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(American Journal of Botany. 2000;87:1765-1768.)
© 2000 Botanical Society of America, Inc.

Unfertilized ovules of Epilobium obcordatum (Onagraceae) continue to grow in developing fruits1

Steven R. Seavey2,0, Susan K. Mangels0 and Natasha J. Chappel3,0

0 Department of Biology, Lewis and Clark College, Portland, Oregon 97219 USA

Received for publication September 14, 1999. Accepted for publication March 2, 2000.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
To determine whether unfertilized ovules continue to grow when in an ovary containing fertilized ovules, we measured ovule lengths in developing fruits of Epilobium obcordatum that were harvested 4, 5, 8, and 10 d post pollination. We found that unfertilized ovules that were in the presence of fertilized ovules continued to grow and that there was a broad range of overlap in their sizes at all sampling times. This effect was found for two types of unfertilized ovules that occur throughout the length of the ovary: normal, unfertilized ovules, apparently bypassed by pollen tubes; and sterile ovules lacking an embryo sac. In addition, there is a position effect within developing fruits. Both fertilized and unfertilized ovules are larger at the stylar end. In six samples resulting from pollination with a single pollen tetrad, a total of 18 embryos were found, and the effect on unfertilized ovules, greatest at the stylar end, diminished with distance from the ovules with embryos. Our results are consistent with the interpretation that diffusible hormones produced by developing seeds cause nearby unfertilized ovules to grow. We conclude that caution is necessary when attempting to infer ovule fertilization histories from the appearances of ovules in developing and mature fruits. What are often inferred to be aborted seeds, in many cases, may not be seeds at all. They may be enlarged, unfertilized ovules.

Key Words: developing seeds • Epilobium obcordatum • hormones • Onagraceae • position effect • unfertilized ovules


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Mature fruits often contain ovules that did not develop into seeds, and determining the causes, as well as the degree, of this reduced fecundity, are important goals of many studies of plant reproduction. Proximate causes may be external (e.g., incomplete fertilization due to pollen limitation), internal (e.g., loss of embryos due to genetic load), or a combination of both (cf. Burd, 1994 ). Visual inspection of developing and mature fruit contents, sometimes aided by a dissecting microscope, is the most common means for distinguishing full, or "expanded," seeds from ovules that did not mature an embryo. Although the former category is usually unequivocal, ambiguity is encountered in the latter category and inferences must be made concerning the ovules that did not develop a mature embryo. Were they fertilized or not? In particularly favorable material, some failing embryos may grow large enough to be readily identified (Nakamura, 1988 ); however, it is often the case that partly enlarged, or "flat," seeds do not show clear signs of containing an embryo. The fertilization histories of these ovules cannot be determined directly.

In the absence of empirical data, it has become common practice to infer that ovules of developing and mature fruits that are similar in size to their original floral state were not fertilized, and to ascribe any that have increased beyond this size, but are not their fully mature size, to embryo failure—i.e., they are presumed to be "aborted" or "empty seeds" (Wiens, 1984 ; Ganeshaiah, Shaanker, and Shivashankar, 1986 ; Lee and Bazzaz, 1986 ; Harper and Wallace, 1987 ; Burbidge and James, 1991 ; Krebs and Hancock, 1991 ; Heering, 1994 ; Jakobsen and Martens, 1994 ; Marshall, James, and Potter, 1996 ; Huang et al., 1997 ; Ramirez and Berry, 1997 ). As far as we are aware, the premise that ovules intermediate in size are the products of post-zygotic failures has not been tested. Is it possible that what some observers have called "aborted seeds" may at times be expanded, unfertilized ovules? This is a crucial question for studies that seek to quantify either the frequency of fertilization or the fates of zygotes.

It has been known for some time that the growth of ovaries containing fertilized ovules and the development of the fertilized ovules themselves are results of hormonal signals communicated between the developing embryos and the parent plant (Gustafson, 1939 ). As a consequence of these signals, developing seeds and fruits become strong sinks for the parent plant's nutrients (Zamski, 1995 ). In a multiovulate ovary it seems likely that any unfertilized ovules in proximity to fertilized ovules would experience a very different environment from the unfertilized ovules in ovaries lacking fertilizations. If the hormones and/or nutrients associated with developing embryos and endosperm stimulate general growth, then the unfertilized ovules may themselves continue to expand beyond their original state. Because the expanded integuments of the ovule would have the appearance of a developing seed coat, both the size and the appearance of these structures in developing and mature fruits could lead one mistakenly to infer that they were partially developed seeds.

