Published online 31 May 2007
Published in Crop Sci 47:1104-1110 (2007)
© 2007 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
CROP PHYSIOLOGY & METABOLISM
Ovary Growth and Maize Kernel Set
J. Cárcova and
M. E. Otegui*
Dep. de Producción Vegetal, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martín 4453 (C1417DSE). J. Cárcova's present address: Monsanto Argentina, Pergamino, Argentina
* Corresponding author (otegui{at}agro.uba.ar).
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ABSTRACT
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Synchronous pollination improves maize (Zea mays L.) kernel set, but the physiological reasons behind this response are yet unclear. We registered ovary fresh weight evolution at three floret positions along the ear (base, middle and tip) of plants subjected to natural (NP) or synchronous (SP) pollination during two growing seasons. Synchronous pollination of ears bagged before silking was performed five days after silking (DAS). Ovary weight increased exponentially at all floret positions (P 
0.01), but a lag in this trait was detected among those at the base and middle of SP ears. At each sampling date, florets along the ear differed (P < 0.01) in ovary weight, but differences were larger for NP than for SP plants. At pollination of each floret position, however, the range in ovary weight was smaller in NP ears (ca. 4 to 5 mg ovary–1) than in SP ears (4 to 9 mg ovary–1). Contrarily, just pollinated ovaries at the tip of the ear of NP plants (i.e. on ca. 4–5 DAS) experienced the high growth rate of those already pollinated at the base (ca. 0.7 mg d–1 for the former and ca. 3.7 mg d–1 for the latter). The range in ovary growth rate along the ear was drastically reduced under synchronous pollination on 5 DAS (ca. 0.55 mg d–1 for the base and ca. 0.47 mg d–1 for the tip). The larger the tip-to-base ratio in ovary growth rate, the larger the number of kernels set per plant (r2= 0.94; P = 0.03).
Abbreviations: DAS, days after silking • DBS, days before silking • KNP, kernel number per plant • NP, natural pollination • ROGR, relative ovary growth rate • SP, synchronous pollination.
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INTRODUCTION
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Maize (Zea mays L.) kernel number per plant depends on ear growth rate during the critical period around silking, which is linearly related to plant growth rate during this stage (Andrade et al., 1999; Echarte et al., 2004). This number, however, is significantly improved when silks from different positions along the ear are synchronously pollinated (Cárcova et al., 2000). As such, a synchronous pollination improves kernel set for the same ear growth rate. Under natural conditions, pollination of ovaries at the base and middle of the ear takes place between silking and one day after silking (DAS), while those from the tip are pollinated from 4 DAS onwards (Bassetti and Westgate, 1993a; Cárcova et al., 2003). Synchronous pollination (SP) can be obtained by hand pollination on 4 or 5 DAS of all silks exposed from ears bagged before silking (i.e. before the first silks are extruded from the husks).
Improved kernel set in SP plants suggests that, under natural pollination (NP), early-fertilized ovaries at the base promote kernel abortion of late-fertilized ovaries from the tip. This interference effect from early-pollinated ovaries on late-pollinated ovaries is also evident between apical and second ears at low stand densities (Cárcova et al., 2000), and is enhanced when the pollination gap is increased among floret positions within an ear (Cárcova and Otegui, 2001). Kernel set at a given floret position along the ear, therefore, does not depend exclusively on assimilate availability per kernel. For a given plant and ear growth rates, it may also depend upon its relative location (‘hierarchy’) with respect to other florets and pollination dynamics.
In maize, this ‘primigenic dominance’ (i.e., inhibition promoted by early developed sinks; Bangerth, 1989) seems to be exerted by ovaries located at the base of the ear after their fertilization, and not by these same ovaries before being pollinated. Maize ovary growth after fertilization has been described in detail for addressing the effects of water stress on kernel abortion (Westgate and Boyer, 1986), and Schussler and Westgate (1995) reported a clear effect of growth rate of ovaries from the middle of the ear on final kernel number. But growth dynamic of ovaries before and after the pollination/fertilization process has never been analyzed for different floret positions along the ear in response to contrasting pollination patterns. Consequently, it is not known if relative ovary size exerts a control on final kernel set. In other words, whether ovary size at pollination differs between apical florets from SP ears and their counterparts from NP plants, giving the former an improved condition for competing for assimilates and setting a kernel. The study of late ovary growth could help elucidate this controversy.
