Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat

CJ-00236; No of Pages 12 TH E C ROP J O U R NA L XX ( 2 0 17 ) XXX–X XX

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Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat☆ Xinglong Dai a,b , Yuechao Wang a,b,c , Xiuchun Dong a,b,d , Taifeng Qian a,b , Lijun Yin a,b , Shuxin Dong a,b , Jinpeng Chu a,b , Mingrong He a,b,⁎ a

State Key Lab of Crop Biology/College of Agronomy, Shandong Agricultural University, Tai'an 271018, Shandong, China Key Lab of Crop Ecophysiology and Farming System, Ministry of Agriculture, Tai'an 271018, Shandong, China c College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China d Jining Agricultural Technology Extension Station, Jining 272037, Shandong, China b

AR TIC LE I N FO

ABS TR ACT

Article history:

Lodging resistance of winter wheat (Triticum aestivum L.) can be increased by late sowing.

Received 16 February 2017

However, whether grain yield and nitrogen use efficiency (NUE) can be maintained with delayed

Received in revised form 25 May 2017

sowing remains unknown. During the 2013–2014 and 2014–2015 growing seasons, two winter

Accepted 9 June 2017

wheat cultivars were sown on three dates (early sowing on October 1, normal sowing on October

Available online xxxx

8, and late sowing on October 15) to investigate the responses of lodging resistance, grain yield, and NUE to sowing date. No significant differences in lodging resistance, grain yield, or NUE

Keywords:

between early and normal sowing were observed. Averaging over the two cultivars and years,

Grain yield

postponing the sowing date significantly increased lodging resistance by 53.6% and 49.6%

Lodging resistance

compared with that following early and normal sowing, respectively. Lodging resistance was

Nitrogen use efficiency

improved mainly through a reduction in the culm height at the center of gravity and an increase

Sowing date

in the tensile strength of the base internode. Late sowing resulted in similar grain yield as well as

Winter wheat

kernel weight and number of kernels per square meter, compared to early and normal sowing. Averaging over the two cultivars and years, delayed sowing resulted in a reduction in nitrogen uptake efficiency (UPE) by 11.0% and 9.9% compared to early and normal sowing, respectively, owing to reduced root length density and dry matter accumulation before anthesis. An average increase in nitrogen utilization efficiency (UTE) of 12.9% and 11.2% compared to early and normal sowing, respectively, was observed with late sowing owing to a reduction in the grain nitrogen concentration. The increase in UTE offset the reduction in UPE, resulting in equal NUEs among all sowing dates. Thus, sowing later than normal could increase lodging resistance while maintaining grain yield and NUE. © 2017 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Abbreviations: AGN, aboveground nitrogen uptake at maturity; CHCG, culm height at the center of gravity; CLRI, culm lodging resistance index; GNC, grain nitrogen concentration; NHI, nitrogen harvest index; NUE, nitrogen use efficiency; RLD, root length density; TFS, tensile failure strength; UPE, nitrogen uptake efficiency; UTE, nitrogen utilization efficiency ☆ Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS. ⁎ Corresponding author at: State Key Lab of Crop Biology/College of Agronomy, Shandong Agricultural University, Tai'an 271018, Shandong, China. E-mail address: [email protected] (M. He).

http://dx.doi.org/10.1016/j.cj.2017.05.003 2214-5141 © 2017 Crop Science Society of China and Institute of Crop Science, CAAS. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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1. Introduction

2. Materials and methods

Lodging [1,2] and decreased nitrogen (N) use efficiency (NUE) [3] are two major limitations in winter wheat (Triticum aestivum L.) production. Lodging, the permanent displacement of stems from the vertical position [1], is responsible for large reductions in grain yield and quality [2,4,5], increases harvesting costs [6], and provides a favorable environment for foliar disease [1], causing potential health risks for humans resulting from increased risk of fungal infection and subsequent development of mycotoxins [7]. Worldwide, excessive N input is responsible for reduced N fertilizer recovery and NUE [3,8]. The loss of N results in both higher production costs and a greater risk of environmental hazards [9,10]. Lodging occurs as a result of the buckling or bending of the culm at the basal stem internodes [1,11], especially at the second base internode [12,13]. Cultural practices (e.g., sowing date, seeding rate), environmental conditions (e.g., occurrence and quantity of rainfall and wind), and plant growth regulators are the main factors that affect lodging in winter wheat [6,11,12,14,15]. The strength of the stem is based on its diameter, wall thickness, and material strength of the stem wall [2]. Seeding rate, sowing date, and their interaction have large effects on grain yield, NUE, and lodging resistance. N uptake is highest with the optimum seeding rate in common wheat [16] or durum wheat (Triticum durum Desf.) [17]. Grain yield and NUE of winter wheat can be simultaneously improved by managing the seeding rate [18,19]. However, increasing the seeding rate makes wheat plants more susceptible to lodging [5,12,20]. Managing the seeding rate and sowing date to improve or maintain lodging resistance without reductions in grain yield and NUE is a major goal of management strategies for wheat research. Because temperatures are increasing worldwide [21], delaying the sowing date may be feasible for wheat. The increased cumulative degree days above 0 °C before wintering [22] may provide a foundation for delaying the current sowing date. Late sowing has been reported to be effective in reducing lodging [20,23,24], and appropriately delaying the sowing date can result in similar grain yields [25–27]. Additionally, late sowing in winter wheat production can allow a timely late harvest of summer maize (Zea mays L.), increasing its yield [28], which is important to total cereal production and food security in China and provides the potential to improve the annual use efficiency of solar radiation, temperature, and moisture [29]. Widdowson et al. [30] reported that late sowing weakened N uptake. Unaffected or increased grain nitrogen concentration (GNC) was reported with late sowing [31–34]. However, few studies have focused on the effects of sowing date with optimum seeding rate on NUE and its two components: nitrogen uptake efficiency (UPE) and nitrogen uptake efficiency (UTE) [3]. The primary objectives of the present study were to determine whether the lodging resistance of winter wheat could be increased and the grain yield and NUE maintained by delaying sowing date. Additionally, changes in morphological and physiological traits associated with lodging resistance and NUE were investigated to explain difference in lodging resistance and NUE variation with different sowing dates.

2.1. Site and growing conditions Field experiments were performed in 2013–2014 and 2014–2015 at the experimental station of Dongwu village, in Dawenkou town, Daiyue district, Tai'an, Shandong, China. Rainfall and temperature data were obtained from a meteorological station located <500 m from the experimental field (Fig. 1). The soil was characterized as sandy loam with a pH of 8.24 [35], and contained 14.51 g kg−1 organic matter (Walkley and Black method) [36], 1.09 g kg−1 total N (semi-micro Kjeldahl method; 8200 Auto Distillation Unit; Kjeltec, Hillerød, Denmark) [37,38], 24.09 mg kg−1 available phosphorus (P; Olsen method) [39], and 40.17 mg kg−1 available potassium (K; Dirks–Sheffer method) [40].