We tested the hypothesis that unfertilized ovules increase in size in the presence of fertilized ovules by measuring fertilized and unfertilized ovules in developing fruits of Epilobium obcordatum. A previous study of this species revealed that the average fertilization frequency, even following excess pollen application, was only ~60%, and that unfertilized ovules were distributed throughout the length of the linear fruits (Seavey and Carter, 1996 ). The fates of these ovules are the subject of this report.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
All plants in this study were grown in the greenhouse. For a description of the species, the pollination technique, and treatment schedules, see Seavey and Carter [1996] . A total of ~44 ovules are linearly arranged in each of four carpels throughout the length of the ovary. Each ovular position in the ovary therefore normally contains four ovules. To determine whether unfertilized ovules in developing fruits continue to enlarge during fruit development, we measured ovules in 4-, 5-, 8-, and 10-d post-pollination (PP) samples. The first fertilizations in E. obcordatum are known to occur ~24 h PP (Seavey and Carter, 1996 ). Measurements of ovule size for 4- and 5-d PP fruits were made on a permanent collection of serial sections created for the 1996 study. Measurements were made using an ocular micrometer in a compound microscope. Serial sections were scanned for the section containing the largest view of each ovule and the length of this section was recorded. Ovules were measured if they contained a normally developing embryo or were unfertilized. Sectioning and analyzing developing fruits much older than 5 d PP are impractical. Therefore, the 8- and 10-d PP samples were stained and cleared using Mayer's hemalum-methyl salicylate (Stelly et al., 1984 ), a technique that allows rapid observation of embryos and endosperm. These ovules were dissected out of the ovary and measured using a dissecting microscope.

Two types of unfertilized ovules occur throughout the length of the ovary: normal ovules with an embryo sac and ovules lacking an embryo sac (cf. figs. 5–6 and 8–9 in Seavey and Carter, 1996 ). A comparison of these two types for the largest sample, 5-d PP, revealed that after accounting for the position effect (see below) in the ovary (ANOVA, F = 19.338; df = 9; P = 0.0001), they do not significantly differ in length (ANOVA, F = 2.476; df = 1; P = 0.116; overall averages for the two types were 1.47 and 1.49 mm, respectively). These two types of unfertilized ovules are therefore combined in the analyses here. A third unfertilized type, consisting of integuments and a shrunken nucellus (cf. figs. 7 and 10 in Seavey and Carter, 1996 ), occurs only in the most basal positions and was not encountered in the present study.

To determine ovule sizes in ovaries lacking fertilizations, we sectioned ovaries of unpollinated flowers and flowers sampled <24 h PP. These provided the baseline for sizes of unexpanded ovules in Fig. 2. We refer to these as floral ovules. Neither ovules nor ovaries expand if flowers are not pollinated. The presence of a single embryo is sufficient to cause the ovary to mature into a fruit.



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  		Fig. 2. Mean ovule lengths, by position in 5-d PP developing fruits of fully pollinated flowers, and floral ovules of ovaries lacking fertilizations. Filled circles = 5-d PP ovules with embryos; half-filled circles = 5-d PP unfertilized ovules; and open circles = floral ovules. Error bars = ±1 SD

 
Finally, in an effort to assess the effects of a limited number of embryos in a developing fruit, we analyzed six samples that each had been produced by pollination with a single pollen tetrad. These 7-d PP developing fruits came from a single individual. These ovaries yielded a total of 18 fertilized ovules (2–4 embryos per ovary, X = 3), three of which had embryos, but no endosperm.

In all samples of sectioned and cleared material we measured ovules in the first ten positions, beginning at the stylar end of the ovary. The stylar end of individual ovaries may be constricted and contain fewer than four ovules. If only one was present, it was combined with those immediately below to be position 1; two or more were assigned the first position. Measurements of a total of 2536 ovules from 65 developing fruits of 19 genets are presented here.

We used a two-factor ANOVA to test for the effects of position and ovule type on ovule size. Both ANOVA and Helmhert contrasts for position effect were performed using SuperANOVATM. Helmhert contrasts compare a given mean response with all subsequent means in an ordered array (SuperANOVA, 1989) . Scheffé's post-hoc comparisons were performed with StatView®.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
All ovules increase in length during fruit development
Ovule lengths for the 4-, 5-, 8-, and 10-d PP samples are presented in Fig. 1 and Table 1. Both the fertilized and the unfertilized ovules increased in size during this period of fruit development. The average lengths of fertilized ovules were significantly larger at each successive sampling day (ANOVA, F = 658.99; df = 3; P = 0.0001; Scheffé's, Pmax = 0.026 for 8–10 d PP). The unfertilized ovules were significantly larger through the 8-d sample, but not larger at 10-d PP (ANOVA, F = 79.671; df = 3; P = 0.0001; Scheffé's, P = 0.0001 through 8 d PP, 0.168 between 8 and 10 d PP). At each sampling day there was a substantial amount of overlap between the sizes of fertilized and unfertilized ovules (Fig. 1, Table 1).