In this work we characterized ovary and kernel growth from different floret positions along the uppermost ear of maize. Starting on two days before silking (DBS), samples were taken from natural and hand-pollinated ears until ca. 9 DAS. Fresh weight was used as an indicator of growth and sink activity of the organs under study.
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MATERIALS AND METHODS
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Crop Husbandry
Field experiments were conducted during two growing seasons (experiment 1: 1999-2000, and experiment 2: 2000-2001) at the experimental unit of the Department of Plant Production of the University of Buenos Aires (35°35'S, 59°29'W). Single cross maize hybrid DK 752MG was sown on 13 September (experiment 1) and 11 October (experiment 2), which represent normal planting dates in the region (Otegui et al., 1996). Plots were hand planted at three seeds per hill and thinned to 8 plants m–2 at the three-ligulated leaf stage. Experiments were fertilized with 100 (experiment 1) and 240 (experiment 2) kg of N ha–1, and soil water content of the uppermost 1 m of the profile was kept near field capacity by means of furrow irrigation throughout the growing cycle. Pests and weeds were adequately controlled.
Treatments and Measurements
Two pollination treatments were evaluated in all experiments: (i) natural pollination (NP), and (ii) synchronous pollination (SP). Treatments were arranged in a completely randomized block design with three replicates. Each replicate had 10 (experiment 1) or 20 (experiment 2) rows, 0.7 m apart and 6.5 m (experiment 1) or 5 m (experiment 2) long. On approximately 15 DBS, at least 40 plants were tagged in the innermost six (experiment 1) or ten (experiment 2) rows of each replicate, and were assigned at random to NP (at least 15 plants) or SP treatments (at least 25 plants). All visible earshoots of plants under SP were bagged before silking, and the date of silking (at least one silk visible from among the husks) was registered for all tagged plants (NP and SP). Pollination of ears assigned to the SP treatment was performed 5 DAS, by adding fresh pollen manually to all silks exposed from bagged ears (for details see Cárcova et al., 2000). After pollination, these ears were left unbagged to allow natural pollination of late-appearing silks. Some ears bagged before silking never received pollen and were assigned to the assessment of ovary growth after 5 DAS (only in experiment 1).
Ear sampling for determination of ovary growth spanned between 1 or 2 DBS up to 8 or 9 DAS. At least one ear per pollination treatment was sampled from each replicate. Silking date of ears sampled before silking was defined by the relative length of silks with respect to the length of husks and knowledge of daily silk growth of a similar hybrid (Cárcova et al., 2003). Husks of these early sampled ears were cut lengthwise carefully, and those with silks visible at less than 5 cm from the tip of the husks were considered representative of 1 DBS. Those with silks visible between 8 and 5 cm from the tip of the husks were considered on 2 DBS.
Ears were sampled between 1000 and 1400 hr, placed in sealed bags to avoid desiccation and immediately brought to the laboratory. For each ear, at least five ovaries were collected from each of three floret positions along the ear: 5th (base of the ear), 20th (middle of the ear) and 35th (tip of the ear). Pistils (ovary+silk) from each position were cleaned from other flower parts (glumes, lemmas and paleas), and their fresh weights (with and without silks) were determined. Data were used for calculating fresh weight evolution of individual ovaries and ovary growth rate at each floret position (in mg of fresh weight per day). Silk length was also determined for each floret position and sampling date. Pistil removal from the ear was performed within a sealed chamber with saturated air, except when they were so small that the use of a dissecting microscope was necessary for sample collection (e.g., tip florets from ears collected before silking). In these cases, each pistil removed was placed on a soaked paper in a covered Petri dish, until a minimum of five pistils were obtained. Additional measurements were performed on each uppermost ear sampled on 8 or 9 DAS, which included (i) ear length without husks, (ii) ear length with husks, and (iii) maximum number of florets per ear (only in experiment 2). The number of florets was counted on two opposite rows of spikelets along the ear, and the average value was multiplied by the number of rows counted at the middle of the ear for obtaining the total number of spikelets per ear.