2.2. Experimental design and treatments Two widely planted cultivars, Tainong 18 (a cultivar with large ears and low tillering capacity) and Shannong 15 (a cultivar with middle-sized ears and high tillering capacity), henceforth referred to as T18 and S15, respectively, were selected as the experimental plants. Early, normal, and late sowing were performed on October 1, 8, and 15, respectively. The cumulative degree days above 0 °C before wintering were 100.8 and 124.4 (°C d) higher with early sowing than for the normal sowing date for 2014 and 2015, respectively, and were reduced by 103.9 and 111.7 (°C d) for late sowing in 2014 and 2015, respectively. Taking into consideration the tillering capacity, grain yield, and NUE potential for each cultivar [18], the cultivars T18 and S15 were sown at densities of 405 and 172.5 plants m−2, respectively. Accordingly, the experiments for each cultivar were established separately, in a completely randomized design with three replicates. The size of each subplot was 25.0 m × 3.0 m (12 rows spaced 25 cm apart). The previous crop in the planting areas was summer maize, and all straw and leaves were returned to the soil before tillage in both years. Basal fertilization of each subplot included N as urea, P as calcium superphosphate, and K as potassium chloride at rates of 120 kg ha−1 N, 90 kg ha−1 P2O5, and 90 kg ha−1 K2O, respectively. An additional 120 kg ha−1 N as urea was applied at the beginning of jointing.

2.3. Crop measurement Plant material samples were taken before wintering, jointing, booting, anthesis, and maturity by manually cutting all plants in a quadrat of 50 cm × 6 rows at ground level and mixing them. Before wintering, jointing, and booting, 30 plants were sampled. At anthesis and maturity, 50 single stems were sampled. Plant samples were separated into sheaths and stems, leaves, glumes, and spike rachis and grains. All separated samples were oven-dried at 70 °C to a constant weight to estimate dry matter accumulation. Oven-dried samples were milled and analyzed for N concentration (semi-micro Kjeldahl method) [37,38], and N accumulation was calculated by multiplying the element concentration by dry weight. Quadrats of 2.0 m (parallel to rows) and 1.5 m (perpendicular to rows) were established in both years, and all spikes

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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40

30

30

20

20

10

10

0

0

-10

Rainfall (mm)

Oct.

Nov.

Dec.

Jan.

Feb.

Mar.

Apr.

May

Jun.

72

30

54

20

36

10

18

0

0

Mean temperature (oC)

Rainfall (mm)

Mean temperature

Mean temperature (oC)

Rainfall

-10 Oct.

Nov.

Dec.

Jan.

Feb.

Mar.

Apr.

May

Jun.

Fig. 1 – Rainfall and mean temperature recorded during the winter wheat growth period (October to June) in 2013–2014 (top) and 2014–2015 (bottom).

in the quadrat were cut and threshed with a small-sized seeds threshing machine (QKT-320A, Weihui seed machine manufactory, Henan Province, P.R. China). The grain was air-dried and weighed. The yield was defined as the grain weight with a standard 12% moisture content (88% dry matter, t ha− 1). The available N from the top 1 m of soil [i.e. Nmin (mineralized N in soil, including NO3-N and NH4-N)], which was used to calculate NUE, was tested before sowing each year using a continuous flow analyzer (AA3; Bran Luebbe, Norderstedt, Germany) [41,42]. The Nmin values in the top 1.0 m of the soil profile were 197.97 and 185.03 kg ha−1 in 2013–2014 and 2014–2015, respectively. Root sampling was performed at jointing, anthesis, and grain filling in both seasons. In each treatment, roots were sampled from a selected area of the field covered by a group of plants. The area was 75 cm in length (covering plants in three rows), 40 cm in width, and 160 cm in depth. All of the roots were sorted after washing out of all soil, and root length was evaluated using a Delta-T SCAN Root Analysis System (Delta-T Devices, Ltd., Cambridge, UK), in which the roots were dyed with methyl blue. All of the roots in the top 160 cm were used to calculate root length density (RLD), the root length per unit of soil volume (mm cm−3). Indices associated with culm lodging resistance were measured at mid-grain filling. The first internode of more

than 10 mm originating at or just below the ground surface was defined as internode 1 [43]. Subsequent internodes up the stem were numbered 2, 3, 4, and/or peduncle. The length of each internode was determined from the midpoint of their adjacent nodes, the length of the peduncle was from the uppermost node to the bottom of spike, and plant height was measured from the base of the plant to the tip of spikes excluding awns using metal tape. The culm height at the center of gravity (CHCG; cm) for each culm was measured by cutting off the roots and measuring from the culm base to the point at which the culm remained balanced in a horizontal position when placed on a fulcrum. Measurement of the base stem was performed on the second base internode of each shoot after detachment of the leaves along with the leaf sheath [12]. The tensile failure strength (TFS) (newtons, N) of the internodes was determined by the three-point bending test [43]. The nodes adjacent to the internode were supported and an even pulling pressure was applied at a constant rate at the middle of the internode using a Stem Strength Tester (YYD-1; Zhejiang Top Instrument Co., Ltd., Hangzhou, China). The peak force recorded just before the internode buckled was taken as its TFS. The culm lodging resistance index (CLRI; the TFS per unit CHCG, N m−1), which is an integrated indicator for evaluating wheat culm lodging resistance ability [12] and has been widely used in evaluating the lodging resistance of winter wheat [44,45], was also calculated. The diameter and

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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stem wall thickness were measured using a digital vernier caliper with an accuracy of 0.01 mm and then averaged. Diameter was measured at the middle of the internode. Stem wall thickness was determined by cutting at the center point and averaging the two values of stem wall thickness taken on opposite sides of the stem [11,43]. All separated samples were oven dried at 70 °C to constant weight to estimate dry weight. The internode dry weight per unit length of the internode was defined as the filling degree (mg mm−1).

and normal sowing and increased by one day with late sowing (Table 1). The onset of jointing was also not affected by early and normal sowing, but was delayed by one day with late sowing, while the onsets of booting and anthesis were unaffected by sowing dates in both growing seasons (Table 1). Because the temperatures in June limited further grain filling and accelerated crop maturation, harvest time was the same among the three sowing dates in each year. All treatment groups were harvested on June 12, 2014 and June 9, 2015.

2.4. Calculation of NUE and relative indices 3.2. Effects of sowing date on lodging resistance NUE is defined as the grain dry matter yield per unit of N available (from the soil and/or fertilizer) and can be divided into UPE (aboveground N uptake at maturity (AGN)/N available) and UTE (grain dry matter yield/AGN) [46]. UTE can be calculated by dividing the N harvest index (NHI; the proportion of AGN in the grain at harvest) by the GNC according to the formulas for NHI and UTE, as follows: NHI ¼ ðyieldñGNCÞ=AGN

UTE ¼ yield=AGN ¼ NHI=GNC

2.5. Statistical analysis Statistical analyses were performed with SPSS 19.0 (SPSS, Inc., Chicago, IL, USA). Because plant density was set separately for each cultivar, an analysis of variance (ANOVA) was performed using the completely randomized design for each cultivar. Means and significant differences between sowing date were judged by the least significant difference (LSD) test at the 0.05 probability level when the ANOVA test indicated a significant effect of the treatment.

