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Field Crops Research 149 (2013) 177–186

Contents lists available at SciVerse ScienceDirect

Field Crops Research

jou rn al hom epage: www.elsev ier .com/ locate / fc r

aize kernel growth at different floret positions of the ear

oujia Chena,b, Gerrit Hoogenboomb, Yuntao Maa, Baoguo Lia, Yan Guoa,∗

Key Laboratory of Arable Land Conservation (North China), Ministry of Agriculture, College of Resources and Environment, China Agricultural University,eijing 100193, ChinaAgWeatherNet, Washington State University, Prosser, WA 99350, USA

r t i c l e i n f o

rticle history:eceived 28 February 2013eceived in revised form 23 April 2013ccepted 27 April 2013

eywords:aize

ernel weight variationloret positionernel growth raterain filling

a b s t r a c t

The variation of individual kernel weight can have a large impact on final yield of maize (Zea mays L.). Thegoal of this research was to investigate the variation of maize kernel dry weight (KW) along the rachis ofthe ear and to determine the effect of kernel growth parameters on this variation. Field experiments wereconducted for three years using two hybrids with contrasting plant densities. The fresh and dry weightsof each kernel from one row of the ear were measured. Kernel growth at the basal, upper and apicalsections of the ear was compared with that at the lower third section. The KW distribution in one rowwas the highest for the lower third section, followed by the basal and upper sections and the lowest forthe apical section. The relative decrease in final KW of the other sections relative to the lower third sectionwas determined by both the decrease in rate and duration of linear grain-filling for the normal densitytreatments, and was only determined by the decrease in growth rate for the low density treatments. The

ield distribution of kernel water mass in one row showed the same trend as KW. However, the developmentsof kernel moisture content among sections were quite similar. The relative change in final KW of theother sections relative to the lower third section was closely correlated with the relative change in kernelmaximum water mass (R2 = 0.99). This study reflects the substantial difference in KW along the rachis ofthe ear and indicates that the mechanism of individual kernel growth should be integrated into maizesimulation models in order to predict yield more accurately.

© 2013 Elsevier B.V. All rights reserved.

. Introduction

Maize (Zea mays L.) is one of the most important cereal crops inhe world. Although maize yield is mainly determined by the kernelumber per unit land area (Otegui, 1995; Chapman and Edmeades,999), large deviations in crop yield estimation can occur because ofhe variation in the weight of individual kernels (Borrás et al., 2004;orrás and Gambín, 2010). A large variation in kernel dry weightKW) for different hybrids and environments has been reportedSaini and Westgate, 1999; Borrás et al., 2004). However, the infor-

ation of kernel variation among the position on the ear and thehysiological mechanisms controlling the variation are still lacking.

The individual KW accumulation is controlled by the kernel

rowth rate and the duration of linear grain-filling (Borrás andambín, 2010). Many studies have been conducted on kernelrowth of cereal crops, including maize (Borrás et al., 2003; Echarte

Abbreviation: KW, kernel dry weight.∗ Corresponding author at: College of Resources and Environment, China Agricul-

ural University, No. 2 Yuanmingyuan West Road, Beijing 100193, China.el.: +86 10 62732959.

E-mail address: yan.guo@cau.edu.cn (Y. Guo).

378-4290/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.fcr.2013.04.028

et al., 2006; Sala et al., 2007a), wheat (Triticum aestivum L.) (Slaferand Savin, 1994; Acreche and Slafer, 2009) and sorghum (Sorghumbicolor (L.) Moench) (Gambín and Borrás, 2005). It has been sug-gested that the assimilate availability per kernel during the earlygrowth stage determines its potential sink capacity and is closelyrelated to the kernel growth rate during the linear grain-fillingperiod (Capitanio et al., 1983; Andrade et al., 1999; Gambín et al.,2006; Borrás and Gambín, 2010). The duration of linear grain-fillingis related to the environmental conditions during the grain-fillingstage for a given hybrid. For example, drought (Barlow et al., 1980;Brooks et al., 1982; Westgate, 1994), severe pathogen infestations(Pepler et al., 2006), or defoliations (Egharevba et al., 1976; Echarteet al., 2006; Sala et al., 2007a) can significantly shorten the fillingduration. On the other hand, an increase in assimilate supply doesnot influence the duration of grain-filling if the assimilate supply isnon-limiting (Borrás et al., 2003).

The water mass of a kernel rapidly increases during the earlystage of kernel growth (Saini and Westgate, 1999) and obtainsits maximum value during the middle of the grain-filling period

(Westgate and Boyer, 1986; Borrás et al., 2003; Gambín et al.,2007a). The maximum water mass of a kernel has been suggestedto be a good indicator of potential kernel sink capacity (Borrás andWestgate, 2006). It was correlated with kernel growth rate and

178 Y. Chen et al. / Field Crops Research 149 (2013) 177–186

Table 1Sowing, emergence and silking dates of each treatment.

Year Hybrid Plant density (plant m−2) Sowing date Emergence date Silking date

2008 ND108 2.8 24 May 1 June 31 JulyND108 5.6 24 May 1 June 31 July

2009 ND108 5.6 8 May 15 May 19 JulyZD958 2.8 8 May 15 May 15 JulyZD958 5.6 8 May 15 May 17 July

2010 ND108 2.8 13 May 21 May 19 July

fia1ipStBmm‘r

obr1Gia(afi1tgdstnG

eodd

2

2

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ND108 5.6

ZD958 2.8ZD958 5.6

nal KW for a wide range of genotypes and environments (Milletnd Pinthus, 1984; Schnyder and Baum, 1992; Saini and Westgate,999; Borrás et al., 2003). After maximum water mass, the water

n a kernel is gradually replaced by dry matter deposition until thehysiological maturity has been reached (Egli and TeKrony, 1997;aini and Westgate, 1999; Sala et al., 2007b). The moisture con-ent declines throughout the grain-filling period (Westgate andoyer, 1986) and it has a close relationship with percentage of dryatter accumulation over a wide range of genotypes and environ-ents (Borrás et al., 2003). The moisture content has been used as a

benchmark’ for estimating kernel development for different envi-onmental conditions (Calderini et al., 2000; Calvino et al., 2002).