At maturity, the number of grained ears per plant (prolificacy) was determined in all remaining tagged plants, and ears of each treatment were harvested and used for the evaluation of final kernel number per plant (KNP). Final kernel number of each ear was obtained as the product of (i) the average of the numbers of kernels counted along four kernel rows, and (ii) the number of kernel rows counted at the middle of the ear.
All data were evaluated by ANOVA. Exponential models (Eq.1) were fitted to the evolution of ovary fresh weight
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where the ordinate (a) represents ovary fresh weight at ear silking (day 0), b is ovary growth rate, and X is time (in days). Differences in ovary growth rate (in mg day–1) between NP and SP treatments were tested by ANOVA (Steel and Torrie, 1960).
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RESULTS
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Pistil and Ovary Growth
There were significant differences (P < 0.01) among floret positions along the ear for both ovary and pistil (ovary+silk) fresh weights (Table 1). Up to silking, those at the base were always the largest and those at the tip were always the smallest. After silking, synchronous pollination modified the pattern of pistil growth along the ear, and significant (P < 0.01) interactions were detected for ovary weight between pollination systems and floret positions (Table 1). For ears under NP, differences in ovary fresh weight among floret positions followed the above-described trend (base > middle > tip), except on 7 DAS of experiment 1 (base = middle > tip). Differences in ovary fresh weight among floret positions along the ear were always smaller in SP ears than in the NP ones (Table 1). This difference between pollination treatments was due to reduced ovary fresh weight increase at basal and middle positions of SP ears, because this trait never differed between florets from the tip of contrasting pollination treatments (Fig. 1). Ovary growth at the base and the middle of unpollinated ears had almost ceased on 7 DAS (Fig. 1).
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Table 1. Fresh weight of ovaries and ovaries plus silks (Ov+Sk) at different positions along the ear for two pollination treatments (NP: natural pollination; SP: synchronous pollination) in two experiments. DBS: days before silking; DAS: days after silking.
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Figure 1. Ovary fresh weight evolution at three floret positions along the ear (base, middle, and tip) of plants under natural (NP) and synchronous (SP) pollination during two experimental years. Asterisks denote significant differences (P < 0.05) between pollination systems. White arrows point out silking of both pollination treatments and start of pollination in NP plants. Black arrows indicate hand-pollination in SP plants. For SP plants, solid lines correspond to ears pollinated on five days after silking (DAS), and dotted lines link ovary weight data of ears that never received pollen.
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Ovary growth rate (in mg day–1) showed the above-described differences between pollination treatments. In NP ears, this rate decreased from bottom to tip and increased all along the period under analysis (Table 2). In non-pollinated ovaries at the base and the middle of the ear, this rate usually declined immediately after silking, and active growth resumed after pollination on 5 DAS (Table 2; Fig. 1). This lag in ovary fresh weight evolution was absent when the whole pistil weight was considered (Table 1), evidenced in (i) lack of differences between NP and SP plants at each floret position on 3 DAS of experiment 1, and (ii) the significant difference (P < 0.01) in pistil weight among all floret positions of SP plants on 3 and 5 DAS, which is not evident between some ovary weights (e.g., basal and middle ovaries in both experiments). Pistils from the base and middle of SP ears had longer silks than their NP counterparts because of continued silk elongation up to pollination (Fig. 2). This difference in silk growth compensated for reduced ovary growth in SP ears, and caused no significant interaction effects for whole pistil weight between pollination systems and floret positions (Table 1). Pistils from the tip did not differ in final silk length between pollination treatments, and no lag in ovary growth rate was evident at this floret position in SP ears (Fig. 1).
