology In order to capture more light under shading conditions, plants are able to increase light interception efficiency by improving canopy size, such as increasing leaf area index (LAI) (Trapani et al., 1992; Cohen et al., 1997), which was also found to occur in our study. In addition, higher tolerance to low light conditions can be achieved by enhanced plasticity of light-harvesting variables (for example of crown morphology and chlorophyll content (Valladares et al., 2002, 2003)). This is supported by our observations in the current study where stems were found to be longer with lower specific internode weight, leaves to be thinner and leaf area to be larger under the applied shading treatments. The increase in length of the peduncle internode was more obvious than the penultimate and the lower internodes. As a result, PAR was intercepted 6.7%, 12.3%, and 17.5% more than the control in S1, S2, and S3, respectively (Table 1). Thus, changed canopy architecture combined with the enlarged leaf area could partially compensate for the reduction in PAR. In addition, the increment in the leaves area and internodes was larger in YM 158 than YM 11 (e.g. the flag leaf area enlarged by 2.01%, 5.15% and 8.61% in YM 158, and 1.95%, 3.12% and 4.57% in YM 11 under S1, S2 and S3, while the lengthened peduncle internode was 2.26%, 5.01% and 5.69% in YM 158%, 1.23%, 2.48% and 3.50% in YM 11, respectively), which indicated that YM 158 has a higher plasticity to cope with shading treatments. 4.4. Light-use efficiency The reduction in PAR via shading was accompanied by an increase in the fraction of diffusion light and by changed spectral fractions (decrease in red light and increase in blue light), which is consistent with other experiments (Bell et al., 2000). Changes in the fractions of the diffusion light and the visible spectra in the canopy could help compensate PAR reduction by improving leaf photosynthesis under shading (Sinclair et al., 1992; Rochette et al., 1996; Gu et al., 1999, 2002). Blue light is reported to improve the formation of the photosynthetic apparatus of chloroplasts (Weston et al., 2000), and is more effective than red light in promoting chlorophyll synthesis (Bach and Krol, 2001). Accelerated CO2 gas exchange, and increased activities of photosynthetic electron transport and of Rubisco by blue light have been reported (Sharkey and Raschke, 1981; Eskins et al., 1991; Talbott et al., 2002). An increase in the photosynthetic pigment content may also contribute to capture and use light more effectively (Possingham and Smith, 1972; Kasemir, 1979; Shaver et al., 2008). Reduction in light intensity and changes in light spectrum under shading have been shown to alter chloroplast ultrastructure and chlorophyll components (Nii and Kuroiwa, 1988; Zhang et al., 1995; Hikosaka, 1996; Evans and Poorter, 2001). In addition, changes of light absorption, electron transport and of the primary light energy conversion in PS II have been reported (Anderson, 1982; Van Rensen and Curwiel, 2000; Govindjee, 2002; Minagawa and Takahashi, 2004). In our study, all shading treatments resulted in an increase in Chl a and Chl b contents (Fig. 3). The increase in Chl b was faster than that of Chl a, resulting in reduced Chl a/b ratios. The increase in Chl