Some studies have found that kernel growth rate and durationf linear grain-filling vary for different floret positions on the rachisecause of the internal competition for assimilate and, therefore,esults in differences in final KW (Tollenaar and Daynard, 1978a,978b; Munier-Jolain et al., 1994; Andrade and Ferreiro, 1996;ambín and Borrás, 2005). For maize, the top kernels on the rachis

nitiate their growth 4–5 days later than the basal ones and have higher possibility of abortion prior to the onset of grain-fillingTollenaar and Daynard, 1978a). The later fertilized kernels have

lower kernel growth rate and shorter duration of linear grain-lling which results in a lower final KW (Tollenaar and Daynard,978a, 1978b; Hanft et al., 1986; Muchow, 1990). Detailed informa-ion about the variation of KW with its growth parameters (kernelrowth rate, duration of linear grain-filling), and kernel waterevelopment along the rachis is scarce. A more detailed under-tanding of the underlying physiological mechanisms that controlhe variation in KW is needed in order to be able to improve mecha-istic crop models for a more accurate yield simulation (Borrás andambín, 2010).

The objectives of this research were (i) to investigate the differ-nce in KW along the rachis of the ear; (ii) to determine the impactf kernel growth parameters on final KW, and (iii) to evaluate theynamics of kernel water for different sections of the ear and toetermine the relation with KW.

. Materials and methods

.1. Experimental design

Field experiments were conducted in 2008, 2009 and 2010 athe Shangzhuang experimental farm (40◦08′ N, 116◦10′ E) of Chinagricultural University. The soil was a sandy clay loam (Aquicambisol). Two maize hybrids, ND108 and ZD958 that have the

argest planting acreage in China since 2000 were used in this studynd two different plant densities were evaluated. Row and plantpacing was 0.6 m for the low density treatment (2.8 plants m−2),hile plant spacing was 0.3 m and row spacing was 0.6 m for the

ormal density treatment (5.6 plants m−2). The normal densityepresents the plant density commonly used by local farmers.n 2008, ND108 was planted at both a low and normal densities.n 2009, both hybrids were used for comparison: using low and

13 May 21 May 20 July13 May 21 May 14 July13 May 21 May 18 July

normal densities for hybrid ZD958 and only normal density forhybrid ND108. In 2010, both hybrids were planted at the low andnormal densities. Seed was sown in north-south oriented rows.

Treatments were arranged in a complete block design with tworeplicates in 2008 and 2009, and four replicates in 2010. The sizeof each plot was 7.5 m × 15 m. Water and nutrients were suppliedas needed according to local standard cultivation. Prior to planting,the field was irrigated and fertilized with 187 kg ha−1 of urea and375 kg ha−1 of compound fertilizer (N:P2O5:K2O = 15%:15%:15%).At anthesis, the field was irrigated again and fertilized with195 kg ha−1 of urea. Weeds were removed by hand to avoid anyherbicide influence on plant growth. No plant disease, pest orstress symptoms were observed. Mean daily air temperature wascalculated as the average of daily maximum and minimum airtemperatures collected from a standard weather station at anapproximate distance of 5.6 km from the experimental field.

2.2. Sampling and measurement

The emergence date of each treatment was recorded when 50%of its plots at emergence stage (Ritchie and Hanway, 1982). At least20 plants in each plot representing average plants were tagged at10 d before silking (the first silk visible of the apical ear). The silk-ing date of the apical ear was recorded for each tagged plant andthe subapical ear was bagged prior to silking to prevent pollination.The silking date of each treatment was the mean silking date of itstagged plants. Sowing, emergence and silking dates for each treat-ment are shown in Table 1. In all three years, beginning at 7 d aftersilking (DAS), the apical ear of one plant per plot was sampled every7–10 d until the kernels reached physiological maturity, which wasdefined as the mean moisture content of all sampled kernels of agiven hybrid × density treatment ≤ 350 g kg−1 (Sala et al., 2007b).However, the sampling of the normal density treatment for thehybrid ND108 in 2008 was stopped earlier because of partial plantlodging due to strong winds. After sampling each ear was enclosedin a plastic bag and transported to the laboratory in an insulatedcooler. In 2008 and 2009, one row of kernels for each ear, whichtypically consists of sixteen rows for both hybrids, was selected.Each kernel was numbered in sequence starting at the bottom ofthe ear and then sampled. Aborted kernels in the apical sectionwere not sampled. Fresh weight of each kernel was determined bya balance with an accuracy of 0.001 g. Dry weight of each kernelwas measured with a balance that had an accuracy of 0.0001 g afterdrying in a forced air oven at 80 ◦C for at least 96 h. In 2010, ten ker-nels from the 10th–15th positions and ten kernels from the apicalregion of each ear from the four replicates were sampled. The freshand dry weights of each group of ten kernels were weighted.