3. Results 3.1. Effects of sowing date on phenological development No differences in seedling number at emergence were observed among sowing dates for either cultivar. The time required from sowing to emergence was similar between early

No appreciable lodging was observed with early and normal sowing for cultivar T18 in either season, but early and normal sowing resulted in much thinner stems than late sowing. Equal lodging was observed with early and normal sowing for S15, with average rates of 31.8% and 36.2% in 2014 and 2015, respectively. No lodging was observed with late sowing for either cultivar in either year. Sowing date had a significant effect on the plant height, CHCG, length, diameter, wall thickness, dry weight, filling degree, TFS and CLRI for each cultivar, while year and sowing date × year interaction showed inconsistent effects on these indices (Table 2). Early and normal sowing did not lead to significant differences in the lodging resistance of winter wheat or relative indices associated with lodging resistance. Compared with early and normal sowing, late sowing significantly decreased the length of each internode (Fig. 2). For the cultivar T18, the plant height, CHCG, and the length of the second base internode with late sowing were respectively 5.7%, 6.9%, and 7.2% lower than those with early sowing and 5.3%, 7.2%, and 7.2% lower than those with normal sowing. The diameter, wall thickness, dry weight, filling degree, and TFS of the second base internode with late sowing were 16.6%, 27.8%, 28.0%, 38.1%, and 39.1% higher than those with early sowing, respectively, and 15.3%, 21.5%, 27.2%, 37.1%, and 37.6% higher than those with normal sowing, respectively. Trends for S15 and T18 were similar (Table 3). The CLRI, an index used to evaluate the lodging resistance of winter wheat, was significantly affected by sowing date in both cultivars (Table 2). Similar CLRIs were observed for early and normal sowing. The CLRI of T18 with late sowing was 49.2% and 48.3% higher than those with early and normal

Table 1 – The date at which wheat reached emergence, jointing, booting, anthesis, and maturity stages for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Year

Sowing date

Emergence

T18

2014

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

2015

S15

2014

2015

1, 2013 8, 2013 15, 2013 1, 2014 8, 2014 15, 2014 1, 2013 8, 2013 15, 2013 1, 2014 8, 2014 15, 2014

8, 2013 15, 2013 23, 2013 9, 2014 16, 2014 24, 2014 9, 2013 16, 2013 24, 2013 9, 2014 16, 2014 24, 2014

Jointing Mar. Mar. Mar. Mar. Mar. Mar. Mar. Mar. Mar. Mar. Mar. Mar.

26, 26, 27, 28, 28, 29, 24, 24, 25, 26, 26, 27,

2014 2014 2014 2015 2015 2015 2014 2014 2014 2015 2015 2015

Booting Apr. Apr. Apr. Apr. Apr. Apr. Apr. Apr. Apr. Apr. Apr. Apr.

22, 22, 22, 26, 26, 26, 21, 21, 21, 24, 24, 24,

2014 2014 2014 2015 2015 2015 2014 2014 2014 2015 2015 2015

Anthesis Apr. 30, 2014 Apr. 30, 2014 Apr. 30, 2014 May 3, 2015 May 3, 2015 May 3, 2015 Apr. 28, 2014 Apr. 28, 2014 Apr. 28, 2014 May 1, 2015 May 1, 2015 May 1, 2015

Maturity Jun. Jun. Jun. Jun. Jun. Jun. Jun. Jun. Jun. Jun. Jun. Jun.

12, 2014 12, 2014 12, 2014 9, 2015 9, 2015 9, 2015 12, 2014 12, 2014 12, 2014 9, 2015 9, 2015 9, 2015

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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Table 2 – Analysis of variance of plant height, culm height at the center of gravity (CHCG), and length, diameter, wall thickness, dry weight, filling degree, tensile failure strength (TFS), and culm lodging resistance index (CLRI) as affected by sowing date (D), year (Y), and their interaction (D × Y) for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar T18

S15

Factor

Plant height

CHCG

Length

Diameter

Wall thickness

Dry weight

Filling degree

TFS

CLRI

D Y D×Y D Y D×Y

10.11 ⁎⁎ 7.26 ⁎

16.80 ⁎⁎⁎

17.93 ⁎⁎⁎ 31.21 ⁎⁎⁎

69.94 ⁎⁎⁎ 36.56 ⁎⁎⁎ 7.04 ⁎⁎ 56.81 ⁎⁎⁎ 126.69 ⁎⁎⁎ 13.30 ⁎⁎⁎

150.48 ⁎⁎⁎ 264.40 ⁎⁎⁎ 4.16 ⁎ 186.64 ⁎⁎⁎ 101.25 ⁎⁎⁎ 5.55 ⁎

201.69 ⁎⁎⁎ 10.36 ⁎⁎

340.29 ⁎⁎⁎ 69.41 ⁎⁎⁎

339.50 ⁎⁎⁎ 295.14 ⁎⁎⁎

0.95 72.72 ⁎⁎⁎ 30.64 ⁎⁎⁎ 0.35

0.39 209.88 ⁎⁎⁎ 0.01 4.17

3.07 369.82 ⁎⁎⁎ 100.30 ⁎⁎⁎ 0.84

518.35 ⁎⁎⁎ 272.25 ⁎⁎⁎ 1.67 622.49 ⁎⁎⁎ 233.11 ⁎⁎⁎

0.27 9.82 ⁎⁎ 0.07 0.15

0.22 0.02 31.33 ⁎⁎⁎ 37.44 ⁎⁎⁎ 2.34

1.82 34.06 ⁎⁎⁎ 28.94 ⁎⁎⁎ 1.09

1.48

⁎ Significant at the 0.05 probability level. ⁎⁎ Significant at the 0.01 probability level. ⁎⁎⁎ Significant at the 0.001 probability level.

sowing, respectively, while the CLRI of S15 with late sowing was 57.7% and 51.0% higher than those with early and normal sowing, respectively (Fig. 3).

3.3. Effects of sowing date on grain yield and yield components Sowing date and sowing date × year interaction had no effect on grain yield, and only the effect of year was significant for the two cultivars (Table 4). Sowing date significantly affected spikes per square meter and kernel per spike but had no effect on kernel weight, kernels per square meter, or harvest index (Table 4). Grain yields of the different sowing dates were similar for the cultivars (Table 5). Early and normal sowing led

Plant height (cm)

100

to similar grain yields and yield components. Compared with early and normal sowing, the maintenance of grain yield with late sowing was due mainly to the similar proportions of decreased spikes per square meter and increased kernels per spike. The spikes per square meter of T18 decreased by 8.1% and 8.3% compared to those with early and normal sowing, respectively, while the number of kernels per spike increased by 8.3% and 7.6% compared to those with early and normal sowing, respectively. Trends for S15 and T18 were similar (Table 5). Across the sowing dates, the grain yields of cultivars T18 and S15 in 2015 were 10.8% and 4.0% lower than those in 2014, respectively, mainly because of a shorter grain filling duration.

