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CROP PHYSIOLOGY & METABOLISM

Synchronous Pollination within and between Ears Improves Kernel Set in Maize

^a Cátedra de Cereales, Dep. de Producción Vegetal, Fac. de Agronomía, Univ. de Buenos Aires, Av. San Martín 4453, Buenos Aires (1417), Argentina
^b Dep. of Agronomy, Iowa State Univ., 1563 Agronomy Hall, Ames, IA 50011-1010 USA

otegui{at}mail.agro.uba.ar

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
In maize (Zea mays L.), the later-fertilized ovaries often abort, thereby reducing kernel set. We examined whether altering the time interval between pollination of florets within an ear or between ears could affect final kernel number per plant. Synchrony of pollination was varied by natural- and hand-pollination of four hybrids, contrasting in prolificacy (ears plant^-1). Plants were grown in the field at low (2.5 and 3 plants m^-2) and high (7.5 and 9 plants m^-2) plant populations, without water or nutrient stress. Increasing plant population generally delayed silk appearance, but most silks were exposed within 5 d after silking (DAS). Synchronous pollination of all exposed silks on apical and sub-apical ears 5 DAS improved kernel number (KN) per plant and the floret fertility index (FFI = number of kernels/number of pollinated silks), relative to open-pollinated plants. At low plant populations, the KN plant^-1 increase resulted primarily from a large increase (39–535%, depending upon the hybrid) in kernels on sub-apical ears. At high plant populations, only apical ears set kernels. Synchronous pollination increased KN in these ears 8 to 31%, depending on the hybrid. Thus, timing of pollination had a large impact on kernel set, and the disadvantage associated with an ontogenetic delay in silk emergence could be partially overcome by synchronous pollination. Because delayed pollination of early-silking ovaries allowed a greater number of the late-silking ones to set kernels, factors other than assimilate availability per fertile floret likely are involved in controlling kernel set.

Abbreviations: DAS, days after silking • E_n, ear number n • ESI, ear silking interval • FFI_n, floret fertility index of ear n • FPE, florets per ear • KN, kernel number

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
CLOSE SYNCHRONY between pollen shed and silk emergence is required for high kernel set in maize. Under stress conditions, silk emergence is delayed relative to pollen shed (Herrero and Johnson, 1981; Jacobs and Pearson, 1991; Bassetti and Westgate, 1993c), which results in lack of pollen for late-appearing silks on apical ears (Hall et al., 1982), reduced silk emergence from sub-apical ears (Hall et al., 1980), failure in ovary fertilization, and ultimately, reduced kernel set (Hall et al., 1981). Fortunately, intense selection for a shorter anthesis-silking interval has improved prolificacy (i.e., number of kernel bearing ears per plant), kernel number (KN), and grain yield in maize under drought conditions (Bolaños and Edmeades, 1993). Similar increases in kernel set resulted when pollination of apical and sub-apical ear shoots was artificially synchronized by hand-pollination (Harris et al., 1976; Sarquís et al., 1998). Nevertheless, abortion of fertilized ovaries at the tip of the ear occurred even when excess pollen was applied to their late-appearing silks (Otegui et al., 1995). Therefore, factors other than greater pollen availability must be involved in improving final KN in response to a shorter interval between anthesis and silking, or between pollination of individual florets.

Research on KN determination in maize has demonstrated that kernel abortion can be partially overcome by increasing assimilate supply of plants under water stress (Boyle et al., 1991; Schussler and Westgate, 1995; Zinselmeier et al., 1995) or low-light stress (Schussler and Westgate, 1991; Otegui, 1997). Nevertheless, these studies did not exclude possible interactions with other mechanisms controlling kernel formation (Boyle et al., 1991, Zinselmeier et al., 1995). Little knowledge exists, for example, on hormone-mediated dominance signals (Bangerth, 1989; Dietrich et al., 1995) or the effect of pollination rate within and between ears (i.e., number of silks that are pollinated simultaneously) on KN determination. In an early study, Freier et al. (1984) reported a significant reduction in kernel set in apical ear positions when the pollination interval between early- and late-appearing silks on the ear was lengthened artificially. Pollination of approximately 50% of fertile florets on the first day silks emerged effectively eliminated kernel set on the remaining florets pollinated 7 d later (Freier et al., 1984).