2.3. Data analysis

To compare the growth of kernels at different positions of maizeear, four sections were defined in each kernel row: basal (B), lowerthird (L), upper (U) and apical (A) section. These corresponded to

Y. Chen et al. / Field Crops Research 149 (2013) 177–186 179

Table 2The measurements and kernel section definitions for analysis for each experimental year.

Year Replicate Measurement Kernel section definition

2008 and 2009 2 Fresh and dry weight of each kernel in one row of anear

Basal, lower third, upper and apical sectionscorrespond to the 1st–6th, 10th–15th, 28th–33rdfloret positions, and the last six floret positions of theear, respectively.

s fromthe ap

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K

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between basal, upper and apical sections with respect to the lowerthird section, respectively, were compared using the Dunnett-testof the ANOVA procedure using SAS 9.2 (SAS Institute Inc., 2009).

2010 4 Fresh and dry weight of ten kernelthird section and ten kernels from

an ear

he 1st–6th, 10th–15th, 28th–33rd floret positions from the bottomf the rachis, and the last six floret positions at the tip of the ear.he mean value of each section was calculated. The measurementsnd kernel section definitions for analysis for each experimentalear are summarized in Table 2.

The final KW of each section was estimated by fitting a sig-oid model (Eq. (1)) (Acreche and Slafer, 2009) with the kernel dryeight plotted against thermal time from one week after silking tohysiological maturity:

W = a

1 + exp(−b ∗ (TT − c))(1)

here KW is the measured kernel dry weight (mg), TT the ther-al time after silking, a, b and c are the estimated parameters, inhich a is the final kernel weight (mg), b the parameter related

o the rate of change in kernel weight, and c the TT at maximumernel growth rate. Daily thermal time was calculated using 8 ◦Cs the base temperature. We did not consider ceiling temperatureecause the maximum daily mean temperature for the three exper-

mental years was 31.9 ◦C which is lower than 34 ◦C (Jones et al.,986; Ritchie and NeSmith, 1991; Echarte et al., 2006).

Since bi-linear model is commonly adopted in estimating kernelrowth rate at linear grain-filling stage, we applied it (Eqs. (2) and3)) (Gambín et al., 2006) to estimate kernel growth rate during theinear phase. The model was fitted with the kernel dry weight from0% of final KW (Tollenaar and Daynard, 1978b; Muchow, 1990) tohysiological maturity against thermal time:

W = d + k ∗ TT for TT ≤ f (2)

W = d + k ∗ f for TT > f (3)

here KW is the measured kernel dry weight (mg), TT (◦C d) thehermal time after silking, d, k and f are the estimated parameters,n which d the Y-intercept (mg), k the kernel growth rate during theinear grain-filling period (mg ◦C−1 d−1), and f the total grain-fillinguration (◦C d).

As kernels at different positions have different silking dates, thenset of linear grain-filling (TTLGF, ◦C d) also changed with positions.he onset of linear grain-filling for each section can be determineds Eq. (4). The duration of linear grain-filling (LGF, ◦C d) correspondso the thermal time from onset of linear grain-filling to physiolog-cal maturity, is calculated using Eq. (5).

TLGF = −d

k(4)

GF = f + d

k(5)

Fresh and dry weight were used to calculate kernel water masss the difference between fresh and dry weight (mg kernel−1) andoisture content (g kg−1) throughout grain-filling. Kernel maxi-um water mass (mg kernel−1) was determined as the maximum

alues measured during grain-filling for each section in one row. A

arabolic model was used to fit the kernel water mass against TTccording to Eq. (6) (Sala et al., 2007a):

WM = g + h ∗ TT + i ∗ TT1.5 + j ∗ TT2 (6)

the lowerical section of

Lower third and apical sections correspond to the10th–15th and the last six floret positions of the ear,respectively.

where KWM is calculated kernel water mass (mg) from one weekafter silking to physiological maturity, g the Y-intercept (mg), h,i and j are empirical model parameters. The parameters of Eqs.(1)–(6) were estimated using the Gauss–Newton algorithm in non-linear regression of SAS 9.2 (SAS Institute Inc., 2009).

The kernels from the lower third section that consisted of the10th–15th florets have commonly been sampled in previous stud-ies (Borrás et al., 2004; Gambín et al., 2006). The relative change(%) of each growth parameter, including final KW, kernel growthrate, duration of linear grain-filling, onset of linear grain-filling, andmaximum water mass, for each section relative to the lower thirdsection was calculated. The differences in each growth parameter

Fig. 1. Dry weight of the individual kernels referring to their position from the baseto the tip of an ear at different grain-filling stages for hybrid ZD958 with two plantdensities in 2009. The silking dates were 15 July for the low density treatment and17 July for the normal density treatment.

180 Y. Chen et al. / Field Crops Research 149 (2013) 177–186

F ions oZ al plb 33rd fl

3

3

fFtentactiKhs

t

ig. 2. Kernel dry weight dynamics for the basal, lower third, upper and apical sectD958 in 2009 with low and normal plant densities, and ND108 in 2009 with normasal, lower third, upper and apical sections refer to the 1st–6th, 10th–15th, 28th–

. Results

.1. Final KW

The dry weights of individual kernels at different floret positionsor hybrid ZD958 at different growing stages in 2009 are shown inig. 1. During the early grain-filling stage, the individual KW alonghe rachis of the ear for different plant densities were quite close,xcept for the tip kernels that significantly smaller than other ker-els. During the later grain-filling stage, the individual KW aroundhe lower third section was the largest while the KW for the basalnd apical positions was substantially lower, especially for the api-al kernels of the normal density treatments. It should be noted thathe variation in dry weight among adjacent kernels substantiallyncreased during the later grain-filling stage (Fig. 1). The individualW accumulations along the rachis of the ear for the treatments of

ybrid ND108 for 2008 and 2009 have the similar trend (data nothown).

