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Crop Science 43:914-920 (2003)
© 2003 Crop Science Society of America

CROP PHYSIOLOGY & METABOLISM

Silk Elongation in Maize

Relationship with Flower Development and Pollination

J. Cárcova*,a, B. Andrieub and M. E. Oteguia

a Dep. de Producción Vegetal, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martín 4453, Buenos Aires (C1417DSE), Argentina
b INRA– Unité Environnement et Grandes Cultures, 78850 Thiverval Grignon, France

* Corresponding author (jcarcova{at}agro.uba.ar)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In maize (Zea mays L.), the gradient in floret development and silk length along the ear at silking determines a time lag between early- and late-appearing silks, which results in pollination asynchrony between them. This asynchrony is partially responsible of reduced kernel set at the ear tip, and hybrids differ in this trait. The objective of this work was to analyze the pattern of floret and silk differentiation and elongation at different spikelet positions (Sn) along the apical ear of two hybrids of contrasting ear size (DEA {cong} 500 spikelets ear-1; DK696 {cong} 800 spikelets ear-1). At silking, both hybrids had reached approximately the same proportion of final ear length (about 44%), but DK696 had differentiated a greater number of spikelets row-1 (46 spikelets) than DEA (33 spikelets). Silk initiation rate was always faster than spikelet initiation rate, and silk extension dynamics was similar for all spikelet positions. Silks from the base of the ear were always longer than those from the tip (S25 in DEA or S35 in DK696). Before pollination, silks experienced an early phase of exponential elongation followed by a phase of linear growth. A drastic reduction in elongation rate followed silk emergence, which did not occur when ears were bagged and pollination was prevented. Convergence in silking among spikelets along the ear could be attained by (i) synchronous silk initiation among spikelet positions, followed by a similar pattern of silk elongation in all florets (hybrid DEA), or (ii) increased silk elongation rate in apical florets (hybrid DK696).

Abbreviations: DAS, days after silking • E1, apical ear • Sn, spikelet number n from the base to the tip of the ear • SL, silk length • TT, thermal time • Vn, leaf stage n


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
IN MAIZE, the harvestable organ is produced by an axillary inflorescence, commonly known as the ear and botanically described as a modified spike. The ear consists of a set of sessile, female pistillated flowers, which are protected from the environment by several layers of husks (modified leaves, mostly represented by the sheaths). In natural conditions, the delay in extension between silks along the ear, together with the position-dependent length required for a silk to emerge (Bonnett, 1966) determines a time lag between the first-appearing silks (from the lower half of the ear) and the late-appearing ones (from the tip of the ear), which results in pollination asynchrony between them. Pollination asynchrony could be partially offset by bagging the ears before silking to delay fertilization of early-silking ovaries. This manipulation allowed silks to receive pollen simultaneously when ears were hand pollinated 5 to 6 d after silking (Cárcova et al., 2000). The result of this artificial convergence in pollination timing was an improved kernel set (Sarquís et al., 1998; Cárcova et al., 2000), suggesting that the rates of silk emergence and pollination might explain part of the genotypic differences observed in final kernel number. Thus, a better knowledge of the pattern of ear development and growth would help identify traits that integrate the effects of several basic processes related to kernel set (Edmeades et al., 2000).

Floret development and silk elongation along the ear seem to depend on early developmental events, like ear meristem initiation and growth (Cheng et al., 1983; Ruget and Duburcq, 1983; Stevens et al., 1986). These characteristics, together with potential ear size, are under a strong genetic control (Bonhomme et al., 1984; Otegui and Melón, 1997), but can be modified by environmental conditions (Lejeune and Bernier, 1996). Anatomical aspects of organogenesis (Bonnett, 1966; Cheng et al., 1983; Stevens et al., 1986) and the effects of environmental factors on the early steps of ear growth (Jacobs and Pearson, 1991; Lejeune and Bernier, 1996) have been previously addressed. Silk elongation and longevity have been well characterized only for the postsilking period (Sadras et al., 1985; Bassetti and Westgate, 1993a, b). On the other hand, few reported studies have examined the relationship between early development and growth events within the ear (Otegui and Melón, 1997; Otegui, 1997). The association between the ontogenic order of floret differentiation within the ear and the pattern of presilking silk elongation has not been studied in detail. Reported data on ear length indicated a uniform pattern among hybrids and environments when data were referred to the date of silking and were normalized by the final ear size (Otegui and Bonhomme, 1998). Conversely, the rate of silk appearance differed among hybrids of contrasting ear size (Bassetti and Westgate, 1993a,b; Cárcova et al., 2000), but data are controversial and inadequate to build a general model.