273

b content would improve the proportion of the antenna pigments in light-harvesting complex II, and enable the leaves to effectively catch light, especially the blue light fraction (Zhang et al., 1995; Hikosaka, 1996). Here, the PSII system centre was not essentially damaged, and even became more active in the penultimate and third leaves under shading conditions as exemplified by increased Fv/Fm and PSII. The relative quantity of electrons passing through PSII in darkadapted leaves was improved (as indicated by increased ETR). Low NPQ in shaded leaves indicated that less light energy absorbed by the antenna pigments in PSII was dispersed via heat (Guo et al., 2006). This agreed with the observation in this study that flag leaf Pn was increased in S1 and S2 in the shading tolerant cultivar of YM 158, and that no significant change in shading-sensitive cultivar of YM 11, and that in both cultivars the decrease in flag leaf Pn was slower than the reduction in PAR under severe shading in S3. Due to the larger interception of radiation by the uppermost leaves, only little radiation reached the leaves in the lower canopy with high shading tolerance (Stanhill and Cohen, 2001; Greenwald et al., 2006). This also could help explain the compensation effect of the improved Pn in the penultimate and third leaves in S3 observed in this and our previous studies (Mu et al., 2010). 4.5. Dry matter redistribution Shading improved the redistribution of storage dry matter from vegetative organs into grains (Table 3). It has been demonstrated that grain filling relies on redistributed reserves from vegetative organs after anthesis (Bidinger et al., 1977; Bell and Incoll, 1990; Blum et al., 1994). The same results were obtained in this study. In addition, loss of dry mass from the penultimate and from the lower internodes was larger than from the peduncle internodes, especially under S3 condition. This indicated that shading promoted remobilization of the stored dry matter in the lower internodes. The difference in the net loss of dry matter between the upper internodes and the lower internodes may be ascribed to the change in availability of photo-assimilates (Cruz-Aguado et al., 2000). Pn of the exposed green parts could compensate the depletion of the remobilized dry matter from the peduncle internode. In contrast, losses of dry matter from the penultimate and lower internodes are hardly compensated by photosynthesis of lower leaves, which have much lower photosynthetic activity than the flag leaf (Takahashi and Nakaseko, 1993). Under S1 and S2, gain filling in the shading tolerant cultivar YM 158 depended more on the assimilate supply from photosynthesis after anthesis than sensitive cultivar YM 11. Compared to YM 11, YM 158 could remobilize more dry matter stored in vegetative organs into grains to alleviate the damage of low light when photosynthesis was impaired by shading. 5. Conclusions Consistent with other reports (Gu et al., 2002; Greenwald et al., 2006), relatively low-intensity shading improved growth of winter wheat in our experiment. This could be explained by: (1) the improved capacity of capturing light due to the enlarged canopy size (higher LAI), changed canopy architecture such as lengthened peduncle internode, enlarged and thinned upper leaves, and increased pigment contents; (2) the enhanced use efficiency of the absorbed light due to increase in diffusion radiation and of blue light, increased Chl b content as well as improved PSII activity as indicated by the measured chlorophyll fluorescence parameters; and (3) the enhanced redistribution of dry matter into grains. Even under heavy shading, yield loss was lower than the decline in PAR. This was found to be closely related to the compensation effects described above. The morphological and physiological traits