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  		Fig. 1. Ovule lengths at 4, 5, 8, and 10 d PP for ovules with embryos and unfertilized ovules. Boxes = median ±25% of range, bars = ±40% of range

 

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  		Table 1. Mean lengths (mm), ranges (mm), and sample sizes for ovules of 4-, 5-, 8-, and 10-d PP developing fruits of E. obcordatum (fertilized/unfertilized)

 
Ovules are larger at the stylar end of the developing fruit
Our 5-d PP sample was large enough to allow an analysis of position effect for the first ten positions in the developing fruit (Fig. 2, Table 2). Position significantly affected ovule lengths in developing fruits, and the significant interaction indicates a differential response to position by the two ovule types. The influence of fertilized ovules on unfertilized ovules is greater at the stylar end of the developing fruit than at the peduncular end. The sizes of floral ovules (N = 101) do not vary by position (ANOVA, F = 0.32; df = 9; P = 0.967), and they are significantly smaller than unfertilized ovules in developing fruits (ANOVA, F = 517.58; df = 1; P = 0.0001).


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  		Table 2. ANOVA results for comparison of lengths, by position, for unfertilized and fertilized ovules in 5-d PP developing fruits of E. obcordatum

 
Effect of embryos on unfertilized ovules is greatest for nearest neighbors
Five of the six flowers pollinated by a single pollen tetrad produced ovaries with fertilizations in the first three positions (Fig. 3A). There was a significant position effect for the length of unfertilized ovules (N = 174) in these ovaries (ANOVA, F = 105.99; df = 9; P = 0.0001), with unfertilized ovules nearest the fertilized ones always growing more than those farther away. This increase was greatest for position 1, diminished through position 7, and completely attenuated by position 8 (Helmhert contrast Pmax through position 7 = 0.038; Pmin for positions 8 and 9 = 0.363).



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  		Fig. 3. Ovule lengths, by position in 7-d PP developing fruits resulting from pollination by single pollen tetrads. (A) Averages for five samples with embryos in the first three positions. (B) Results from a single developing fruit with three embryos. Filled circles = ovules with embryos, numbers above each represent total number of embryos observed at that position; open circles = unfertilized ovules. Nmax = 20 per position in (A), = 4 per position in (B). Error bars = ±2 SE.

 
The sixth sample contained embryos at positions 1 and 2, as well as at the distant position 7 (Fig. 3B). The position effect for unfertilized ovules (N = 32) was significant (ANOVA, F = 24.08; df = 9; P = 0.0001). The effect of the upper two embryos was attenuated by position 4 (Helmhert contrast, P = 0.0001 for positions 1 to 3; Pmin = 0.325 from positions 4 to 6). The effect of the single embryo at position 7 was significant only for the unfertilized ovules of that same position (Helmhert contrast, P = 0.0001 for position 7; Pmin = 0.185 for positions 8 and 9).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Our purpose in this study was to determine whether the sizes of unfertilized ovules are affected by the presence of fertilized ovules in the same ovary. This is an important question to address because many studies of plant reproductive biology rely on observations of the contents of developing and mature fruits. These studies often contain an important premise: ovules that have enlarged beyond their floral state represent failed seeds. Our results indicate that this is not true for E. obcordatum. Both normal, unfertilized ovules, apparently bypassed by pollen tubes, and sterile ovules lacking an embryo sac continue to expand when in the presence of ovules containing embryos.

By 4 and 5 d PP, a time of rapid growth of embryos and endosperm (Seavey and Carter, 1996 ), the ovules containing embryos have increased in length an average of 65 and 117%, respectively. During this same period, the unfertilized ovules in these ovaries have increased an average of 46 and 74%, respectively. By 10 d PP, a time when the torpedo-stage embryos are at or near their maximum size, the fertilized ovules have increased an average of 140% and their unfertilized neighbors have increased 102%. In addition, the range of lengths of the two types of ovule broadly overlap throughout development, with 44% overlap at 10 d PP (0.80–2.40 mm vs. 1.65–2.50 mm). Because unfertilized ovules grow in size in maturing fruits, and because many of these are as large, or larger than, ovules with embryos, neither growth nor absolute size of an ovule in E. obcordatum is indicative of embryo failure.