Dominance mechanisms are likely involved in establishing total kernel set among ear shoots as well. It is well established that kernel set in the sub-apical ear depends on synchronous silking and pollination of both ear shoots (Harris et al., 1976; Motto and Moll, 1983; Sarquís et al., 1998). Reduced kernel set in sub-apical ears results primarily from their delay in growth and development relative to apical ears (Hall et al., 1980; Jacobs and Pearson, 1991; Otegui, 1997). This delay in silk emergence and lack of kernel set upon pollination of sub-apical ears may be indicative of (i) a dominance mechanism exerted by the apical ear (Pinthus and Belcher, 1994), (ii) the competition for assimilates between ears (Tollenaar et al., 1992), or (iii) "correlative dominance signals" (Bangerth, 1989), in which dominance and competition for assimilates take place simultaneously. Correlative dominance signals may explain why more assimilates per kernel are necessary to set kernels on the sub-apical ear than on the apical ear (Tollenaar et al., 1992; Otegui and Bonhomme, 1998).

It may be possible to overcome the effects of such dominance signals on kernel set by altering the silking dynamics within and/or between ears. We tested this possibility under field conditions using four hybrids of contrasting prolificacy, grown in two environments, and at two plant populations to establish a range of silking and pollination dynamics. Pollination treatments (natural- and hand-pollinations) were used (i) to modify the number of simultaneously pollinated silks, (ii) to determine the relationship between KN on the sub-apical ear and the silking interval between ears, and (iii) to quantify the efficiency of pollination via the floret fertility index.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Field Plots and Treatments
Field experiments were conducted during 1997 at Morris, MN (45°35'N, 95° 55'W), and during 1997–1998 at Salto (34°33'S, 60°33'W), Argentina. Soils were Hammerly clay loam soil (Aeric Calcaquolls, fine-loamy, frigid) at Morris and silty clay loam soil (Typic Argiudol) at Salto. Two contrasting hybrids and plant populations were used at both sites. At Morris, `AgriPro AP 162' (nonprolific) and `AP 9191' (prolific) were sown on 19 May at 2.5 and 7.5 plants m^-2. At Salto, `Dekalb DK 752' (nonprolific) and `DK 664' (prolific) were sown on 7 November at 3 and 9 plants m^-2. These contrasting plant populations were selected to create consistent differences in plant, ear, and silk growth at silking (Otegui, 1997). Treatments were arranged in a split-plot design with two replicates. Plant populations were main plots with hybrids as subplots. At Morris, each subplot was 40 rows wide x 15 m in length planted in 0.75-m rows. At Salto, subplots were 20 rows wide x 15 m long planted in 0.70-m rows. In both cases, subplots were large enough to control the natural pollen distribution within the sampling area. Experimental plots were kept free of weeds and pests, and plants exhibited no visible signs of water or nutrient stress during the growing season.

Flowering Dynamics and Pollination Treatments
At least 30 plants were tagged at random within each subplot prior to silk emergence. The date of silking (first silks visible) for both ears (E₁ = apical ear, E₂ = sub-apical ear) was recorded for each tagged plant, and used to calculate the ear silking interval (ESI = silking E₂ - silking E₁) in days.

From this pool of tagged plants in each subplot, a minimum of 10 plants were subjected to natural pollination; at least 10 others were used for hand pollination. For those plants destined for hand pollination, both E₁ and E₂ were bagged before silks emergence. Both ears were pollinated on the fifth day after silks first emerged from the husks of E₁ (i.e., 5 DAS for E₁ = Day 0 for pollination). We used the natural variation in ESI among plants within the naturally and hand-pollinated treatments (-1 to +6 d) to test the importance of between-ear synchrony in controlling kernel set. For plants with ESI = 0 d, for example, both E₁ and E₂ were pollinated on 5 DAS. If a plant had an ESI = 3 d, however, E₁ was pollinated on 5 DAS and E₂ was pollinated 2 DAS. This approach differed from that of Harris et al. (1976) and Sarquís et al. (1998) who used fixed pollination intervals between ears regardless of when the two ears actually silked. Hence, the pollination interval between ears assigned to a plant was not necessarily its actual ESI. In the present work, pollination of the hand pollinated plants was delayed only to 5 DAS to ensure a large proportion of ovaries had silks exposed for pollination (Bassetti and Westgate, 1993a; Maddonni et al., 1999, Cárcova et al., 1998), and to guarantee receptivity of all florets on E₁ with silks exposed for pollination (Sadras et al., 1985; Bassetti and Westgate, 1993b).