274

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275

used here could be recommended as useful indicators for breeding the shading tolerant cultivars. YM158 was found to be more tolerant to shading than YM11. Grain yield was higher in YM 158 than YM 11 under all shading treatments. This could be also explained by better light capture and use, and dry matter redistribution from vegetative organs to grains in YM 158 than YM 11. Acknowledgements This study was funded by projects of National Natural Science Foundation of China (30700483 and 30971734), the Natural Science Foundation of Jiangsu Province (BK2008329), and the Specialized Research Fund for the Doctoral Program of Higher Education (20090097110009), the MATS (nycytx-03) and KYZ200915. References ˜ Acreche, M.M., Briceno-Félix, G., Sánchez, J.A.M., Slafer, G.A., 2009. Grain number determination in an old and a modern Mediterranean wheat as affected by preanthesis shading. Crop Pasture Sci. 60, 271–279. Anderson, J.M., 1982. The role of chlorophyll–protein complexes in the function and structure of chloroplast thylakoids. Mol. Cell. Biol. 46, 161–172. Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts polyphenoloxidase in Bera vulgaris. Plant Physiol. 24, 1–15. Bach, A., Krol, A., 2001. Effect of light quality on somatic embryogenesis in Hyacinthus orientalis L. ‘Delft’s blue’. Biol. Bull. Poznan 38, 103–107. Barnes, C., Bugbee, B., 1992. Morphological responses of wheat to blue light. Plant Physiol. 139, 339–342. Bell, C.J., Incoll, L.D., 1990. The redistribution of assimilate in field-grown winter wheat. J. Exp. Bot. 41, 949–960. Bell, G.E., Danneberger, T.K., McMahon, M.J., 2000. Spectral irradiance available for turfgrass growth in sun and shade. Crop Sci. 40, 189–195. Bidinger, F., Musgrave, R.B., Fischer, R.A., 1977. Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley. Nature 270, 431–433. Blackwell, M.J., 1966. Radiation meteorology in relation to field work. In: Bainbridge, R., Evans, G.C., Rackham, O. (Eds.), Light as an Ecological Factor. Blackwell Scientific Publ., Oxford, Edinburgh, pp. 17–39. Blum, A., Sinmena, B., Mayer, J., Golan, G., Shpiler, L., 1994. Stem reserve mobilisation supports wheat-grain filling under heat stress. Funct. Plant Biol. 21, 771–781. Boardman, N.K., 1977. Comparative photosynthesis of sun and shade plants. Annu. Rev. Plant Physiol. 28, 355. Burkey, K.O., Wells, R., 1991. Response of soybean photosynthesis and chloroplast membrane function to canopy development and mutual shading. Plant physiol. 97, 245–252. Casal, J.J., 1988. Light quality effects on the appearance of tillers of different order in wheat (Triticum aestivum). Ann. Appl. Biol. 112, 167–173. Chen, H.Z., Shi, G.Y., Zhang, X.Y., Arimoto, R., Zhao, J.Q., Xu, L., Wang, B., Chen, Z.H., 2005. Analysis of 40 years of solar radiation data from China, 1961–2000. Geophys. Res. Lett., 32. Cohan, D.S., Xu, J., Greenwald, R., Bergin, M.H., Chameides, W.L., 2002. Impact of atmospheric aerosol light scattering and absorption on terrestrial net primary productivity. Global Biogeochem. cy., 16. Cohen, S., Moreshet, S., Guillou, L.L., Simon, J.-C., Cohen, M., 1997. Response of citrus trees to modified radiation regime in semi-arid conditions. J. Exp. Bot. 48, 35–44. Cruz-Aguado, J.A., Rodés, R., Pérez, I.P., Dorado, M., 2000. Morphological characteristics and yield components associated with accumulation and loss of dry mass in the internodes of wheat. Field Crops Res. 66, 129–139. Dai, Y., Shen, Z., Liu, Y., Wang, L., Hannaway, D., Lu, H., 2009. Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ. Exp. Bot. 65, 177–182. Eskins, K., Jiang, C.Z., Shibles, R., 1991. Light-quality and irradiance effects on pigments, light-harvesting proteins and Rubisco activity in a chlorophyll- and lightharvesting-dericient soybean mutant. Physiol. Plantarum 83, 47–53. Evans, J.R., Poorter, H., 2001. Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ. 24, 755–767. Forster, P., Ramaswamy, V., Artaxo, P., Berntsen, T., Betts, R., Fahey, D.W., Haywood, J., Lean, J., Lowe, D.C., Myhre, G., Nganga, J., Prinn, R., Raga, G., Schulz, M., van Dorland, R., Bodeker, G., Boucher, O., Collins, W.D., Conway, T.J., Dlugokencky, E., Elkins, J.W., Etheridge, D., Foukal, P., Fraser, P., Geller, M., Joos, F., Keeling, C.D., Kinne, S., Lassey, K., Lohmann, U., Manning, A.C., Montzka, S., Oram, D., O’Shaughnessy, K., Piper, S., Plattner, G.K., Ponater, M., Ramankutty, N., Reid, G., Rind, D., Rosenlof, K., Sausen, R., Schwarzkopf, D., Solanki, S.K., Stenchikov, G., Stuber, N., Takemura, T., Textor, C., Wang, R., Weiss, R., Whorf, T., 2007. Changes in Atmospheric Constituents and in Radiative Forcing. Cambridge University Press, Cambridge, United Kingdom/New York, USA. Furuya, M., Kanno, M., Okamoto, H., Fukuda, S., Wada, M., 1997. Control of mitosis by phytochrome and a blue-light receptor in fern spores. Plant Physiol. 113, 677–683.