100

a

Spike Internode 3

Peduncle Internode 2

Internode 4 Internode 1

b

80

80

60

60

40

40

20

20

0

0 Oct.1

Oct.8

Oct.15

100

c Plant height (cm)

Oct.1

Oct.8

Oct.15

Oct.1

Oct.8

Oct.15

100

d

80

80

60

60

40

40

20

20

0

0 Oct.1

Oct.8

Sowing date

Oct.15

Sowing date

Fig. 2 – The effect of sowing date on the length of each internode, peduncle, spike, and plant height in a) Tainong 18 in 2014, b) Tainong 18 in 2015, c) Shannong 15 in 2014, and d) Shannong 15 in 2015. Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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Table 3 – The effect of sowing date on plant height, culm height at the center of gravity (CHCG), and length, diameter, wall thickness, dry weight, filling degree, and tensile failure strength (TFS) of the second base internode for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Year

Sowing date

Plant height (cm)

CHCG (cm)

Length (mm)

Diameter (mm)

Wall thickness (mm)

Dry weight (mg)

Filling degree (mg mm−1)

T18

2014

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

79.02 78.81 75.20 82.07 81.73 76.75 79.20 78.70 75.12 78.99 79.04 74.26

51.46 51.63 47.99 51.83 51.96 48.13 47.85 47.68 44.28 52.24 52.03 46.03

88.35 88.12 80.06 81.39 81.54 77.23 90.42 90.06 83.02 86.15 85.61 75.52

3.06 3.10 3.75 3.42 3.45 3.78 3.74 3.72 3.98 3.05 3.16 3.80

0.29 0.31 0.39 0.37 0.39 0.45 0.42 0.41 0.51 0.35 0.37 0.47

72.03 71.45 90.86 73.26 74.87 95.20 83.29 82.16 94.48 77.21 76.09 90.17

0.82 0.81 1.13 0.90 0.92 1.23 0.92 0.91 1.14 0.90 0.89 1.19

2015

S15

2014

2015

1 8 15 1 8 15 1 8 15 1 8 15

a a b a a b a a b a a b

a a b a a b a a b a a b

a a b a a b a a b a a b

b b a b b a b b a b b a

b b a b b a b b a b b a

b b a b b a b b a b b a

b b a b b a b b a b b a

TFS (N) 2.69 2.72 3.97 3.48 2.51 4.54 2.94 3.08 4.05 2.55 2.64 3.74

b b a b b a b b a b b a

Values followed by the same letter within a column, within the same cultivar, in the same year are not significantly different at P < 0.05, as determined by the LSD test.

Table 6 shows dry matter accumulation through the entire growing season. Before wintering and at jointing, early sowing led to an average of 32.1% and 21.6% more accumulated dry matter compared with normal sowing for cultivar T18 and an average of 51.8% and 28.9% more dry matter for S15, respectively. In contrast, before wintering and at jointing, late sowing led to an average of 34.0% and 20.7% less accumulated dry matter for T18 compared with normal sowing, and an average of 38.3% and 22.2% less dry matter for S15, respectively. Similar dry matter was observed between early and normal sowing at booting. However, compared with early and normal sowing, late sowing at booting led to an average of 12.9% and 9.0% less accumulated dry matter for T18, respectively, and averages of respectively 16.5% and 13.8% less dry matter for S15, averaged over the years. Equal dry matter accumulation was observed at different sowing dates in both seasons for each cultivar at anthesis and maturity. Similar dry matter accumulation resulted in equal grain yields at different sowing dates with equal harvest indices (Table 5).

12

3.4. Effects of sowing date on NUE and its associated parameters Sowing date had no significant effect on NUE in either cultivar (Table 7). Accordingly, similar NUEs were observed among sowing dates for each cultivar (Table 6). The NUE in 2015 was 8.1% lower than that in 2014 for T18, because of a lower grain yield. Similar NUEs between the two years were observed for S15. The primary effects of sowing date and year significantly affected UPE for both cultivars (Table 7). Early and normal sowing led to no difference in UPE, while UPE with late sowing was respectively 11.9% and 10.1% lower than with early and normal sowing for cultivar T18, and 10.5% and 9.2% lower for S15 (Table 8). Sowing date and year significantly influenced AGN for both cultivars (Table 7). Table 9 shows aboveground N uptake over the entire growing season. Before wintering and jointing, the aboveground N uptake with early sowing was 33.9% and 17.1% higher than those with normal sowing for cultivar T18 and 47.7% and 27.7% higher for S15, respectively. The aboveground

12 2013-2014

CLRI (N m-1)

2014-2015 9

9

6

6

3

3

0

0 Oct.1

Oct.8 Sowing date

Oct.15

Oct.1

Oct.8

Oct.15

Sowing date

Fig. 3 – The effect of sowing date on culm lodging resistance index (CLRI) in both years for cultivars Tainong 18 (left) and Shannong 15 (right). The error bars indicate standard errors of the mean. Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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Table 4 – Analysis of variance of grain yield, kernel weight, spikes per square meter, kernels per spike, kernels per square meter and harvest index as affected by sowing date (D), year (Y), and their interaction (D × Y) for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Factor

T18

D Y D×Y D Y D×Y

S15

Yield

Kernel weight

Spikes per square meter

Kernels per spike

Kernels per square meter

Harvest index

0.02 94.33 ⁎⁎⁎ 0.50 0.00 9.78 ⁎⁎

0.60 34.86 ⁎⁎⁎ 0.05 0.31 3.37 0.05

23.64 ⁎⁎⁎ 123.88 ⁎⁎⁎ 2.76 12.11 ⁎⁎ 20.56 ⁎⁎⁎

19.68 ⁎⁎⁎ 1.46 1.43 7.70 ⁎⁎ 38.19 ⁎⁎⁎

0.25

0.62

0.14 24.07 ⁎⁎⁎ 0.06 0.17 0.65 0.02

0.16 0.99 0.17 1.11 15.88 ⁎⁎ 0.02

0.13

⁎⁎ Significant at the 0.01 probability level. ⁎⁎⁎ Significant at the 0.001 probability level.

N uptake with late sowing was 34.9% and 26.5% lower than with normal sowing for T18 before wintering and at jointing, respectively, and 37.9% and 26.4% lower for S15, respectively. From booting to anthesis and maturity, early and normal sowing led to similar aboveground N uptakes. In contrast, for cultivar T18, late sowing resulted in an average of 17.8%, 8.6%, and 11.7% less N uptake than early sowing at booting, anthesis, and maturity, respectively, which were 12.4%, 7.2%, and 9.2% lower than with normal sowing, respectively. Trends for S15 and T18 were similar (Table 9). RLD with early sowing at jointing was 12.8% and 19.7% higher than with normal sowing for T18 and S15, respectively, whereas RLD with late sowing was 30.1% and 31.1% lower than with normal sowing for T18 and S15, respectively. Similar RLDs were observed between early and normal sowing at anthesis and filling. Averaged over years, RLDs of T18 with late sowing were respectively 17.0% and 20.5% lower than with early sowing at anthesis and filling and 16.0% and 17.5% lower than with normal sowing. Trends for S15 and T18 were similar (Fig. 4). Sowing date and year had significant effects on UTE for the two cultivars, but the effect of their interaction was not significant (Table 7). Similar UTEs were observed with early and normal sowing, whereas the UTEs were respectively

14.0% and 11.2% higher with late sowing than with early and normal sowing for cultivar T18, and 12.0% and 10.3% higher for S15 (Table 8). The UTE in 2015 was 4.3% and 20.8% lower than the values in 2014 for T18 and S15, respectively. Neither sowing date nor year nor their interaction had significant effects on the NHI for the two cultivars (Table 7); that is, no differences in NHI were observed among sowing dates or between years (Table 8). The main effects of sowing date and year were significant for GNC for the two cultivars, whereas the effect of their interaction was not significant (Table 7). Similar GNCs were observed between early and normal sowing, whereas the GNC values observed with late sowing were 12.0% and 10.6% lower than with early and normal sowing, respectively, for T18, and 10.3% and 10.1% lower, respectively, for S15 (Table 8).