Dynamics of KW accumulation in the four sections showed thathe KW of lower third sections was almost always the largest and

f the ear as a function of thermal time after silking for hybrids ND108 in 2008 andant density. The mean value of each section and the fitted curve is presented. Theoret positions, and the last six floret positions at the tip of the ear, respectively.

that of the apical sections were always the lowest (Fig. 2). Thisresulted in that the final KW of the lower third sections was thelargest except for the low density treatment for the hybrid ND108for 2008, in which the basal section had the largest KW (Table 3).The final KW of the apical section was the smallest and significantlydifferent with that of the lower third sections for all treatments(P < 0.05; Table 3). The final KW of upper section was significantlysmaller than that of the lower third section for the normal den-sity treatment for hybrid ND108 for 2009 (P < 0.05; Table 3). Thepercentage decrease in final KW for the normal density comparedto the low density of each section generally showed that the ker-nel weight of the basal and apical sections had a larger decreasethan those of the lower third and upper sections, expect for theupper section of hybrid ZD958, in which the decrease also was large(Fig. 3).

3.2. Kernel growth parameters

The onset of linear grain-filling (◦C d) varied among the differentsections of the ear. In general, linear grain-filling for the kernels of

Y. Chen et al. / Field Crops Research 149 (2013) 177–186 181

Table 3Final kernel weight, kernel growth rate, duration of linear grain-filling, onset of linear grain-filling, and kernel maximum water mass for the different kernel sections of theear.

Year Hybrid Plant density Section Final kernel weight(mg kernel−1)

Kernel growth rate(mg ◦C−1 d−1)

Duration of lineargrain-filling (◦C d)

Onset of lineargrain-filling (◦C d)

Kernel maximum watermass (mg kernel−1)

2008 ND108 Low B 378* 0.596 641 239* 239*

L 363 0.552 665 204 256U 347* 0.511 691 205 252A 330* 0.501* 693 242* 209*

2008 ND108 Normal B 328 0.560 – 251 192L 352 0.570 – 221 204U 343 0.548 – 245 186A 299* 0.504* – 283* 161*

2009 ND108 Normal B 317 0.424 714 232 169*

L 351 0.437 769 207 187U 293* 0.419 690 244 161*

A 236* 0.397* 625* 306* 147*

2009 ZD958 Low B 396 0.495 770 234 228L 404 0.512 748 211 228U 381 0.467* 774 216 213*

A 346* 0.435* 739 257* 177*

2009 ZD958 Normal B 337 0.386* 812 193 172*

L 365 0.444 801 185 199U 320 0.394* 795 186 163*

A 289* 0.362* 780 230* 138*

2010 ND108 Low L 319 0.469 679 181 200A 228* 0.309* 726 226* 131*

2010 ND108 Normal L 292 0.417 705 164 195A 196* 0.303* 620 214* 135*

2010 ZD958 Low L 328 0.437 768 177 195A 247* 0.357* 702 293* 144*

2010 ZD958 Normal L 297 0.384 793 158 182A 214* 0.313* 685* 237* 133*

parinr l sects

tb(wtao

efwwatcnsbng−o

fatdtdN

* Significant difference at P < 0.05 level determined by Dunnett test in ANOVA comespectively, in each variable × treatment group. Basal, lower third, upper and apicaix floret positions of the ear, respectively.

he lower third sections started first, followed by the kernels of theasal and upper sections, and finally the kernels of the apical sectionTable 3). The onset of the linear grain-filling of the apical sectionsas significantly later than that of the lower third section for all

reatment combinations in three years. In 2008, the basal sectionlso showed a significant difference for the low density treatmentf hybrid ND108 (P < 0.05; Table 3).

The kernel growth rate varied for the different sections of thear. It had the largest values for the lower third sections exceptor the low density treatment for the hybrid ND108 for 2008, inhich the basal section had the largest kernel growth rate (Table 3),hile the kernel growth rates for the upper and apical sections were

lways smaller. For 2008 and 2010, only the apical section for allreatments showed a significant difference in kernel growth rateomparing to the lower third section (P < 0.05; Table 3). In 2009,ot only the apical section for all treatments, but also the upperection of the low and normal densities of hybrid ZD958 and theasal section of the normal density of hybrid ZD958 showed a sig-ificant difference (P < 0.05; Table 3). The relative change in kernelrowth rate from the lower third section to the apical section was17% on average for all normal density treatments, and was −19%n average for all low density treatments (Fig. 4a).

The duration of linear grain-filling varied from 620 to 769 ◦C dor the hybrid ND108 and from 685 to 812 ◦C d for the hybrid ZD958mong the section × density × year treatment combinations. Forhe low density treatments, there was no significant difference in

uration of linear grain-filling of the other sections comparing tohe lower third section (P < 0.05; Table 3). However, for the normalensity treatment, the duration of the apical section for the hybridD108 in 2009 and hybrid ZD958 in 2010 was significantly shorter

g basal (B), upper (U) and apical (A) sections to lower third (L) section on the rachis,ions correspond to the 1st–6th, 10th–15th, 28th–33rd floret positions, and the last

than that of lower third section (P < 0.05; Table 3). The relativechange in duration of the linear grain-filling from the lower thirdsection to the apical section was −12% on average for all normaldensity treatments, and was marginal for low density treatments(Fig. 4b).