Gill, R., Singh, B., Kaur, N., 2009. Productivity and nutrient uptake of newly released wheat varieties at different sowing times under poplar plantation in northwestern India. Agroforest Syst. 76, 579–590. Govindjee, 2002. A role for a light-harvesting antenna complex of photosystem II in 18 photoprotection. Plant Cell 14, 1663–1668. Grant, R.H., Heisler, G.M., Gao, W., 1996. Photosynthetically-active radiation: sky radiance distributions under clear and overcast conditions. Agric. Forest Meteorol. 82, 267–292. Greenwald, R., Bergin, M.H., Xu, J., Cohan, D., Hoogenboom, G., Chameides, W.L., 2006. The influence of aerosols on crop production: a study using the CERES crop model. Agric. Syst. 89, 390–413. Gu, L., Baldocchi, D., Verma, S.B., Black, T.A., Vesala, T., Falge, E.M., Dowty, P.R., 2002. Advantages of diffuse radiation for terrestrial ecosystem productivity. J. Geophys. Res., 107. Gu, L., Fuentes, J.D., Shugart, H.H., Staebler, R.M., Black, T.A., 1999. Responses of net ecosystem exchanges of carbon dioxide to changes in cloudiness: results from two North American deciduous forests. J. Geophys. Res. 104 (31), 421–431, 434. Guo, H.X., Liu, W.Q., Shi, Y.C., 2006. Effects of different nitrogen forms on photosynthetic rate and the chlorophyll fluorescence induction kinetics of flue-cured tobacco. Photosynthetica 44, 140–142. Healey, K.D., Rickert, K.G., Hammer, G.L., Bange, M.P., 1998. Radiation use efficiency increases when the diffuse component of incident radiation is enhanced under shade. Aust. J. Agric. Res. 49, 665–672. Hikosaka, K., 1996. Effects of leaf age,nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Iponioeatricolor Cav.) grown horizontally to avoid mutual shading of leaves. Plant Springer–Verlag 198, 144–150. Jiang, H., Wang, X.H., Deng, Q.Y., Yuan, L.P., Xu, D.Q., 2002. Comparison of some photosynthetic characters between two hybrid rice combinations differing in yield potential. Photosynthetica 40, 133–137. Jiang, Y., Duncan, R.R., Carrow, R.N., 2004. Assessment of low light tolerance of seashore paspalum and bermudagrass. Crop Sci. 44, 587–594. Kasemir, H., 1979. Control of chloroplast formation by light. Cell Biol. Int. Rep. 3, 197–214. Minagawa, J., Takahashi, Y., 2004. Structure, function and assembly of photosystem II and its light-harvesting proteins. Photosynth. Res. 82, 241–263. Mitchell, R., Gibbard, C., Mitchell, V., Lawlor, D., 2006. Effects of shading in different developmental phases on biomass and grain yield of winter wheat at ambient and elevated CO2 . Plant Cell Environ. 19, 615–621. Mu, H., Jiang, D., Wollenweber, B., Dai, T., Jing, Q., Cao, W., 2010. Long-term low radiation decreases leaf photosynthesis, photochemical efficiency and grain yield in winter wheat. J. Agron. Crop Sci. 196, 38–47. Munzner, P., Voigt, J., 1992. Blue light regulation of cell division in chlamydomonas reinhardtii. Plant Physiol. 99, 1370–1375. Nii, N., Kuroiwa, T., 1988. Anatomical changes including chloroplast structure in peach leaves under different light conditions. J. Hortic. Sci. 67, 37–45. Pearcy, R.W., 2007. Responses of plants to heterogeneous light environments. In: Pugnaire, F.I., Valladares, F. (Eds.), Functional Plant Ecology, 2nd ed. CRC, pp. 213–246. Possingham, J.V., Smith, J.W., 1972. Factors affecting chloroplast replication in spinach. J. Exp. Bot. 23, 1050–1059. Qian, Y., Wang, W., Leung, L.R., Kaiser, D.P., 2007. Variability of solar radiation under cloud-free skies in China: the role of aerosols. Geophys. Res. Lett., 34. Ramanathan, V., Feng, Y., 2009. Air pollution, greenhouse gases and climate change: global and regional perspectives. Atmos. Environ. 43, 37–50. Rochette, P., Desjardins, R.L., Pattey, E., Lessard, R., 1996. Instantaneous measurement of radiation and water use efficiencies of a maize crop. J. Agron. 88, 627–635. Schulze, E.D., Caldwell, M.M.E., 1994. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Bjorkman, O., Denmig-Adams, B. (Eds.), Ecophysiology of Photosynthesis. Springer, Berlin, pp. 17–47. Sharkey, T.D., Raschke, K., 1981. Effect of light quality on stomatal opening in leaves of Xanthium strumarium L. Plant Physiol. 68, 1170. Shaver, J.M., Oldenburg, D.J., Bendich, A.J., 2008. The structure of chloroplast DNA molecules and the effects of light on the amount of chloroplast DNA during development in Medicago truncatula. Plant Physiol. 146, 1064– 1074. Sinclair, T.R., Shiraiwa, T., Hammer, G.L., 1992. Variation in crop radiation-use efficiency with increased diffuse radiation. Crop Sci. 32, 1281–1284. Spitters, C.J.T., Toussaint, H.A.J.M., Goudriaan, J., 1986. Separating the diffuse and direct component of global radiation and its implications for modeling canopy photosynthesis Part I. Components of incoming radiation. Agric. Forest Meteorol. 38, 217–229. Stanhill, G., Cohen, S., 2001. Global dimming: a review of the evidence for a widespread and significant reduction in global radiation with discussion of its probable causes and possible agricultural consequences. Agric. Forest Meteorol. 107, 255–278. Takahashi, T., Nakaseko, K., 1993. Varietal difference in morphology and photosynthetically active radiation distribution in spring wheat canopy. Jpn. J. Crop Sci. 62, 554–559. Talbott, L.D., Zhu, J., Han, S.W., Zeiger, E., 2002. Phytochrome and blue light-mediated stomatal opening in the orchid, paphiopedilum. Plant Cell Physiol. 43, 639–646. Tan, W., Liu, J., Dai, T., Jing, Q., Cao, W., Jiang, D., 2008. Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis waterlogging. Photosynthetica 46, 21–27.