4. Discussion In the present study, late sowing significantly decreased the risk of lodging in two wheat cultivars, mainly by reducing the length of each internode, plant height, and CHCG, and increasing the diameter, wall thickness, dry weight, filling degree, and TFS of the internode. These observations are

Table 5 – The effect of sowing date on grain yield, kernel weight, spikes per square meter, kernels per spike, kernels per square meter, and harvest index for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Year

Sowing date

Yield (t ha−1)

Kernel weight (mg)

Spikes per square meter (no.)

Kernels per spike (no.)

Kernels per square meter (no.)

Harvest index (%)

T18

2014

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

9.83 a 9.89 a 9.78 a 8.74 a 8.70 a 8.85 a 10.16 a 10.18 a 10.11 a 9.74 a 9.70 a 9.78 a

36.25 36.12 36.59 33.63 33.75 34.25 41.32 41.26 41.68 40.25 40.56 40.79

738.00 746.00 665.00 643.03 638.67 602.00 746.57 750.00 699.00 790.54 781.33 743.33

38.25 38.60 42.40 39.38 39.74 41.84 30.95 30.73 32.72 28.81 28.96 29.99

28,228.5 28,795.6 28,196.0 25,324.3 25,380.6 25,187.7 23,106.5 23,047.5 22,871.3 22,804.3 22,630.5 22,289.6

42.15 42.52 43.20 42.76 42.46 43.25 45.27 45.21 46.22 47.48 47.53 48.26

2015

S15

2014

2015

1 8 15 1 8 15 1 8 15 1 8 15

a a a a a a a a a a a a

a a b a a b a a b a a b

b b a b b a b b a b b a

a a a a a a a a a a a a

a a a a a a a a a a a a

Values followed by the same letter within a column, within the same cultivar, in the same year are not significantly different at P < 0.05 as determined by the LSD test.

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

8

TH E C ROP J O U R NA L XX ( 2 0 17 ) XXX–X XX

Table 6 – The effect of sowing date on dry matter accumulation before wintering, before jointing, booting, anthesis, and maturity for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

T18

Year

2014

2015

S15

2014

2015

Dry matter accumulation (t ha−1)

Sowing date

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

1 8 15 1 8 15 1 8 15 1 8 15

Before wintering

Before jointing

Booting

Anthesis

Maturity

2.63 2.12 1.35 2.96 2.11 1.44 2.65 1.85 1.26 2.44 1.52 0.84

3.49 2.99 2.31 3.73 2.95 2.40 3.56 2.79 2.23 2.85 2.18 1.65

5.86 5.58 4.83 6.48 6.23 5.95 5.74 5.56 4.69 6.75 6.56 5.77

11.45 a 11.26 a 10.99 a 10.38 a 10.22 a 9.96 a 9.75 a 9.83 a 9.59 a 12.17 a 11.99 a 11.89 a

20.51 20.46 19.90 17.98 18.03 18.00 19.75 19.82 19.24 18.04 17.95 17.84

a b c a b c a b c a b c

a b c a b c a b c a b c

a a b a a b a a b a a b

a a a a a a a a a a a a

Values followed by the same letter within a column, within same cultivar, in the same year are not significantly different at P < 0.05 as determined by the LSD test.

consistent with previous reports [1,12,43]. Late sowing significantly decreased the length of each internode and plant height, consequently reducing the CHCG. The reduction in the length of the second internode and increases in the diameter, wall thickness, and dry weight resulted in increased filling, which enhanced the mechanical strength of the internode. Thus, TFS was increased with late sowing. According to the definition of CLRI, late sowing increased the CLRI mainly by reducing the CHCG and increasing the TFS of the base internode. The results of the present study reveal that sowing date did not affect the time of booting, anthesis, and grain filling or dry matter accumulation at or after anthesis during winter wheat production. Thus, equal grain yield was obtained using early, normal, or late sowing dates. This finding indicates that the sowing date can be postponed to October 15 in this region. The maintenance of grain yield with late sowing depends mainly on the compensatory relationship between decreased spikes per square meter and increased kernels per spike. The equal number of kernels per square meter originated from an increased number of kernels per spike and a decreased number of spikes per square meter. Tradeoff relationships between number of spikes per square meter and number of kernels per spike have been observed in common wheat [47] and hard red spring wheat [48], probably because of competition for radiation, nutrients,

and moisture. However, these results are not in complete agreement with those of Sun et al. [25], who observed equal grain yield among sowing dates, mainly because of equal yield components. However, if the next growing season is colder than in normal years, reduced yield may occur in consequence of lower tillers and spikes per square meter. For this reason, in consideration of the balance between lodging resistance and grain yield, winter wheat cultivars that are insensitive to cumulative degree days before winter should be selected when winter wheat is sown late [49]. Additionally, the fertilization and irrigation can shifted to an early date than conventional practice according to the tillers per square meter in early spring. However, based on long-term weather prediction, increased daily average temperatures during the winter wheat growing season are projected to occur [50]. Accordingly, according to the results of present study, future sowing dates may be postponed by seven days or even longer. Changes in NUE could be explained by UPE and UTE values. Few studies have investigated the response of NUE to sowing date. Although similar NUEs were observed among early, normal, and late sowing, UPE and UTE, the two components of NUE, were similar between early and normal sowing, but showed opposite trends in their responses to delayed sowing. Late sowing maintained high NUE, mainly through increased

Table 7 – Analysis of variance of nitrogen use efficiency (NUE), nitrogen uptake efficiency (UPE), nitrogen utilization efficiency (UTE), aboveground nitrogen uptake at maturity (AGN), nitrogen harvest index (NHI), and grain nitrogen concentration (GNC) as affected by sowing date (D), year (Y), and their interaction (D × Y) for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Factor

T18

D Y D×Y D Y D×Y

S15

NUE

UPE

UTE

AGN

NHI

GNC

0.02 51.44 ⁎⁎⁎ 0.51 0.00 0.72 0.14

44.30 ⁎⁎⁎ 12.22 ⁎⁎ 0.44 30.53 ⁎⁎⁎ 343.04 ⁎⁎⁎

49.94 ⁎⁎⁎ 13.72 ⁎⁎ 0.02 34.87 ⁎⁎⁎ 381.78 ⁎⁎⁎

44.36 ⁎⁎⁎ 36.52 ⁎⁎⁎ 0.58 30.78 ⁎⁎⁎ 257.08 ⁎⁎⁎

70.09 ⁎⁎⁎ 38.20 ⁎⁎⁎ 0.10 53.75 ⁎⁎⁎ 528.52 ⁎⁎⁎

0.19

1.72

0.25

0.01 1.51 0.03 0.17 1.21 0.00

0.00

⁎⁎ Significant at the 0.01 probability level. ⁎⁎⁎ Significant at the 0.001 probability level.