The relative change in final KW of the other sections relative tothe lower third section, were both positively correlated with therelative changes in kernel growth rate and duration of linear grain-filling for the normal density treatment (R2 = 0.99; P < 0.01; Fig. 4a;R2 = 0.99; P < 0.01; Fig. 4b). However, the relative changes in finalKW for the other sections relative to the lower third sections, wereonly correlated with the relative changes in kernel growth rate forthe low density treatments (R2 = 0.96; P < 0.05; Fig. 4a).

3.3. Kernel water mass

The water mass of kernels increased rapidly during the early ker-nel growth stage, reached their maximum values around the middlekernel growth stage, and then decreased gradually until physiolog-ical maturity (Fig. 5). The water mass was the highest for the lowerthird sections, and smallest for the apical sections throughout thegrain-filling period (Fig. 5). The results of 2010 were similar (datanot shown).

The developments of kernel moisture content among the sec-tions were extremely similar (Fig. 6; data for 2010 not shown).The kernel moisture content changed from 900 g kg−1 to 300 g kg−1

during the kernel growth period evaluated (Fig. 6). The maximumkernel water mass of the apical section was significantly lowerthan the lower third section for all treatments for the three years(P < 0.05; Table 3). In addition, in 2008 the maximum kernel water

182 Y. Chen et al. / Field Crops Research 149 (2013) 177–186

Fig. 3. Relative change (%) in final kernel weight for each section of the ear for thenormal density treatments relative to the low density treatments for ND108 for2sfl

mmTsslmsatm

4

a

Fig. 4. Relationship between the relative change in final kernel weight and the rel-ative change in kernel growth rate (a) and duration of linear grain-filling (b) for thebasal (�), lower third (•), upper (�) and apical (�) sections relative to the lowerthird section, in normal density (closed symbols) and low density (open symbols)treatments. The basal, lower third, upper and apical sections refer to the 1st–6th,10th–15th, 28th–33rd floret positions, and the last six floret positions at the tip ofthe ear, respectively. Average values of the same plant density from all treatments

008 and ZD958 for 2009. The basal (B), lower third (L), upper (U) and apical (A)ections refer to the 1st–6th, 10th–15th, 28th–33rd floret positions, and the last sixoret positions at the tip of the ear, respectively.

ass of the basal section for hybrid ND108 in low density treat-ent was significantly lower than the lower third section (P < 0.05;

able 3). In 2009, the maximum kernel water mass of the upperection for all treatments, and the basal section of the normal den-ity treatments for both hybrids were significantly lower than theower third section (P < 0.05; Table 3). The relative change in maxi-

um kernel water mass from the lower third section to the apicalection was −28% on average for all treatments (Fig. 7). The rel-tive change in final KW of each section comparing to the lowerhird section was positively correlated with the relative change in

aximum kernel water mass (R2 = 0.99; P < 0.01; Fig. 7).

. Discussion

In previous studies kernels at specific positions of the ear, usu-lly the 10th–15th kernels, were sampled for investigating kernel

were presented, and bars indicate the S.D. The symbol (×) represents the data fromTollenaar and Daynard (1978b); the symbol (+) represents the data from Muchow(1990).

growth over a wide range of genotypes and environmental condi-tions (Borrás et al., 2003; Gambín et al., 2006; Sala et al., 2007a).These studies have shown that kernels from this region have a sig-nificantly larger KW than other regions of the ear (Tollenaar andDaynard, 1978b), which indicates that the variation in growth of

individual kernels along the rachis cannot be neglected. However,information on the difference of kernel growth among the differ-ent ear positions is lacking, and the physiological mechanism thatcontrols this variation is not clear. In this study, the dry matter

Y. Chen et al. / Field Crops Research 149 (2013) 177–186 183

Fig. 5. Dynamics of kernel water mass for the basal, lower third, upper and apical sections of the ear as a function of thermal time after silking for hybrids ND108 in 2008a ormab 3rd fl

awfiwtr

emcfoaaawtti

nd ZD958 in 2009 with low and normal plant densities, and ND108 in 2009 with nasal, lower third, upper and apical sections refer to the 1st–6th, 10th–15th, 28th–3

ccumulation and water mass of kernels for different ear positionsas studied throughout the grain-filling phase. The variation innal KW and kernel growth parameters among sections of the earas analyzed by comparing them with the kernels in the lower

hird section, i.e. the 10th–15th positions, and their underlyingelations were analyzed.

It should be noted that only two ears were sampled fromach treatment in 2008 and 2009 due to heavy time-consumingeasurement in the study. The results for these two years were

onsistent with those for 2010, in which four ears were sampled. Foruture research at least three replicates are recommended throughptimizing experimental design, sample collection and samplenalysis. Kernel growth rate levels off after kernel biomass reachbout 90% of final KW (Tollenaar and Daynard, 1978b; Tollenaarnd Bruulsema, 1988). In this study, we used bilinear models in

hich the ‘level off’ phase was neglected. This can result in devia-

ion in estimating kernel growth rate, although it should not affecthe comparison of growth difference among kernel sections signif-cantly.

l plant density. Mean value of each section and the fitted curve are presented. Theoret positions, and the last six floret positions at the tip of the ear, respectively.