Silks were pollinated by hand between 1000 and 1200 h with fresh pollen. For pollen collection, tassels with anthers visible only in the main branch were bagged late in the afternoon, and sampled for pollen the next morning. After hand pollination, ears were left unbagged to allow natural pollination of late-appearing silks. Pollination of these late-appearing silks (i.e., after 5 DAS) was likely because pollen was available throughout the silking period from border plots surrounding the experiment. Therefore, final kernel number on hand pollinated ears could be greater than the number of silks pollinated by hand on 5 DAS.

Prior to pollination, the apical section of the exposed silks was removed to leave a brush of silks for pollination. Silk tissues removed from E₁ (Morris and Salto), and E₂ (Salto) were stored in 700 g kg^-1 ethanol until counted.

Silk emergence dynamics and total number of florets per ear were determined on bagged ears of the remaining tagged plants in each subplot (at least 10 plants). At Morris, exposed sections of silks were cut from E₁ every 1 to 2 d from 0 to 5 DAS. All newly exposed silks (i.e., those with a bisected apical end) were counted to develop a cumulative curve of silk emergence. At Salto, exposed silks were cut from E₁ on 2 and 5 DAS. On 9 DAS, all E₁ used for silk number determination were collected for a final counting of exposed silks and total number of differentiated florets (FPE₁ = florets per ear). This latter value was estimated from the product of floret rows per ear (counted in the middle of the ear) and the number of florets per row (two counts at opposite sides of the ear) (Otegui, 1997).

Kernel number per E₁ and E₂ was determined for each naturally or hand-pollinated plant at maturity (Salto) or at mid grain filling (Morris). All ears with at least 10 kernels ear^-1 (Tollenaar et al., 1992) were considered fertile. Consequently, the ESI, the number of pollinated silks on 5 DAS, and KN per ear were matched for each tagged plant in the hand-pollination treatment. These data were used to calculate kernel set as a floret fertility index (FFI) for each apical (FFI₁, Morris and Salto) and sub-apical (FFI₂, Salto) ear according to Eq. [1].

(1)

The number of silks exposed on 5 DAS was assumed to be the same for naturally and hand-pollinated plants. Thus, the average value of exposed silks per ear obtained from hand-pollinated plants in each subplot was used to calculate the FFI of the naturally-pollinated plants in that sub-plot. Values greater than 1 indicate silks exposed after 5 DAS were receptive to pollen and set kernels. This was also possible for hand-pollinated ears, which were left unbagged after pollination.

Data were analyzed by standard ANOVA, and a t-test analysis was used to determine significant (P < 0.05) differences between treatment means. Standard regression analysis was applied to the relationship between E₂ kernel number and ESI.