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

9

TH E C ROP J O U R NA L XX ( 2 0 17 ) XXX–X XX

Table 8 – The effect of sowing date on nitrogen use efficiency (NUE), nitrogen uptake efficiency (UPE), nitrogen utilization efficiency (UTE), nitrogen harvest index (NHI), and grain nitrogen concentration (GNC) for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

Year

Sowing date

NUE (kg kg−1)

UPE (kg kg−1)

UTE (kg kg−1)

NHI (%)

GNC (%)

T18

2014

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

19.74 19.87 19.63 18.09 18.01 18.32 20.41 20.46 20.30 20.16 20.08 20.26

75.81 74.83 66.22 72.53 71.17 64.38 69.67 69.29 61.66 86.29 85.10 78.79

26.04 26.55 29.64 24.94 25.31 28.45 29.30 29.53 32.93 23.36 23.59 25.71

66.11 66.37 66.27 67.21 67.07 67.37 69.64 69.97 69.41 68.69 69.12 68.53

2.54 2.50 2.24 2.69 2.65 2.37 2.38 2.37 2.11 2.94 2.93 2.66

2015

S15

2014

2015

1 8 15 1 8 15 1 8 15 1 8 15

a a a a a a a a a a a a

a a b a a b a a b a a b

b b a b b a b b a b b a

a a a a a a a a a a a a

a a b a a b a a b a a b

Values followed by the same letter within a column, within same cultivar, in the same year are not significantly different at P < 0.05 as determined by the LSD test.

UTE resulting from reduced GNC and no change in NHI; however, UPE was reduced owing to decreased AGN. Although aboveground N uptake with early sowing was higher than that with normal sowing before wintering and jointing, values were optimized at and after booting, whereas N uptake with late sowing was always lower than that with normal sowing until maturity. Lower AGN with late sowing was also observed by Widdowson et al. [30], indicating that late sowing decreases N uptake. High AGN depends mainly on N availability [3], efficient uptake of N from soil [18,51], and a high aboveground storage capacity of the plant [52]. Optimizing the root system is an important consideration for improving N uptake [53–55], and a positive relationship between N uptake and RLD has been confirmed by Wiesler and Horst [56] and Kristensen and Thorup-Kristensen [57,58]. N uptake by the roots is down regulated by the saturation effect of plant storage capacity [59], and a significant correlation between dry matter and N accumulation has been shown [52]. In the present study,

significant decreases in RLD at jointing, anthesis, and grain filling and dry matter accumulation before anthesis were observed with late sowing. Based on similarities in available N, the decrease in AGN with late sowing was probably due to the reduction in RLD and lower dry matter accumulation before anthesis, given that 70%–80% or more N is absorbed before anthesis in winter wheat [24,60].

5. Conclusions Early and normal sowing led to no differences in lodging resistance, grain yield, or NUE. Postponing the sowing date significantly increased lodging resistance by reducing plant CHCG and increasing the TFS of the base internode, and resulted in a grain yield maintained at the same level as that for early and normal sowing, owing to the compensatory relationship between decreased spikes per square meter and increased kernels per spike. Late sowing resulted in lower N

Table 9 – The effect of sowing date on the aboveground nitrogen uptake before wintering, before jointing, booting, anthesis, and maturity for cultivars Tainong 18 (T18) and Shannong 15 (S15). Cultivar

T18

Year

2014

2015

S15

2014

2015

Aboveground nitrogen uptake (kg ha− 1)

Sowing date

Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct. Oct.

1 8 15 1 8 15 1 8 15 1 8 15

Before wintering

Before jointing

Booting

Anthesis

Maturity

99.13 74.96 46.90 91.08 67.14 45.45 68.36 49.83 34.32 80.09 50.65 27.99

113.45 a 98.50 b 70.81 c 112.06 a 94.23 b 70.82 c 110.63 a 87.36 b 68.40 c 121.03 a 93.94 b 64.65 c

225.40 214.67 187.35 224.34 211.21 197.40 218.91 213.90 171.42 243.39 236.50 202.86

280.45 272.59 251.04 266.56 258.89 242.61 249.45 240.08 225.07 322.03 318.46 298.85

332.04 327.77 290.04 308.27 302.49 273.63 305.15 303.50 270.09 366.72 361.67 334.85

a b c a b c a b c a b c

a a b a a b a a b a a b

a a b a a b a a b a a b

a a b a a b a a b a a b

Values followed by the same letter within a column, within same cultivar, in the same year are not significantly different at P < 0.05 as determined by the LSD test.

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

10

TH E C ROP J O U R NA L XX ( 2 0 17 ) XXX–X XX

10

10

a

Oct.1

b

RLD (mm cm-3)

Oct.8 8

Oct.15

6

6

4

4

2

2 Jointing 6

RLD (mm cm-3)

8

Anthesis

Filling 6

c

5

5

4

4

3

3

Jointing

Anthesis

Filling

Jointing

Anthesis

Filling

d

2

2 Jointing

Anthesis

Filling

Fig. 4 – The effect of sowing date on root length density (RLD) in a) Tainong 18 in 2014, b) Tainong 18 in 2015, c) Shannong 15 in 2014, and d) Shannong 15 in 2015. The error bars indicate standard errors of the mean.

uptake owing to lower dry matter accumulation before anthesis and RLD, and a higher UTE as a result of a reduced GNC. The increase in UTE offset the reduction in UPE, so that a similar NUE was observed for all sowing dates. Thus, appropriate sowing at later times can increase lodging resistance while maintaining grain yield and NUE.

Acknowledgments This study was supported by the National Basic Research Program of China (2015CB150404), Shandong Province Higher Education Science and Technology Program (J15LF07), Youth Science and Technology Innovation Foundation of Shandong Agricultural University (2014-2).

REFERENCES [1] M.J. Pinthus, Lodging in wheat, barley and oats; the phenomenon-its causes and preventative measures, Adv. Agron. 25 (1973) 209–263. [2] M.J. Foulkes, G.A. Slafer, W.J. Davies, P.M. Berry, R. SylvesterBradley, P. Martre, D.F. Calderini, S. Griffiths, M.P. Reynolds, Raising yield potential of wheat: III. Optimizing partitioning to grain while maintaining lodging resistance, J. Exp. Bot. 62 (2011) 469–486.