The variation in individual KW among different positions of arachis has been observed in cereal crops, e.g. wheat (Cook andEvans, 1978; Snyder et al., 1993), rice (Patel and Mohapatra, 1996)and sorghum (Gambín and Borrás, 2005). From our one-by-onesample, the visible difference of KW between adjacent kernels inone row of the ear became more apparent toward the end of thegrain-filling phase (Fig. 1). Although it is hard to find an explanationto this variation, the ‘wave-like’ pattern still reflected that unevengrowth existed in local region. One hypothesis is that the kernelthat has a larger size limits the potential growth space of its adja-cent kernels, which cause their differences in final kernel weight.Physical restriction to kernel expansion could reduce individualKW (Kiniry et al., 1990; Gambín et al., 2007b; Sara et al., 2007a).However, no increase in individual KW was found when increas-ing the space around kernels beyond the period of sink strength

set (Gambín et al., 2007b). We found that the growth differenceamong different sections in one row of the ear was significant (Fig. 2and Table 3). The typical distribution of dry matter along the rachisis the highest for the lower third section, lower for the basal and

184 Y. Chen et al. / Field Crops Research 149 (2013) 177–186

F apical

Z al pl1 he ea

uTtrtrvcne

gKerupmssd

ig. 6. Dynamics of kernel moisture content for the basal, lower third, upper and

D958 in 2009 with low and normal plant densities, and ND108 in 2009 with norm0th–15th, 28th–33rd floret positions, and the last six floret positions at the tip of t

pper sections, and the lowest for the apical section (Fig. 1 andable 3). The variation in final KW was, on average, up to 26% forhe two hybrids for the normal density treatment (Fig. 4) whichepresented the commercial plant density for local farmers’ prac-ices (Ma et al., 2008). However, for the low plant density whichepresented a higher assimilates availability for kernel growth, theariation was still substantial (Fig. 4). Such a large variation indi-ated that the individual KW variation along the rachis cannot beeglected for estimation of maize yield, especially for stress-pronenvironments.

Results from other studies showed that the variation in kernelrowth rate is the most important factor for the differences in finalW for different genotypes and environmental conditions (Borrást al., 2003, 2009; Echarte et al., 2006; Gambín et al., 2006). Similaresults have also been found for sorghum with variations in individ-al kernel weight among contrasting positions within the sorghumanicle (Kiniry, 1988; Gambín and Borrás, 2005). In our study for

aize, for the low density treatments in which the assimilate

upply was high, the decrease in final KW of the basal and apicalections comparing to the lower third section was only due to theecrease in kernel growth rate (Fig. 4a). For the normal density

sections of the ear with thermal time after silking for hybrids ND108 in 2008 andant density. The basal, lower third, upper and apical sections refer to the 1st–6th,r, respectively.

treatments, it seemed that the insufficient assimilate supply causedthe shorter duration of linear grain-filling for the later growingkernels, so the decrease of final KW was caused by decrease inkernel growth rate and duration of linear grain-filling (Fig. 4a andb). This result was in accordance with the results from Tollenaarand Daynard (1978b) and Muchow (1990), who showed that thefinal KW, kernel growth rate and duration of linear grain-filling alldecreased from the lower third section along the ear toward thetip section. The relation of the relative change in final KW and therelative change in kernel growth parameters were similar to therelation for the normal density treatments in our study (Fig. 4).

The silking times are different for kernels at different floretpositions (Cárcova and Otegui, 2001; Lizaso et al., 2003). Theflorets on the lower third region of the ear are fertilized first,initiate endosperm cell division earlier, while the apical floretsare inhibited by the growth of earlier fertilized kernels during celldivision, so that the number of cells was restricted and the actual

sink strength was reduced (Reddy and Daynard, 1983; Cárcova andOtegui, 2007). It has been reported that dry matter accumulationof the basal kernels is limited by kernel sink strength regardlessof assimilate supply (Tollenaar and Daynard, 1978b; Frey, 1981).

Y. Chen et al. / Field Crops Resea

Fig. 7. Relation between the relative change in kernel maximum water mass andthe relative change in final kernel weight for basal (�), lower third (•), upper (�) andapical (�) sections relative to the lower third section. The basal, lower third, upperatt

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ccS2imnTwrst

ahdiky

5

eg

nd apical sections refer to the 1st–6th, 10th–15th, 28th–33rd floret positions, andhe last six floret positions at the tip of the ear, respectively. Average values for allreatments are presented, and bars indicate the S.D.

n contrast, the growth of apical kernels is mainly limited byn inadequate assimilate supply rather than their sink strengthHanft et al., 1986). In our study we found that kernels startedinear grain-filling earlier, had a larger final KW, while kernels thattarted linear grain-filling later had a lower final KW (Table 3). Inddition, with an increase in plant density, the decrease of KW forhe apical and basal sections were much larger than that of the

iddle sections (Fig. 3), which indicated that the later fertilizedernels were more sensitive to the change of assimilate supply.enerally, the kernels that start growth earlier seem to have thedvantage that they get sufficient assimilates to ensure that theirink demand can be met in limited assimilate supply conditions.

The maximum kernel water mass has been regarded as an indi-ator of kernel sink capacity (Borrás and Westgate, 2006). It islosely related to final kernel weight (Millet and Pinthus, 1984;chnyder and Baum, 1992; Saini and Westgate, 1999; Borrás et al.,003). Our study showed that these relations are stable and are

ndependent of kernel position (Fig. 7), which indicates that theaximum kernel water mass still could be the indicator of ker-

el sink capacity when applied to different positions of the ear.he developments of kernel moisture content with thermal timeere extremely similar among different sections of the ear, which

eflected the kernels from different positions of the ear have theame progress in dry matter accumulation based on moisture con-ent (Fig. 6).

Canopy-level crop models (Jones et al., 1986; Lizaso et al., 2011)nd organ-level functional–structural models (Guo et al., 2006)ave been developed in order to simulate crop assimilate pro-uction. These models could also integrate the knowledge at the

ndividual kernel level in order to help explain the variation ofernel weight and thus improve their capacity in predicting maizeield for different genotypes and environmental conditions.