The degree of overlap in sizes is due in part to a position effect in the developing fruits. Fertilized ovules, like the embryos they contain (Seavey and Carter, 1996 ), are larger at the stylar end of the developing fruit. The unfertilized ovules display a similar pattern, and the lengths of those that occur at the stylar end overlap the lengths of the fertilized ovules at all positions.

We do not know what causes unfertilized ovules to continue growing in the presence of others that are fertilized, although it has been established for some time that the auxins and other hormones produced by developing seeds move outward to surrounding tissues and stimulate development of the fruit (Gustafson, 1939 ). This effect can be localized to tissues in the immediate vicinity of the embryo-containing ovules (Crane, 1964 ; Pechan and Morgan, 1985 ), and it is therefore reasonable to suspect that nearby unfertilized ovules might be stimulated by these same growth substances. The stylar ovules are apparently the first to be fertilized in E. obcordatum, and these first embryos would cause other stylar ovules to begin enlarging. Subsequent fertilizations at lower positions would stimulate a wave of influence, thus causing the position effect seen here.

This hypothesis is consistent with our observation of a position effect on ovule size, and our observation of a significant interaction between position and ovule type. The lower ovule positions are known to have fewer and smaller embryos (Seavey and Carter, 1996 ), and presumably less endosperm, and therefore there would be less diffusible hormone in this region of the developing fruit. (Additional factors that can have position effects within ovaries are discussed by Rocha and Stephenson [1990] ).

The results of our single tetrad pollinations support the conclusion that the effect of fertilized ovules is localized to near neighbors. When the fertilized ovules occurred only in the top three positions, the effect on the unfertilized ovules was greatest at position 1 and then diminished through position 7, with no effect on positions 8 and 9 (Fig. 3A). This position-dependent response is what would be expected if ovule growth is caused by a hormone concentration gradient whose source is the fertilized ovules. Moreover, in the single incidence of an embryo at a lower position (Fig. 3B), only the group of adjacent ovules at the same position were significantly affected. (Individual ovules at contiguous positions may have increased in size, but they would not have been identified if the average for their position was not raised sufficiently.) The distinctive response in this sample is a result of only two embryos in the upper positions (up to four were present in the samples in Fig. 3A) and a single embryo at position 7.

It is difficult to predict how widespread this intraovarian phenomenon might be. Because it is localized to near neighbors in E. obcordatum, the interovule effect we observed may be limited to species whose ovaries contain ovules in close proximity to one another. Perhaps the less intimate contact among ovules of legumes, for example, is not sufficient for the kind of effect we found here. On the other hand, the embryos and seeds of E. obcordatum are relatively small, and it is possible that in species with larger embryos proportionately larger effects would be seen. In either case, until more is known about the impact of fertilized ovules on their neighbors, it cannot be taken for granted that ovule sizes are dependable indicators of fertilization history.

In early investigations that predated our understanding of self-sterility in E. obcordatum (Seavey and Carter, 1994 ), we categorized the seed contents of mature fruits as "full," "flat," or "undeveloped." It was our working hypothesis that these represented successful seeds, failed seeds, and unfertilized ovules, respectively. It is clear now that this approach is not tenable for this species. The "flat seeds" were certainly a mixture of failed seeds and enlarged unfertilized ovules, and the "undeveloped" structures were not simply the remnants of unfertilized normal ovules. Included in this latter type, occurring only in the lowest positions, and not encountered in the present study, are sterile ovules consisting of empty integuments. These were present in 31% of the fruits analyzed in the 1996 study. A variety of types of sterile ovules has been reported for other species (Tomer and Gottreich, 1976 ; Guth and Weller, 1986 ; Palser, Rouse, and Williams, 1990 ), and it seems likely these also could further confound inferences based on their external appearances.

The observations presented here demonstrate that unfertilized ovules in E. obcordatum continue to grow in the presence of developing embryos, and their external appearance in developing and mature fruits cannot be used to infer their fertilization histories. Large ovules are not necessarily seeds, and their associated large integuments are not necessarily seed coats.