[3] M.J. Foulkes, M.J. Hawkesford, P.B. Barraclough, M.J. Holdsworth, S. Kerr, S. Kightley, P.R. Shewry, Identifying traits to improve the nitrogen economy of wheat: recent advances and future prospects, Field Crop Res. 114 (2009) 329–342. [4] R.A. Fischer, M. Stapper, Lodging effects on high yielding crops of irrigated semi-dwarf wheat, Field Crop Res. 17 (1987) 245–248. [5] D.L. Easson, E.M. White, S.J. Pickles, The effects of weather, seeding rate and cultivar on lodging and yield in winter wheat, J. Agric. Sci. 121 (1993) 145–156. [6] C.J. Baker, P.M. Berry, J.H. Spink, R. Sylvester-Bradley, J.M. Griffin, R.K. Scott, R.W. Clare, A method for the assessment of the risk of wheat lodging, J. Theor. Biol. 194 (1998) 587–603. [7] K.A. Scudamore, Mycotoxins in stored grain, Proceedings of the Seventh Home-grown Cereals Association R&D Conference on Cereals and Oilseeds, HGCA, London, UK, 2000. [8] W.R. Raun, J.B. Solie, G.V. Johnson, M.L. Stone, R.W. Mullen, K.W. Freeman, W.E. Thomason, E.V. Lukina, Improving nitrogen-use efficiency in cereal grain production with optical sensing and variable rate application, Agron. J. 94 (2002) 815–820. [9] W.R. Raun, G.V. Johnson, Improving nitrogen use efficiency from cereal production, Agron. J. 91 (1999) 357–363. [10] X.P. Chen, F.Z. Zhang, V. Römheld, D. Horlacher, R. Schulz, M. Böning-Zilkens, P. Wang, W. Claupein, Synchronizing N supply from soil and fertilizer and N demand of winter wheat by an improved Nmin method, Nutr. Cycl. Agroecosyst. 74 (2006) 91–98. [11] S.C. Tripathi, K.D. Sayre, J.N. Kaul, R.S. Narang, Growth and morphology of spring wheat (Triticum aestivum L.) culms and their association with lodging: effects of genotypes, N levels and ethephon, Field Crop Res. 84 (2003) 271–290.

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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[12] J.C. Li, J. Yin, F.Z. Wei, Effects of planting density on characters of culm and culm lodging resistant index in winter wheat, Acta Agron. Sin. 51 (2005) 662–666 (in Chinese with English abstract). [13] F.Z. Wei, J.C. Li, C.Y. Wang, H.J. Qu, X.S. Shen, Effects of nitrogenous fertilizer application model on culm lodging resistance in winter wheat, Acta Agron. Sin. 34 (2008) 1080–1085 (in Chinese with English abstract). [14] M.J. Crook, A.R. Ennos, The effect of nitrogen and growth regulators on stem and root characteristics associated with lodging in two cultivars of winter wheat, J. Exp. Bot. 46 (1995) 931–938. [15] P.M. Berry, R. Sylvester-Bradley, S. Berry, Ideotype design for lodging-resistant wheat, Euphytica 154 (2007) 165–179. [16] K. Blankenau, H.W. Olfs, Effect of different crop densities of winter wheat on recovery of nitrogen in crop and soil within the growth period, J. Agron. Crop Sci. 186 (2001) 151–156. [17] I. Arduini, A. Masoni, L. Ercoli, M. Mariotti, Grain yield, and dry matter and nitrogen accumulation and remobilization in durum wheat as affected by variety and seeding rate, Eur. J. Agron. 25 (2006) 309–318. [18] X.L. Dai, X.H. Zhou, D.Y. Jia, L.L. Xiao, H.B. Kong, M.R. He, Managing the seeding rate to improve nitrogen-use efficiency of winter wheat, Field Crop Res. 154 (2013) 100–109. [19] X.L. Dai, L.L. Xiao, D.Y. Jia, H.B. Kong, Y.C. Wang, C.X. Li, Y. Zhang, M.R. He, Increased plant density of winter wheat can enhance nitrogen-uptake from deep soil, Plant Soil 384 (2014) 141–152. [20] P.M. Berry, M. Sterling, J.H. Spink, C.J. Baker, R. Sylvester-Bradley, S.J. Mooney, A.R. Tams, A.R. Ennos, Understanding and reducing lodging in cereals, Adv. Agron. 84 (2004) 217–271. [21] E.A. Ainsworth, D.R. Ort, How do we improve crop production in a warming world, Plant Physiol. 154 (2010) 526–530. [22] Q.R. Ma, L. Cheng, G.X. Yang, Discussion of suitable index for wheat before overwintering based on interval sowing test, Meteorol. Environ. Sci. 34 (2011) 63–67 (in Chinese with English abstract). [23] A.F. Fielder, Interactions between variety and sowing date for winter wheat and winter barley, HGCA Research Review, Home-Grown Cereals Authority, London, UK, 1988. [24] M. Stapper, R.A. Fischer, Genotype, sowing date and plant spacing influence on high-yielding irrigated wheat in southern New South Wales. I. Phasic development, canopy growth and spike production, Aust. J. Agric. Res. 41 (1990) 997–1019. [25] H.Y. Sun, X.Y. Zhang, S.Y. Chen, D. Pei, C.M. Liu, Effects of harvest and sowing time on the performance of the rotation of winter wheat-summer maize in the North China Plain, Ind. Crop. Prod. 25 (2007) 239–247. [26] G.C. Zhao, X.H. Chang, Y.S. Yang, Z.H. Li, G.J. Yu, H.L. Li, Study on high-yield, high-efficiency and adapting cultivating technology in winter wheat, J. Triticeae Crop. 29 (2009) 690–695 (in Chinese with English abstract). [27] X.Q. Zhang, S.Z. Du, C.F. Cao, Y.Q. Qiao, Z. Zhao, Y.L. Zhao, Effects of sowing date on population traits, yield and chlorophyll fluorescence characteristics of winter wheat, J. Triticeae Crop. 34 (2014) 71–77 (in Chinese with English abstract). [28] Y.E. Liu, R.Z. Xie, H.B. Zhang, S.K. Li, S.J. Gao, Study on increasing rate of maize yield after putting off harvest time in different ecoregions, Sci. Agric. Sin. 43 (2010) 2820–2828 (in Chinese with English abstract). [29] X.L. Fu, H. Zhang, J.Z. Jia, L.F. Du, J.D. Fu, M. Zhao, Yield performance and resources use efficiency of winter wheat and summer maize in double late-cropping system, Acta Agron. Sin. 35 (2009) 1708–1714 (in Chinese with English abstract). [30] F.V. Widdowson, A. Penny, R.J. Darby, E. Bird, M.V. Hewitt, Amount of NO3-N and NH4-N in soil, from autumn to spring, under winter wheat and their relationship to soil type, sowing date, previous crop and N uptake at Rothamsted,

[31]

[32]

[33]

[34]

[35] [36]

[37] [38]

[39]

[40]

[41]

[42]

[43]

[44]

[45]

[46]

[47]

[48]

[49]

[50]