. Conclusions

The variation of KW among different floret positions of the maizear was substantial, which is related to changes mostly in kernelrowth rate, and in the duration of the linear grain-filling under the

rch 149 (2013) 177–186 185

condition of insufficient assimilates supply. Differences in final KWare related to changes in maximum water mass, while the devel-opment of moisture content is similar across floret positions of themaize ear. The stable relationship of kernel water and dry matterindicates that kernel water could be used to estimate KW accumu-lation in different floret positions of the ear. This is a promising firststep in finding the physiological mechanism that controls KW vari-ation, which should be integrated into maize simulation models inorder to predict yield more accurately.

Acknowledgements

This work was supported by the National Natural Science Foun-dation of China (Grant No. 30771260). It was also part of the PhDproject of YJ Chen, which was funded by the China ScholarshipCouncil with the support of the AgWeatherNet Program at Wash-ington State University, Prosser, WA, USA.

References

Acreche, M.M., Slafer, G.A., 2009. Grain weight, radiation interception and use effi-ciency as affected by sink-strength in Mediterranean wheats released from 1940to 2005. Field Crops Res. 110, 98–105.

Andrade, F.H., Ferreiro, M.A., 1996. Reproductive growth of maize, sunflower andsoybean at different source levels during grain filling. Field Crops Res. 48,155–165.

Andrade, F.H., Vega, C., Uhart, S., Cirilo, A., Cantarero, M., Valentinuz, O., 1999. Kernelnumber determination in maize. Crop Sci. 39, 453–459.

Barlow, E., Lee, J., Munns, R., Smart, M., 1980. Water relations of the developingwheat grain. Funct. Plant Biol. 7, 519–525.

Borrás, L., Gambín, B.L., 2010. Trait dissection of maize kernel weight: towardsintegrating hierarchical scales using a plant growth approach. Field Crops Res.118, 1–12.

Borrás, L., Slafer, G.A., Otegui, M.E., 2004. Seed dry weight response to source–sinkmanipulations in wheat, maize and soybean: a quantitative reappraisal. FieldCrops Res. 86, 131–146.

Borrás, L., Westgate, M.E., 2006. Predicting maize kernel sink capacity early indevelopment. Field Crops Res. 95, 223–233.

Borrás, L., Westgate, M.E., Otegui, M.E., 2003. Control of kernel weight and ker-nel water relations by post-flowering source–sink ratio in maize. Ann. Bot. 91,857–867.

Borrás, L., Zinselmeier, C., Senior, M.L., Westgate, M.E., Muszynski, M.G., 2009. Char-acterization of grain-filling patterns in diverse maize germplasm. Crop Sci. 49,999–1009.

Brooks, A., Jenner, C., Aspinall, D., 1982. Effects of water deficit on endospermstarch granules and on grain physiology of wheat and barley. Funct. Plant Biol.9, 423–436.

Calderini, D.F., Abeledo, L.G., Slafer, G.A., 2000. Physiological maturity in wheatbased on kernel water and dry matter. Agron. J. 92, 895–901.

Calvino, P.A., Studdert, G.A., Abbate, P.E., Andrade, F.H., Redolatti, M., 2002. Use ofnon-selective herbicides for wheat physiological and harvest maturity acceler-ation. Field Crops Res. 77, 191–199.

Capitanio, R., Gentinetta, E., Motto, M., 1983. Grain weight and its components inmaize inbred lines. Maydica 28, 365–379.

Cárcova, J., Otegui, M.E., 2001. Ear temperature and pollination timing effects onmaize kernel set. Crop Sci. 41, 1809–1815.

Cárcova, J., Otegui, M.E., 2007. Ovary growth and maize kernel set. Crop Sci. 47,1104–1110.

Chapman, S.C., Edmeades, G.O., 1999. Selection improves drought tolerance in trop-ical maize populations: II. Direct and correlated responses among secondarytraits. Crop Sci. 39, 1315–1324.

Cook, M., Evans, L., 1978. Effect of relative size and distance of competing sinkson the distribution of photosynthetic assimilates in wheat. Funct. Plant Biol. 5,495–509.

Echarte, L., Andrade, F.H., Sadras, V.O., Abbate, P., 2006. Kernel weight and itsresponse to source manipulations during grain filling in Argentinean maizehybrids released in different decades. Field Crops Res. 96, 307–312.

Egharevba, P.N., Horrocks, R.D., Zuber, M.S., 1976. Dry matter accumulation in maizein response to defoliation. Agron. J. 68, 40–43.

Egli, D.B., TeKrony, D.M., 1997. Species differences in seed water status during seedmaturation and germination. Seed Sci. Res. 7, 3–12.

Frey, N.M., 1981. Dry matter accumulation in kernels of maize. Crop Sci. 21, 118–122.Gambín, B.L., Borrás, L., 2005. Sorghum kernel weight. Crop Sci. 45, 553–561.Gambín, B.L., Borrás, L., Otegui, M.E., 2006. Source–sink relations and kernel weight

differences in maize temperate hybrids. Field Crops Res. 95, 316–326.Gambín, B.L., Borrás, L., Otegui, M.E., 2007a. Kernel water relations and duration of

grain filling in maize temperate hybrids. Field Crops Res. 101, 1–9.Gambín, B.L., Borrás, L., Otegui, M.E., 2007b. Is maize kernel size limited by its

capacity to expand? Maydica 52, 431–441.