The objective of the present work was to analyze the pattern of floret and silk differentiation along the ear of two hybrids of contrasting ear size (i.e., number of spikelets per ear) to (i) establish the relationship between spikelet initiation and silk initiation, (ii) characterize the pattern of silk elongation before and after silking, and (iii) evaluate the role of silk emergence (i.e., exposure to sunlight) and/or pollination on the pattern of silk elongation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Crop Husbandry
Field experiments were conducted in two contrasting environments: (i) on a silty loam soil (Typic Eutrochrept, Soil Survey Staff, 1996) at Grignon, France (48°51'N, 1°58'E), during 2000, and (ii) on a silty clay loam soil (Vertic Argiudol, Soil Survey Staff, 1996) at Buenos Aires, Argentina (34°25'S, 58°25'W), during the 2000-2001 growing season. In France, the small-eared ({approx}500 spikelets ear-1; Otegui and Bonhomme, 1998), non-prolific hybrid DEA was machine-planted on 15 May at 10 plants m-2. The plot was 40 rows, 0.8 m apart, and 100 m long. The site was fertilized at planting with 100 kg P ha-1, 100 kg K ha-1, and 140 kg N ha-1, and at the four-leaf stage (V4, ligulated leaves) with 30 kg N ha-1. In Argentina, the large-eared ({approx}800 spikelets ear-1), semiprolific hybrid DK696 was sown on 10 November at 8 plants m-2. The plot was hand-planted at three seeds per hill and thinned at V3. The experiment covered 12 rows, 0.7 m apart by 20 m length, and was fertilized with 150 kg of N ha-1 at V5. Weeds were controlled with 4 L ha-1 half-strength atrazine (2-chloro-4-ethylamino-6-isopropylamino-1,3,5-triazine) when planted, and by hand weeding after the crop was established. Water stress was prevented with sprinkler irrigation, with soil water content near field capacity throughout the growing season.

Measurements
Leaf phenology was determined on approximately 100 plants at V3, and 20 uniform, representative plants were tagged within the population. The number of ligulated leaves and visible leaf tips were recorded twice a week on these tagged plants.

Floral development of the uppermost axillary bud was inspected daily, between V4 (France) or V10 (Argentina) and 10 d after silking (DAS), by dissecting the ears of three untagged plants. Plants were taken from the inner rows of each experiment, leaving at least three (France) or two (Argentina) border rows on each side, starting at 5 m (France) or 2 m (Argentina) from the end of each plot, and leaving at least 1m between consecutive sampling sites. Plants sampled for dissection always had the same number of emerged leaves as the 20-tagged plants. In France, observations started before panicle initiation, and ear initiation was recognized as an elongation of the apical meristem of the axillary bud (Stevens et al., 1986). In Argentina, there were already 18 differentiated spikelets row-1 in the apical ear (E1) at the first sampling date. Therefore, the time of E1 initiation was later estimated, assuming that the initiation rate of the first spikelets was the same as in the related (half-sib) hybrid DK638 (Otegui and Melón, 1997).

The number of spikelets per row and total ear length from the lowest to the uppermost spikelet were measured on each sampled ear. Spikelets along the ear were numbered acropetally, and Sn identifies the position of a spikelet on a row relative to the base of the ear. In France, the pattern of spikelet elongation was examined at different sections along the ear. Sections were identified as (i) Section 1, between the base of the ear and S10, (ii) Section 2, between S11 and S20, and (iii) Section 3, between S21 and S30. For each section, measurements started after the corresponding spikelets (e.g., S11 to S20) were differentiated in the meristem. The length of an individual spikelet within a section was estimated as one tenth of the section length (i.e., an average spikelet length), and was assumed to be representative of the central spikelet of each section (e.g., S5, S15, S25).

Kinetics of silk extension was characterized (i) for the central spikelet of each section (i.e., S5, S15, and S25) in France or (ii) for S5, S10, S15, S20, S25, S30, S35, and S40 in Argentina. Observations were made by means of a 50x binocular microscope in France, and a 16x binocular microscope in Argentina. Measurements started when silks were at least 0.01 cm long, and continued up to 7 d after silking (DAS) or until no effective extension could be detected because of silk senescence. To characterize silk elongation after silking, two treatments were established in Argentina: open pollination and no pollination. Only open-pollinated ears were studied in France. For the no pollination treatment, apical ears were bagged just before silking with 30 µm transparent plastic bags to avoid pollination and to allow exposure of silks to sunlight. Light quality inside the bag was characterized by means of a Skye sensor (SKR 110 Model, Llandrindod Wells, UK), which determines the red to far-red ratio. Measurements were also made inside opaque white bags like those used by Bassetti and Westgate (1993a) for silk growth analysis. Twenty-one uniform plants were tagged at random in each treatment before silking, and the date of silking (first silks visible) was recorded individually for each plant. Between silking (Day 1) and 7 DAS, silk length for the above-mentioned flower positions was determined daily on three plants per treatment (open- and nonpollinated). The progress of silk emergence in relation to flower position (Bassetti and Westgate, 1993a) was also recorded.