   FOOTNOTES
 
1 The authors thank Paulette Bierzychudek, Clyde Calvin, Keith Karoly, Gary Reiness and two anonymous reviewers for reading earlier versions of this manuscript and providing suggestions that improved its content; Kellar Autumn for statistical assistance throughout the project; and Cynthia Dyrnes and Tristi Wood for slide preparations. This research was supported in part by the M. J. Murdock Charitable Trust. Back

2 Author for correspondence. Back

3 Current address: Mary Knoll School, 1402 Punahou Street, Honolulu, Hawaii 96822 USA. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Burbidge, A. H., and S. H. James. 1991 Postzygotic seed abortion in the genetic system of Stylidium (Angiospermae: Stylidiaceae). Journal of Heredity 82: 319–328[Abstract/Free Full Text]

Burd, M. 1994 Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60: 83–139[CrossRef]

Crane, J. C. 1964 Growth substances in fruit setting and development. Annual Review of Plant Physiology 15: 303–326

Ganeshaiah, K. N., R. Uma Shaanker, and G. Shivashankar. 1986 Stigmatic inhibition of pollen grain germination—its implication for frequency distribution of seed number in pods of Leucaena leucocephala (Lam) de Wit. Oecologia 70: 568–572[CrossRef][ISI]

Gustafson, F. G. 1939 Auxin distribution in fruits and its significance in fruit development. American Journal of Botany 26: 189–194[CrossRef][ISI]

Guth, C. J., and S. G. Weller. 1986 Pollination, fertilization and ovule abortion in Oxalis magnifica. American Journal of Botany 73: 246–253

Harper, J. L., and H. L. Wallace. 1987 Control of fecundity through abortion in Epilobium montanum L. Oecologia 74: 31–38[CrossRef][ISI]

Heering, J. H. 1994 The reproductive biology of three perennial Sesbania species (Leguminosae). Euphytica 74: 143–148[CrossRef][ISI]

Huang, Y. H., C. E. Johnson, G. A. Lang, and M. D. Sundberg. 1997 Pollen sources influence early fruit growth of southern highbush blueberry. Journal of the American Society for Horticultural Science 122: 625–629[ISI]

Jakobsen, H. B., and H. Martens. 1994 Influence of temperature and ageing of ovules and pollen on reproductive success in Trifolium repens L. Annals of Botany 74: 493–501[Abstract/Free Full Text]

Krebs, S. L., and J. F. Hancock. 1991 Embryonic genetic load in the highbush blueberry, Vaccinium corymbosum (Ericaceae). American Journal of Botany 78: 1427–1437[CrossRef][ISI]

Lee, T. D., and F. A. Bazzaz. 1986 Maternal regulation of fecundity: non- random ovule abortion in Cassia fasciculata Michx. Oecologia 68: 459–465[CrossRef][ISI]

Marshall, A. H., I. R. James, and J. F. Potter. 1996 Ovule abortion in white clover (Trifolium repens L.). Annals of Applied Biology 128: 95–103[CrossRef][ISI]

Nakamura, R. R. 1988 Seed abortion and seed size variation within fruits of Phaseolus vulgaris: pollen donor and resource limitation effects. American Journal of Botany 75: 1003–1010[CrossRef][ISI]

Palser, B. F., J. L. Rouse, and E. G. Williams. 1990 Aberrant ovules and megagametophytes in Rhododendron nuttallii (Ericaceae). Botanical Gazette 151: 73–87

Pechan, P. A., and D. G. Morgan. 1985 Defoliation and its effects on pod and seed development in oil seed rape (Brassica napus L.) Journal of Experimental Botany 36: 458–468[Abstract/Free Full Text]

Ramirez, N., and P. E. Berry. 1997 Effect of sexual systems and dichogamy on levels of abortion and biomass allocation in plant reproductive structures. Canadian Journal of Botany 75: 457–461

Rocha, O. J., and A. G. Stephenson. 1990 Effect of ovule position on seed production, seed weight, and progeny performance in Phaseolus coccineus L. (Leguminosae). American Journal of Botany 77: 1320–1329[CrossRef][ISI]

Seavey, S. R., and S. K. Carter. 1994 Self-sterility in Epilobium obcordatum (Onagraceae). American Journal of Botany 81: 331–338[CrossRef][ISI]

———, and ———. 1996 Ovule fates in Epilobium obcordatum (Onagraceae). American Journal of Botany 83: 316–325[CrossRef][ISI]

Stelly, D. M., S. J. Peloquin, R. G. Palmer, and C. F. Crane. 1984 Mayer's hemalum-methyl salicylate: a stain-clearing technique for observations within whole ovules. Stain Technology 59: 155–161[ISI][Medline]

SuperANOVA. 1989 Abacus concepts Inc., version 1.11, Berkeley, California, USA

Tomer, E., and M. Gottreich. 1976 Defective ovules in avocado cultivars. Journal of the Society for Horticultural Science 101: 620–623

Wiens, D. 1984 Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64: 47–53[CrossRef][ISI]

Zamski, E. 1995 Transport and accumulation of carbohydrates in developing seeds: the seed as a sink. In J. Kigel and G. Galili [eds.], Seed development and germination, 25–44. Marcel Dekker, New York, New York, USA





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