	Results and discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Kernel Number Determination
At each site, significant (P < 0.05) differences were detected among hybrids for total number of differentiated florets in E₁ (FPE₁ in Table 1) , with AP 9191 > AP 162 and DK 752 > DK 664. For all four hybrids, there were no significant differences between plant populations for this trait, in agreement with observations by Otegui (1997) on a different set of hybrids grown under similar conditions. In the present work, potential size of the apical ear (FPE₁) was determined by both floret rows ear^-1 (r = 0.98, n = 8) and florets row^-1 (r = 0.95, n = 8). In most cases, all differentiated florets on E₁ had silks exposed for pollination by 9 DAS (compare Table 1 and Fig. 1) . Only DK 664 grown at 9 plants m^-2 had significantly (P < 0.05) fewer silks exposed by 9 DAS than the total number of differentiated florets on E₁ (10%). Increasing plant population also caused a significant (P < 0.05) reduction in the number of silked ears per plant on all hybrids (Table 1), and generally decreased the number of E₁ silks emerged at 5 DAS when hand pollinations were made (Fig. 1). A notable exception was AP 9191, whose rate of silk emergence was similar at 2.5 and 7.5 plants m^-2. Taken together, these results suggest the primary effect of high population stress on ear development was a reduction in the rate of silk elongation, as previously observed under nitrogen and defoliation stress (Jacobs and Pearson, 1991). The consequences for kernel set were significant (P < 0.05) reductions in KN plant^-1 for all hybrids and pollination treatments (Table 1). The decrease in KN with increasing population reflected a lack of kernel set on E₂ (i.e., reduced prolificacy) plus fewer kernels set on E₁.

View larger version (33K): [in this window] [in a new window]   Fig. 1 Pattern of silk exsertion on apical ears of maize hybrids grown at Morris, MN (AP 162, AP 9191) and Salto, Argentina (DK 752, DK 664) at low (2.5 or 3.0 plant m-2) and high (7.5 or 9.0 plant m-2) plant populations. Data are the mean of 20 plants. Vertical bars represent ± the standard deviation

In general, the ESI had a dramatic effect on the KN of E₂ (Fig. 2) . In several cases, there was a significant (P < 0.05) negative relationship between KN on E₂ and the ESI. The response to increasing ESI, however, varied with each hybrid. Naturally pollinated plants of the non-prolific hybrid AP 162, for example, lost 67 E₂ kernels for each daily increment in ESI. This value was 105 E₂ kernels d^-1 for the prolific hybrid, AP 9191. Hand pollination of E₁ and E₂ limited the negative impact of an increasing ESI on E₂ kernel number in both of these hybrids, although the response was not significant for AP 9191. Kernel number on E₂ was low at all ESI for naturally pollinated plants of DK 752. Sub-apical KN in this non-prolific, large-eared hybrid increased dramatically in response to hand pollination with E₁, particularly at the shorter ESI. But this positive response faded quickly as E₂ set about 83 fewer kernels for each daily increment in ESI. The other prolific hybrid, DK 664, presented no clear relationship between KN on E₂ and the ESI. Although, synchronous pollination improved KN on E₂ in plants whose apical and sub-apical ears exserted silks within 1 or 2 d.

View larger version (31K): [in this window] [in a new window]   Fig. 2 Relationship between kernel number on sub-apical ears (E2) and the silking interval between apical (E1) and sub-apical (E2) ears of four maize hybrids. Plants were grown at 2.5 (AP 162 and AP 9191) or 3 plants m-2 (DK 752 and DK 664), and subjected to natural pollination as silks emerged, or to synchronous hand pollination five days after first silks appeared on E1. The ear silking interval is the number of days between first silk appearance on E2 and E1. At least 20 plants were included in each hybrid x plant population x pollination treatment

Although initiation and differentiation of the reproductive shoots is nearly simultaneous for E₁ and E₂ (Otegui and Melón, 1997), growth and development of E₂ is usually delayed relative to E₁ (Jacobs and Pearson, 1991; Pinthus and Belcher, 1994; Otegui, 1997). This apparent dominance of the apical ear is thought to be mediated by competition for assimilates and/or the action of an undetermined growth inhibitor (Bangerth, 1989; Tollenaar et al., 1992; Pinthus and Belcher, 1994). Whatever the cause, its impact on E₂ development and function can be manifested in two stages: pre-silking and post-silking. Prior to silk emergence, dominance of E₁ determines the extent of the ESI. Then, as E₂ silks are exposed for pollination, prior fertilization of E₁ ovaries affects the success of pollination in fertile ovaries on E₂. Under natural pollination, the combined effects of pre- and post-silking dominance by E₁ essentially precluded kernel set on E₂ at ESI greater than 3 d for AP 9191, DK 752 and DK 664, and greater than 5 d for AP 162 (Fig. 2). These maximum values of ESI for kernel set on E₂ coincide with the onset of active mitotic activity and rapid cytokinin accumulation in the earliest-formed E₁ kernels (Dietrich et al., 1995). This flush of mitotic activity may represent the signal to limit kernel set in later fertilized ovaries of E₂. The increased kernel set and FFI of E₂ observed in most cases in response to hand pollination (Tables 1 and 2) suggests that the impact of such a signal on subsequent kernel set can be moderated by the timing and intensity of early kernel development on both ear shoots. In our study, closer synchrony in pollination between E₁ and E₂ provided the sub-apical ears greater opportunity to express their potential for kernel set. Further investigation is needed to determine if the relationship between ESI for kernel set in E₂ is linked to the activation and/or transport of metabolic or hormonal signals from E₁ (Harris et al., 1976).