Weather Data and Data Analysis
Air temperature at a 15-cm height was recorded hourly at each site in a meteorological station located in the experimental field. Thermal units (°C d) were calculated from daily average temperature above 9.7° (Durand et al., 1982; Ben Haj Salah and Tardieu, 1996) and accumulated from E1 differentiation until 7 DAS.

Exponential and linear models were calculated between silk length and accumulated thermal time (TT) for specific flower positions. For computing these relationships, TT was set to zero at silking (i.e., negative values of TT for the presilking period and positive ones after silking), which was an unambiguously identifiable event for any plant, and observed silk lengths were referred to it. Alternatively, to compare silk elongation kinetics between floret positions, TT was also calculated taking as reference a commonly measured silk length (0.02 cm) for the corresponding floret position. The median of the three plants sampled everyday was used to fit silk elongation models. The limit between the exponential and the linear phases was established based on the rate of silk elongation between two successive measures. Regression analysis was applied to the relationships under study and the parameters of the fitted models were statistically compared. A t test analysis was used to determine significant (P < 0.05) differences between treatment averages.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The relationship between ear elongation and TT was well described by an exponential function (Fig. 1) , which was fitted separately to each hybrid. Final ear length was 12.9 cm for the DEA and 21.7 cm for the DK696, and ear elongation rate was of 0.013 cm (°Cd)-1 for the former and 0.0086 cm (°Cd)-1 for the latter. The proportion of final ear length attained at silking was almost the same for both hybrids (41% for DEA and 46% for DK696). Hybrid DEA differentiated 33.3 ± 1.2 spikelets row-1 (Fig. 2) . The first 10 spikelets were initiated in less than 20°C d at a rate of at least 0.47 spikelets (°Cd)-1. Spikelets 10 to 30 were initiated at an almost constant and lower rate (0.18 spikelets (°Cd)-1). The last three spikelets were initiated at a decreasing rate. Hybrid DK696 differentiated 46.3 ± 1.1 spikelets row-1, and the rate of initiation of S20 to S43 (0.17 spikelets (°Cd)-1) almost equaled that of DEA for spikelets above S10 (Fig. 2).



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  		Fig. 1. Apical ear length as a function of thermal time from apical ear differentiation in hybrids DK696 (Argentina) and DEA (France). Thermal time was calculated using a base temperature of 9.7°C. Arrows indicate silking.

 


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  		Fig. 2. Number of initiated spikelets, visible initiated silks and emerged silks as a function of thermal time from apical ear differentiation in hybrids DEA and DK696.

 
Silks from S1 to S10 were first visible (i.e., length about 0.02 cm) almost simultaneously (Fig. 2). Initiation of silks at higher flower positions was also very fast up to S25 for both hybrids, and then declined (DK696). The rate of visible silk initiation between S5 and S15 (1.25 silks (°Cd)-1 for DEA and 1.8 silks (°Cd)-1 for DK696) was higher than the rate of spikelet initiation. Thus, the delay between spikelet initiation and visible silk initiations was larger for flowers at the base (113°C d for DEA and 137°C d for DK696 between S1 and S15) than at the tip of the ear (83°C d for DEA and 86°C d for DK696 at S25).

Thermal time from silk initiation to emergence from the husks was 368°C d in DK696 and 178°C d in DEA. At the arrest of spikelet differentiation at the ear tip (initiation of spikelet 46 in DK696 and 33 in DEA) the length of the longest silk (S5) was 0.26 cm in DK696 and 0.03 cm in DEA. The time lag between visible silk initiation at a given floret and the corresponding silk extrusion from the husk was independent of flower position along the ear in both genotypes. Silks from successive florets emerged from the husks at essentially a constant TT from the date they were first observed.

Silk extension dynamic was similar for both hybrids and all flower positions (Fig. 3) . Final silk length, however, varied among flower positions and pollination conditions. Pollinated silks at a given spikelet order along the ear of the DK696 were always shorter then their nonpollinated counterparts. Final length of the former was always less than 4 cm longer than the length attained at silking for all flower positions. On the other hand, final length of nonpollinated silks (e.g., 22 cm for S35) was two or three times their length at silking (e.g., 6 for S35), depending on flower position (Fig. 3).