1 Resea

G

H

J

K

K

L

L

M

M

M

M

O

P

P

R

86 Y. Chen et al. / Field Crops

uo, Y., Ma, Y., Zhan, Z., Li, B., Dingkuhn, M., Luquet, D., de Reffye, P., 2006. Parameteroptimization and field validation of the functional–structural model GREENLABfor maize. Ann. Bot. 97, 217–230.

anft, J.M., Jones, R.J., Stumme, A.B., 1986. Dry matter accumulation and carbohy-drate concentration patterns of field-grown and in vitro cultured maize kernelsfrom the tip and middle ear positions. Crop Sci. 26, 568–572.

ones, C.A., Kiniry, J.R., 1986. CERES-Maize: A Simulation Model of Maize Growthand Development. Texas A&M University Press, College Station, Texas.

iniry, J.R., 1988. Kernel weight increase in response to decreased kernel numberin sorghum. Agron. J. 80, 221–226.

iniry, J.R., Wood, C.A., Spanel, D.A., Bockholt, A.J., 1990. Seed weight response todecreased seed number in maize. Agron. J. 82, 98–102.

izaso, J.I., Boote, K.J., Jones, J.W., Porter, C.H., Echarte, L., Westgate, M.E., Sonohat, G.,2011. CSM-IXIM: a new maize simulation model for DSSAT version 4.5. Agron.J. 103, 766–779.

izaso, J.I., Westgate, M.E., Batchelor, W.D., Fonseca, A., 2003. Predicting poten-tial kernel set in maize from simple flowering characteristics. Crop Sci. 43,892–903.

a, Y., Wen, M., Guo, Y., Li, B., Cournède, P.H., de Reffye, P., 2008. Parameter opti-mization and field validation of the functional–structural model GREENLAB formaize at different population densities. Ann. Bot. 101, 1185–1194.

illet, E., Pinthus, M.J., 1984. The association between grain volume and grainweight in wheat. J. Cereal Sci. 2, 31–35.

uchow, R.C., 1990. Effect of high temperature on grain-growth in field-grownmaize. Field Crops Res. 23, 145–158.

unier-Jolain, N., Ney, B., Duthion, C., 1994. Reproductive development of anindeterminate soybean as affected by morphological position. Crop Sci. 34,1009–1013.

tegui, M.E., 1995. Prolificacy and grain yield components in modern Argentinianmaize hybrids. Maydica 40, 371–376.

atel, R., Mohapatra, P., 1996. Assimilate partitioning within floret components ofcontrasting rice spikelets producing qualitatively different types of grains. Funct.

Plant Biol. 23, 85–92.

epler, S., Gooding, M.J., Ellis, R.H., 2006. Modelling simultaneously water contentand dry matter dynamics of wheat grains. Field Crops Res. 95, 49–63.

eddy, V.M., Daynard, T.B., 1983. Endosperm characteristics associated with rate ofgrain filling and kernel size in corn. Maydica 28, 339–355.

rch 149 (2013) 177–186

Ritchie, J.T., NeSmith, D.S., 1991. Temperature and Crop Development. In: Hanks, J.,Ritchie, J.T. (Eds.), Modeling Plant and Soil Systems-Agronomy Monograph No.31. American Society of Agronomy, Inc., Crop Science Society of America, Inc.,Soil Science Society of America, Inc., Madison, WI, pp. 5–29.

Ritchie, S.W., Hanway, J.J., 1982. How a corn plant develops. Special report. IowaState University of Science and Technology, Cooperative Extension Service,Ames, IA.

Saini, H.S., Westgate, M.E., 1999. Reproductive development in grain crops dur-ing drought. In: Donald, L.S. (Ed.), Advances in Agronomy. Academic Press, pp.59–96.

Sala, R.G., Westgate, M.E., Andrade, F.H., 2007a. Source/sink ratio and the relation-ship between maximum water content, maximum volume, and final dry weightof maize kernels. Field Crops Res. 101, 19–25.

Sala, R.G., Andrade, F.H., Westgate, M.E., 2007b. Maize kernel moisture at physio-logical maturity as affected by the source–sink relationship during grain filling.Crop Sci. 47, 711–714.

SAS Institute Inc., 2009. SAS 9.2. SAS 9.2 SQL Procedure User’s Guide. SAS InstituteInc., Cary, NC.

Schnyder, H., Baum, U., 1992. Growth of the grain of wheat (Triticum aestivum L.), Therelationship between water content and dry matter accumulation [sink capacity,dry matter accumulation]. Eur. J. Agron. 1, 51–57.

Slafer, G.A., Savin, R., 1994. Source–sink relationships and grain mass at differentpositions within the spike in wheat. Field Crops Res. 37, 39–49.

Snyder, G.W., Sammons, D.J., Sicher, R.C., 1993. Spike removal effects on dry mat-ter production, assimilate distribution and grain yields of three soft red winterwheat genotypes. Field Crops Res. 33, 1–11.

Tollenaar, M., Bruulsema, T.W., 1988. Effects of temperature on rate and durationof kernel dry matter accumulation of maize. Can. J. Plant. Sci. 68, 935–940.

Tollenaar, M., Daynard, T.B., 1978a. Dry weight, soluble sugar content, and starchcontent of maize kernels during the early postsilking period. Can. J. Plant. Sci.58, 199–206.

Tollenaar, M., Daynard, T.B., 1978b. Kernel growth and development at two positions

on the ear of maize (Zea mays). Can. J. Plant. Sci. 58, 189–197.

Westgate, M.E., 1994. Water status and development of the maize endosperm andembryo during drought. Crop Sci. 34, 76–83.

Westgate, M.E., Boyer, J.S., 1986. Water status of the developing grain of maize.Agron. J. 78, 714–719.