H. Li et al. / Europ. J. Agronomy 33 (2010) 267–275 Trapani, N., Hall, A.J., Sadras, V.O., Vilella, F., 1992. Ontogenetic changes in radiation use efficiency of sunflower (Helianthus annuus L.) crops. Field Crops Res. 29, 301–316. Valladares, F., Chico, J., Aranda, I., Balaguer, L., Dizengremel, P., Manrique, E., Dreyer, E., 2002. The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees Struct. Funct. 16, 395–403. Valladares, F., Hernandez, L.G., Dobarro, I., Garcia-Perez, C., Sanz, R., Pugnaire, F.I., 2003. The ratio of leaf to total photosynthetic area influences shade survival and plastic response to light of green-stemmed leguminous shrub Seedlings. Ann. Bot. 91, 577–584. Van Rensen, J.J., Curwiel, V.B., 2000. Multiple functions of photosystem II. Indian J. Biochem. Biophys. 37, 377–382. Wang, Z., Yin, Y., He, M., Zhang, Y., Lu, S., Li, Q., Shi, S., 2003. Allocation of photosynthates and grain growth of two wheat cultivars with different potential grain growth in response to pre- and post-anthesis shading. Crop Sci. 189, 280–285.

275

Weston, E., Thorogood, K., Vinti, G., López-Juez, E., 2000. Light quantity controls leaf-cell and chloroplast development in Arabidopsis thaliana wild type and blue-light-perception mutants. Planta 211, 807–815. Zandomeni, K., Schopfer, P., 1993. Reorientation of microtubules at the outer epidermal wall of maize coleoptiles by phytochrome, blue-light photoreceptor, and auxin. Protoplasma 173, 103–112. Zelitch, I., 1982. The close relationship between net photosynthesis and crop yield. BioScience 32, 796–802. Zhang, C.J., Chu, H.J., Chen, G.X., Shi, D.W., Zuo, M., Wang, J., Lu, C.G., Wang, P., Chen, L., 2007. Photosynthetic and biochemical activities in flag leaves of a newly developed superhigh-yield hybrid rice (Oryza sativa) and its parents during the reproductive stage. J. Plant Res. 120, 209–217. Zhang, H., Sharifi, M.R., Nobel, P.S., 1995. Photosynthetic characteristics of sun versus shade plants of Encelia farinosa as affected by photosynthetic photon flux density, intercellular CO2 concentration, leaf water potential, and leaf temperature. Aust. J. Plant Physiol. 22, 833–842.