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  		Fig. 3. Silk length as a function of thermal time from silking for open-pollinated ears in DEA and DK696 and for non-pollinated ears in DK696. Values and arrows indicate thermal time at a commonly silk length measure ({cong} 0.02 cm) for selected spikelet positions (Sn).

 
When TT was set to zero at silking two phases could be distinguished in the kinetics of presilking silk extension: (i) an early phase of exponential elongation (Phase 1, Table 1) and (ii) a later phase of linear elongation (Phase 2, Table 2) . In nonpollinated ears of DK696, Phase 2 extended up to 100°C d after silk emergence. For open pollinated ears of DK696, a postpollination linear phase was distinguished (Phase 3). Final silk length was shorter for pollinated than for nonpollinated ears because of the early silk senescence of the former (Fig. 3). Only Phases 1 and 3 could be characterized for open-pollinated ears of DEA (Table 1 and 2). Phase 2 could not be distinguished in this hybrid because the exponential phase lasted almost up to silking and silk length was not measured in bagged ears. Consequently, silks were pollinated almost immediately after the end of Phase 1 and started Phase 3.


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  		Table 1. Models fitted to the relationship between silk length (SL) and thermal time (TT) from silking during the exponential phase (Phase 1) of silk growth. The duration of Phase 1 and silk length achieved for each flower position at the end of the exponential phase are also presented.

 

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  		Table 2. Models fitted to the relationship between silk length (SL) and thermal time (TT) from silking during the linear phases. Phase 2: linear elongation for bagged ears, Phase 3: postpollination linear elongation in open pollinated ears. In DK696 no postpollination elongation was detected for S20 to S40.

 
Thermal time to reach a silk length of 0.02 cm was longer from the base to the tip of the ear (Fig. 3), and a delay of 78 (DK696) or 31(DEA) °C d was established between S25 and S5 for this event. When TT was calculated from a commonly measured silk length (0.02 cm) onwards for each flower position, the kinetics of silk elongation could be clearly compared among them for each hybrid (Fig. 4) . Hybrid DEA exhibited a uniform pattern of silk elongation along the ear. The slight delay in initiation from S5 to S25 (31°C d) was compensated by a shorter distance to the tip of the husks for S25 than for S5, that resulted in slightly reduced TT requirements between silk initiation and silking itself for the former (Fig. 4). All spikelets had a similar extension rate in Phase 1 and there is a trend of a longer duration of this phase for S25 (Table 1). However, silks from the tip required the same TT as those from the bottom to emerge from the husks, though the former needed to elongate a shorter distance to emerge than the latter. For the DK696, the trend (only statistically significant in Phase 2) from the base to the tip of the ear was to (i) increase the elongation rate (Table 2) and (ii) decrease the duration of Phase 1. Thermal time requirement between a commonly measured silk length and silking itself for each flower position decreased from base to tip in both hybrids (Fig. 4), suggesting that increased elongation rates could have compensated for a shorter duration of exponential elongation (Table 1).



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  		Fig. 4. Silk elongation pattern for three (hybrid DEA) and four (hybrid DK696) selected spikelet positions (Sn). Values and arrows indicate thermal time (TT) at silk emergence from the husks for each Sn. Solid lines represent fitted exponential and linear models. Data correspond to open-pollinated ears in DEA and bagged-ears in DK696.

 
The relationship between silk length and spikelet length was similar for all flower positions (S5, S15, and S25) evaluated in hybrid DEA (Fig. 5) . Once silks reached a length between 0.2 and 0.5 cm, silk extension increased sharply in comparison to spikelet elongation, and the relationship between them became dependent on flower position. Below this threshold, silk extension was six times larger than spikelet extension, independently of floret position. Above this threshold, silk extension was 35, 24, and 23 times greater than spikelet extension for S5, S15, and S25, respectively. In hybrid DK696, silk length of S5, S10, and S15 at the end of spikelet initiation was between 0.2 and 0.3 cm.



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  		Fig. 5. Relationship between spikelet and silk length for different spikelet positions along the ears of hybrid DEA. Sections 1, 2 and 3 correspond to flowers 1-10, 11-20 and 21-30 from the base to the tip of the ear, respectively. Solid lines indicate the fitted linear models.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Our data on ear elongation are in close agreement with previous findings (Otegui and Bonhomme, 1998), which determined that hybrids differed in maximum ear length but not in the proportion of final ear length attained at silking. Collectively, it can be stated that there is a clear genotypic difference for potential ear growth (expressed as length), but a very species-dependent timing for this growth to take place. The potential for ear elongation is mainly reflected in the number of spikelets per row. Part of the variation was due to differences in relation to spikelet differentiation arrest, which can range between two weeks before silking (Ruget and Duburcq, 1983) and silking itself (Bonnett, 1966; Fischer and Palmer, 1984).