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Table 2. Ovary growth rate of plants under natural (NP) or synchronous (SP) pollination treatments. Data were computed for different periods around silking (silking day= 0), and correspond to three ovary positions along the ear (base, middle and tip) and two experiments. Ears of SP plants were pollinated on day 5.
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Figure 2. Silk length evolution at three floret positions along the ear (base, middle, and tip) of plants under natural (NP) and synchronous (SP) pollination during two experimental years. Dotted lines indicate that silk senescence prevented silk length determination. Asterisks denote significant differences (P < 0.05) between pollination systems. White arrows point out silking of both pollination treatments and start of pollination in NP plants. Black arrows indicate hand-pollination in SP plants.
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Ovary fresh weight during the period under analysis increased exponentially at all floret positions along the ears of NP plants (Table 3). This trend was also evident in SP plants, but the above-described alteration in ovary growth at some floret positions (Fig. 1) resulted in (i) a reduced accuracy in fitted exponential models (r2 values), and (ii) significant differences (P < 0.05) between NP and SP plants in the parameter b (growth rate) of these models, which was larger for the former than for the latter (Table 3). These differences between pollination systems were less evident among ovaries from the tip.
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Table 3. Exponential models fitted to mean ovary fresh weight (in mg) evolution of plants under natural (NP) and synchronous (SP) pollination treatments. Data correspond to three ovary positions along the ear (base, middle and tip) and two experiments.
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Kernel Number Determination
Final KNP differed significantly (P < 0.05) between NP and SP treatments (Table 4). In experiment 1, differences in KNP could be attributed exclusively to variation in kernel set in the uppermost ear, because treatments did not differ in the number of grained ears per plant (Table 4). In experiment 2, SP determined a 29% increase in final KNP, and 60% of this increase corresponded to kernels set in subapical ears (data not shown). Maximum number of florets per uppermost ear, ear length (with and without husks), and rows of kernels per ear did not differ between pollination treatments (Table 4).
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Table 4. Quantitative descriptors of uppermost ear size on 8 or 9 days after silking (SPE: spikelets per ear; EL: ear length without husks; HL: ear length with husks) and at final harvest (Prolificacy: grained ears per plant; KNP: final kernel number per plant; Rows: kernel rows per ear) of natural (NP) and synchronous pollination (SP) treatments in two experiments.
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Final KNP was affected by the above-described differences between treatments in the pattern of ovary growth rate between 3 and 5 DAS. The larger the ratio in ovary growth rate between extreme floret positions during this period (ROGR= Ovary growth rate at tip florets/Ovary growth rate at base florets) the larger the number of kernels set per plant (Fig. 3).
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Figure 3. Response of kernel number per plant (KNP) to relative ovary growth rate (ROGR) between extreme floret positions (ROGR= ovary growth rate at tip florets/ovary growth rate at basal florets) determined for the period between three and five days after silking. Data correspond to natural (NP) and synchronous (SP) pollinated ears.
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DISCUSSION
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In previous studies (Cárcova et al., 2003) we reported differences in silk growth at different floret positions promoted by pollination treatments like those used in the present research (i.e., natural pollinated ears and ears bagged before silking). From those studies we learned that final silk length always decreased from the base to the tip of the ear independently of the pollination treatment, but that lack of pollination determined an extension of the silk elongation period. Current results confirmed these findings and expanded our knowledge on this subject. During the period under analysis (from 2 DBS to 9 DAS), ovaries from all floret positions of NP ears had an exponential growth pattern, as already described for silks (Cárcova et al., 2003). This pattern was also evident in SP ears, but lack of pollination between silking and 5 DAS was accompanied by a lag in ovary growth, evident in florets from the base and the middle of the ear but not in those from the tip. This difference among floret positions has not been reported before, and may be related to the natural ontogenic delay along the ear (Otegui, 1997; Cárcova et al., 2003), which sets an interval between early silking ovaries from the base and the late silking ones from the tip (Bassetti and Westgate, 1993a; Cárcova et al., 2003). In all conditions (i.e., NP and SP plants), ovaries at the tip of the ear had not reached maximum ovary size at the time of silking. Consequently, they did not show a lag in growth during the period under analysis under any pollination treatment. Florets from the base and the middle of the ear of SP plants recovered active ovary growth after pollination on 5 DAS, evidence of a still intact silk receptivity (Bassetti and Westgate, 1993b) that allowed for successful fertilization and kernel set.