Floret Fertility Index
A Floret Fertility Index (FFI = KN plant^-1/silks pollinated 5 DAS) was calculated to document the changes in fecundity of E₁ and E₂ florets associated with the timing of pollination (Table 2). At low plant populations, pollination timing had no impact on KN for E₁ or FFI₁, but synchronous pollination increased the FFI for E₂ (data from Salto only). However, FFI₁ decreased with increasing plant population in naturally pollinated plants, but synchronous pollination helped restore FFI₁ to its low-population level.

Values of FFI₁ >1.1 for AP 162 and FFI₁ >1.3 for AP 9191 at the low plant population (Table 2) indicate that additional silks exserted after 5 DAS were receptive and their florets set kernels. In fact, 95 to 98% of E₁ florets of AP 162 and AP 9191 set kernels in this treatment. Dekalb hybrids DK 752 and DK 664, however, behaved very differently at low plant density. They apparently failed to set kernels at floral positions whose silks exserted after 5 DAS (i.e., FFI₁ = 1.0), which limited kernel set to about 70 to 80% of E₁ florets. These hybrids exposed a large number of silks within the first 2 d of silking (Fig. 1), which could be advantageous for synchronous pollination of these florets, but may have negative consequences for kernel set of the later-fertilized ovaries, according to Freier et al. (1984). Experiments are underway to test this possibility.

Because the naturally and hand-pollinated plants were tagged at random within each hybrid x plant population density sub-plot, it is unlikely that differences in assimilate status between pollination treatments could bias the results. Also, the increase in FFI in response to synchronous pollination (at high plant populations for E₁ and low plant populations for E₂) suggests there is not a fixed threshold of assimilate availability per fertile floret to ensure kernel set. Our pollination treatments (natural versus synchronous) modified kernel set per fertile floret, independent of changes in current assimilate availability. In other research, synchronous pollination did alter the subsequent pattern of assimilate partitioning to support a larger reproductive sink (Lafitte and Edmeades, 1995). This result suggests that the temporal pattern of silk emergence and ovary fertilization in maize provides a fairly conservative mechanism to control kernel set even under favorable growing conditions. As such, variation in KN per plant among hybrids grown under similar environmental conditions reflects differences in silking (ESI) and pollination dynamics (Bolaños and Edmeades, 1993; Sarquís et al., 1998) as well as inherent variation in assimilate partitioning to the developing ear (Tollenaar et al., 1992; Andrade et al., 1999).

	Conclusions

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Maize kernel set can be significantly improved through synchronous pollination, both between ears at low plant populations and within ears at high plant populations. By delaying fertilization of early-silking ovaries, later-developing flowers are able to achieve their potential for kernel set. This unrealized potential for kernel set indicates that assimilate availability per fertile floret is not the only factor limiting kernel number per plant. Silking dynamics, which ultimately affects fertilization dynamic, may explain, at least in part, differences observed in final kernel number among genotypes grown under similar environmental conditions.

	ACKNOWLEDGMENTS

 
This work was supported by Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Fundación Antorchas, the Univ. of Buenos Aires (UBACyT AG04), the USDA-ARS, and Dekalb Argentina. J. Cárcova and M. Uribelarrea held a grant from Universidad de Buenos Aires. M. Otegui is a member of CONICET.

Received for publication July 22, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 

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