Data in the present work indicate that estimated initiation of the first silks (S5) occurred before the arrest of floret differentiation at the tip of the ear in both hybrids. First silks of 0.02 cm were observed 10°C d before the arrest of spikelet differentiation in the ear meristem of DEA and almost a week in advance (84°C d) in DK696. We were better able to compare the timing of spikelet differentiation and silk initiation than Otegui (1997) because our data were based on daily observations. The long-eared hybrid (DK696) had a delayed silk elongation, which together with a slower silk extension rate resulted in a longer time lag between silk differentiation and silking than was the case in the short-eared hybrid (DEA).

The pattern of silk elongation was similar for all flower positions along the ear but with an ontogenic delay from base to tip, as reported previously for other ear developmental processes (Bonnett, 1966; Ruget and Duburcq, 1983; Otegui, 1997). On the basis of data from bagged ears of DK696, where no restriction (i.e., pollination) was impossed on silk elongation, it was determined that most of the final silk length was formed during the linear phase of elongation (Phase 2), as in other organs like internodes and leaves (Ritchie and NeSmith, 1991; Fournier and Andrieu, 2000). Our results from pollinated and bagged ears of DK696 showed that the drastic reduction in silk elongation after silking could possibly be due to pollination, but was probably not the result of the perception of sunlight as observed for coleoptiles and leaves (Karlen and Camp, 1985). This evidence differs from data obtained by Bassetti and Westgate (1993a), who observed a decreasing rate of silk elongation early after silking. Differences are probably related to the type of bag used to cover the ears, which were transparent in our experiment and opaque in their work, creating a difference in light quality (red to far-red ratio of 1.07 for transparent bags and 0.81 for opaque bags) for which there is no reference of possible effects on silk elongation, like there is for other organs (Karlen and Camp, 1985). The delay between spikelet and silk initiation at a given floret position decreased from base to tip along the ear. For the short-eared DEA, however, convergence in silking among flowers was mostly related to synchronous silk initiation along the ear, with almost no difference in the pattern of silk elongation among flowers. For the long-eared DK696 this convergence was mainly based on increasing elongation rates from the base to the tip of the ear, both in Phases 1 and 2. The former is a development-based response, while the latter is a growth-related one and consequently may be more dependent on environmental conditions that control growth (e.g., water, light). Future studies should determine (i) the effect on kernel set under stress conditions of each response pattern, to test the hypothesis of the convenience of selecting for short ears (i.e., reduced number of spikelets per row) when breeding for stress prone environments (Lafitte and Edmeades, 1995), and (ii) if synchronous silk initiation is always related to short ears or can be selected independently of ear size.

Finally, silk elongation in hybrid DEA proceeded at two highly different rates with respect to spikelet elongation, which was higher once a silk length of approximately 0.3 cm had been attained. This change in relative growth of both structures has never been reported previously and may be indicative of a shift in assimilate partitioning within the ear, which could not be detected from silk elongation patterns.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Hybrids used in this study had a distinctive number of spikelets per row and displayed different rates of ear and silk elongation. However, a similar trend was observed for (i) the proportion of ear size reached at silking, (ii) the dynamic of spikelet and silk initiation, and (iii) the pattern of silk elongation, which was repetitive along the ear and acropetally delayed in time. Silk elongation exhibited an early phase of exponential growth that was followed by a linear phase of growth. Most part of silk elongation took place during the latter for all flower positions studied in both hybrids. Silk elongation was drastically reduced after silking when pollination was permitted. When pollination was prevented, silk elongation maintained the high presilking expansion rate. Exposure of silks to sunlight does not seem to affect silk extension. Finally, convergence in silking among spikelets could be attained by (i) synchronous silk initiation along the ear and a similar pattern of silk elongation among florets (as in hybrid DEA) or (ii) an increased silk elongation rate from the base to the tip of the ear (as in hybrid DK696).


   ACKNOWLEDGMENTS
 
Thanks to G. Litwin and A. Fortineau for their helpful assistance in field experiments, and to R. Ruiz for his advice with statistical analyses. This work was supported by Fundación Antorchas, INRA, SecyT-Ecos (A98B03), the Univ. of Buenos Aires (AG012), the National Council for Research (CONICET), and the National Agency for Promotion of Science and Technology (PICT 08-06608). J. Cárcova held a grant from Fundación Antorchas and M.E. Otegui is a member of CONICET.

Received for publication December 5, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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