Ovaries from different positions along the ear of plants under NP had similar fresh weights (between 4 and 5 mg ovary–1) at their corresponding pollination date, which usually takes place on 0 to 1 DAS for those from the base and on 4 to 5 DAS for those from the tip (Bassetti and Westgate, 1993a). The opposite happened in SP ears, which exhibited a larger gradient in ovary fresh weight along the ear (between 4 and 9 mg ovary–1) when silks were synchronously pollinated on 5 DAS (Fig. 1). Ovary size, therefore, cannot be claimed to be alone responsible for commonly observed variations in final kernel number (Schussler and Westgate, 1995), which in the apical ear are always related to variable kernel set capacity in distal florets (Cárcova et al., 2000; Cárcova and Otegui, 2001). Nevertheless, we could determine a distinctive aspect between pollination systems: a huge contrast in ovary growth rate along the ear when tip florets are fertilized. At their pollination on ca. 4 to 5 DAS, ovaries at the tip of the ear of NP plants experienced the high growth rate of those located at the base, which had been pollinated previously (between 0 and 1 DAS) and had already started active kernel growth. Under synchronous pollination on 5 DAS, ovaries from the tip of the ear were smaller than those from the base, but all had a similar growth rate when expressed in fresh weight. On the basis of these findings, kernel set at distal floret positions seemed to depend upon the relative growth rate of other growing sinks (e.g., ovaries or kernels from the base and middle sections of the ear), as evidenced in the strong relationship established between KNP and relative ovary growth rate of extreme floret positions. This issue has not been addressed in previous studies (Schussler and Westgate, 1995). Our hypothesis is supported also by evidence from previous research using a contrasting approach and the same hybrid (Cárcova and Otegui, 2001): in a stand of uniform plants, kernel abortion increased when the pollination gap among florets along the ear was artificially enhanced. Under this manipulation, ovary growth rate of bottom florets at pollination of tip ovaries must have been larger than in the present research, explaining the remarkable reduction in kernel set observed for some treatments (e.g., 49% kernel set of the control when the pollination gap was increased by two days at a stand density of only 3 plants m–2). A similar analysis applies to any stress condition that enhances the pollination gap among florets along the ear.
In summary, previous (Tollenaar and Daynard, 1978) and current evidence suggests that fertilization of early silking florets triggers a shift in assimilate partitioning within the ear, which may affect kernel set in late pollinated ovaries. The magnitude of the effect will depend upon assimilate availability per plant and its partitioning to the ear (Andrade et al., 1999; Echarte et al., 2004, D'Andrea et al., 2006), but also upon the pollination gap among florets. Longer gaps will determine larger differences in growth rate between growing kernels from the base of the ear (dominant sinks) and silking ovaries from the tip (dominated sinks), giving the latter a reduced opportunity for setting a kernel.
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ACKNOWLEDGMENTS
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Authors wish to thank Drs. Lucas Borrás and Victor Sadras for their helpful comments on the manuscript. This work was supported by Fundación Antorchas, the National Agency for Promotion of Science and Technology of Argentina (ANPCyT), the University of Buenos Aires, and the National Council for Research of Argentina (CONICET). J. Cárcova held a grant from Fundación Antorchas and M.E. Otegui is a member of CONICET.
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NOTES
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All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.
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TOP
ABSTRACT
INTRODUCTION