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Woburn and Saxmundham, 1979–1985, J. Agric. Sci. 108 (1987) 73–95. J.G. Mcleod, C.A. Campbell, F.B. Dyck, C.L. Vera, Optimum seeding date for winter wheat in southwestern Saskatchewan, Agron. J. 84 (1992) 86–90. B. Ehdaie, J.G. Waines, Sowing date and nitrogen rate effects on dry matter and nitrogen partitioning in bread and durum wheat, Field Crop Res. 73 (2001) 47–61. A. Ozturk, O. Caglar, S. Bulut, Growth and yield response of facultative wheat to winter sowing, freezing sowing and spring sowing at different seeding rates, J. Agron. Crop Sci. 192 (2006) 10–16. M. Alignan, J. Roche, A. Bouniols, M. Cerny, Z. Mouloungui, O. Merah, Effects of genotype and sowing date on phytostanolphytosterol content and agronomic traits in wheat under organic agriculture, Food Chem. 117 (2009) 219–225. B.W. Jiang, J.J. Dai, Experiment of Soil and Fertilizer Science, Peking University Press, Beijing, China, 2003 (in Chinese). A. Walkley, I.A. Black, An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method, Soil Sci. 37 (1934) 29–38. J.M. Bremner, Determination of nitrogen in soil by the Kjeldahl method, J. Agric. Sci. 55 (1960) 11–33. S.H. Yuen, A.G. Pollard, Determination of nitrogen in soil and plant materials: use of boric acid in the micro-Kjeldahl method, J. Sci. Food Agric. 4 (1953) 490–496. H.G. Zandstra, Automated determination of phosphorus in sodium bicarbonate extracts, Can. J. Soil Sci. 48 (1968) 219–220. A. Melich, Determination of P, Ca, Mg, K, Na, NH4, Short Test Methods Used in Soil Testing Division, Department of Agriculture, Raleigh, North Carolina, USA, 1953. R. Wagner, A new method for automated nitrate determination in sea water using the AutoAnalyzer, Technicon Symposium, Frankfurt am Main, Germany, 1974 (in German). R. Benesch, P. Mangelsdorf, A method for the colorimetric determination of ammonia in seawater, Helgoländer Meeresun. 23 (1972) 365–375 (in German with English abstract). P.M. Berry, J.M. Griffin, R. Sylvester-Bradley, R.K. Scott, J.H. Spink, C.J. Baker, R.W. Clare, Controlling plant form through husbandry to minimize lodging in wheat, Field Crop Res. 67 (2000) 59–81. X.G. Chen, C.Y. Shi, Y.P. Yin, Z.L. Wang, Y.H. Shi, D.L. Peng, Y.L. Ni, T. Cai, Relationship between lignin metabolism and lodging resistance in wheat, Acta Agron. Sin. 37 (2011) 1616–1622 (in Chinese with English abstract). C.Y. Wang, X.L. Dai, Y.H. Shi, Z.L. Wang, X.G. Chen, M.R. He, Effects of nitrogen application rate and plant density on lodging resistance in winter wheat, Acta Agron. Sin. 38 (2012) 121–128 (in Chinese with English abstract). R.H. Moll, E.J. Kamprath, W.A. Jackson, Analysis and interpretation of factors which contribute to efficiency to nitrogen utilization, Agron. J. 75 (1982) 562–564. J. Lloveras, J. Manent, J. Viudas, A. López, P. Santiveri, Seeding rate influence on yield and yield components of irrigated winter wheat in a Mediterranean climate, Agron. J. 96 (2004) 1258–1265. C.C. Chen, K. Neill, D. Wichman, M. Westcott, Hard spring wheat response to row spacing, seeding rate and nitrogen, Agron. J. 100 (2008) 1296–1302. L.H. Lv, S.B. Liang, L.H. Zhang, X.L. Jia, Z.Q. Dong, Y.R. Yao, Yield response to accumulated temperature before winter in winter wheat, Acta Agron. Sin. 42 (2016) 149–156 (in Chinese with English abstract). Z.F. Lv, X.J. Liu, W.X. Cao, Y. Zhu, Climate change impacts on regional winter wheat production in main wheat production regions of China, Agric. For. Meteorol. 171–172 (2013) 234–248.

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003

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[51] P.B. Barraclough, J.R. Howarth, J. Jones, R. Lopez-Bellido, S. Parmar, C.E. Shepherd, M.J. Hawkesford, Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement, Eur. J. Agron. 33 (2010) 1–11. [52] R. Ferrise, A. Triossi, P. Stratonovitch, M. Bindi, P. Martre, Sowing date and nitrogen fertilization effects on dry matter and nitrogen dynamics for durum wheat: an experimental and simulation study, Field Crop Res. 117 (2010) 245–257. [53] J.A. King, A. Gay, R. Sylvester-Bradley, I. Bingham, M.J. Foulkes, P.J. Gregory, D. Robinson, Modelling cereal root systems for water and nitrogen capture towards an economic optimum, Ann. Bot. 91 (2003) 383–390. [54] O. Gaju, V. Allard, P. Martre, J.W. Snape, E. Heumez, J. Le Gouis, D. Moreau, M. Bogard, S. Griffiths, S. Orford, S. Hubbart, M.J. Foulkes, Identification of traits to improve the nitrogenuse efficiency of wheat genotypes, Field Crop Res. 123 (2011) 139–152. [55] E.M. Wahlsoröm, E.M. Hansen, A. Mandel, A. Garbout, H.L. Kristensen, L.J. Munkholm, Root development of fodder radish and winter wheat before winter in relation to uptake of nitrogen, Eur. J. Agron. 71 (2015) 1–9.

[56] F. Wiesler, W.J. Horst, Root growth and nitrate utilization of maize cultivars under field conditions, Plant Soil 163 (1994) 267–277. [57] H.L. Kristensen, K. Thorup-Kristensen, Uptake of 15N labeled nitrate by root system of sweet corn, carrot and white cabbage from 0.2–2.5 meters depth, Plant Soil 265 (2004) 93–100. [58] H.L. Kristensen, K. Thorup-Kristensen, Root growth and nitrate uptake of three different catch crops in deep soil layers, Soil Sci. Soc. Am. J. 68 (2004) 529–537. [59] D.T. Clarkson, Regulation of the absorption and release of nitrate by plants: a review of current ideas and methodology, in: H. Lambers, J.J. Neeteson, I. Stulen (Eds.), Developments in Plant Sciences, Fundamental, Ecological and Agricultural Aspects of Nitrogen Metabolism in Higher Plants, vol. 19, Martinus Nijhoff Publishers, Dordrecht, the Netherlands, 1986. [60] X.K. Zhu, W.S. Guo, C.N. Feng, Y.X. Peng, Q.H. Ling, Nitrogen absorption and utilization differences among wheat varieties for different end uses, Plant Nutr. Fert. Sci. 11 (2005) 148–154 (in Chinese with English abstract).

Please cite this article as: X. Dai, et al., Delayed sowing can increase lodging resistance while maintaining grain yield and nitrogen use efficiency in winter wheat, The Crop Journal (2017), http://dx.doi.org/10.1016/j.cj.2017.05.003