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Reproductive Biology |
2Center for Ecological Research, Kyoto University, Kamitanakami-Hirano, Otsu 520-2113 Japan; 3Department of Botany, Graduate School of Science, Kyoto University, Kitashirakawa-oiwake, Sakyo, Kyoto 606-8502 Japan; and 4Forest Department Sarawak, 93660 Kuching, Sarawak, Malaysia
Received for publication January 2, 2001. Accepted for publication July 6, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: breeding system • canopy access • Dipterocarpaceae • inbreeding depression • Lambir Hills National Park • pollination experiment • pollen-tube guidance • self-incompatibility
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). de Nettancourt (1977)
suggested that in most cases post-fertilization self-rejection does not contribute extensively to outcrossing and that the term "self-incompatibility" should be used only for the pre-fertilization mechanism. On the other hand, Seavey and Bawa (1986)
pointed out that post-fertilization self-rejection are quite common and proposed the concept of late-acting self-incompatibility. The relative contribution of such self-rejection systems varies according to life form or phylogenetic background (e.g., Seavey and Bawa [1986]
pointed out that late-acting self-incompatibility is characteristic of woody plants). In addition to these early- and late-acting types of self-incompatibility, early-acting inbreeding depression (Wiens, 1984
; Wiens et al., 1989
) and late-acting maternal selection (Bookman, 1984
; Stephenson and Winsor, 1986
; Griffin, Moran, and Fripp, 1987
; Kenrick and Knox, 1989
; Waser, 1993
) may also increase realized outcrossing rates. Characterizing such phenomena is necessary to understand how outcrossing is maintained within a population or species.
Recent studies in species-rich tropical rainforests have reported the predominance of outcrossing in trees (Bawa, 1974
; Hamrick and Murawski, 1990
; Kitamura et al., 1994
; Murawski and Bawa, 1994
), although Fedorov (1966)
and Van Steenis (1969)
claimed that trees must be self-compatible and self-pollinated because of the spatial isolation of individuals. High outcrossing rate indicates that the self-rejection systems are common in tree species of the tropical rainforest.
Dipterocarpus tempehes is an emergent tree of lowland tropical rainforests in southeast Asia. The breeding system of dipterocarps in this region may be influenced by general flowering, a phenomenon unique to this region. General flowering refers to supra-annual and irregular mass flowering, which is followed by mast fruiting at the community level. General flowering occurs at intervals of 5 yr on average (Ashton, Givinish, and Appanah, 1988
; Appanah, 1993
). During the general flowering period, a large portion of species of Dipterocarpaceae, and many species of other families, bloom heavily while they hardly bloom at all at another period (Ashton, Givinish, and Appanah, 1988
; Appanah, 1993
; Sakai et al., 1999b
). The population size of pollinators in the forest also fluctuates depending on the magnitude of general flowering (Nagamitsu, 1998
; Itioka et al., in press
). These large fluctuations in the flowering synchrony of plants and the population size of pollinators probably result in uncertain pollination efficiency and variable availability of pollen source. In response, flexibility in the self-rejection system, including partial self-incompatibility and delayed abortion, could have evolved to allow the proper choice of parents depending on the variable conditions. To date, however, studies on the breeding systems of dipterocarps (Chan, 1981
; Dayanadan et al., 1990
; Sakai et al., 1999a
) have given little attention to the relative importance of different self-rejection systems. Although such studies have estimated the existence of self-incompatibility, they have not attempted to clarify the actual systems and timing of self-rejection.
In this study, we investigated the breeding system and the possible existence of a self-rejection system enhancing outcrossing in D. tempehes. We addressed three questions in particular. (1) Does D. tempehes have a self-rejection system? (2) If so, what is this mechanism? (3) Is there a flexible self-rejection system, such as partial self-incompatibility or delayed self-rejection? We also discussed the possible advantages of such a flexible mechanism in D. tempehes with respect to the general-flowering phenomenon in the lowland dipterocarp forest.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Dipterocarpus tempehes belongs to the family Dipterocarpaceae, a family of dominant emergent trees in the lowland forest of West Malaysia (Ashton, 1982
). Dipterocarpus tempehes frequently reaches a height of >50 m. It flowers at supra-annual and irregular intervals, but with relatively higher frequency than other typical general-flowering trees, which flower only in the general-flowering periods (T. Kenta et al., unpublished data). The flower longevity is 
1 d. The flowers are 3–5 cm long and 2–4 cm in diameter and have hollow-type styles (K. K. Shimizu, personal observation). Flowers of D. tempehes open sequentially from the inflorescence base towards the apex. An ovary contains six ovules, and usually only one ovule can mature to seed. The mature fruit is 2–4 cm in diameter. In most dipterocarp species, some or all of the five calyces enlarge as the fruits grow and develop into fruit wings, which are thought to enhance fruit dispersal. However, fruit wings are not developed in this species. Mature seeds germinate in a few days after dispersal.
The breeding system and flower demography of three D. tempehes individuals (Trees A, B, and C) in and around the 8-ha plot of Lambir Hills National Park were studied from May to September of 1998, when many species of Dipterocarpaceae and other families in this region flowered (general flowering) (Kato et al., 2000
). The distribution of adult (diameter at breast height >30 cm) D. tempehes trees around these three individuals is shown in Fig. 1. We used the single-rope climbing technique (Perry, 1978
) to access the forest canopy. Because access to flowers by the single-rope climbing technique is limited to those just around the main stem and most parts of the crown surface cannot be reached in the case of tropical emergent trees, we fixed additional 30–50 m ropes between >15 branches per canopy, and the observations were conducted along these ropes after accessing the crown.
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0.3 mm) before onset of flowering to exclude flower visitors. In the SELF treatment, the flower was hand-pollinated with pollen of the same flower. In the CROSS treatment, pollen of Tree A was applied to flowers on Tree B, pollen of Tree B to those on Tree C, and pollen of Tree C to those on Tree A. Pollen for the CROSS treatment was collected from flowers that opened on the same day as the treated flowers in the crown or on water-soaked branches sampled 1–3 d before the treatment (water-soaked branches naturally produce flowers in a few days after sampling). In the BAG treatment, bagged flowers were kept intact. Although the SELF, CROSS, and BAG treatments were carried out in the same bag, only a single treatment was conducted on any given individual in the course of a single day to avoid pollen contamination inside bags. In the CONTROL treatment, flowers were not bagged and were naturally pollinated. We monitored a total of 3437 flowers on 101 branches (mean = 34 flowers per bag) for the SELF, CROSS, and BAG treatments. For the CONTROL treatment, 2830 flowers on 67 branches were monitored.
Fruit maturation and germination of mature seeds
We monitored flower abscission and ovary development in all the treatments. Ovary development was recorded using five stage categories: I, before swelling (0.7 cm in diameter); II, after swelling and smaller than 1 cm in diameter; III, 1–2 cm; IV, 2–3 cm; and V, >3 cm. Seeds in stages IV and V have the ability to germinate (T. Kenta, unpublished data). The census was carried out every 1–3 d during the flowering period (1 May–10 June) and every 1–4 wk thereafter until fruit dispersal.
After seed maturation (stages IV and V), sound mature seeds fell from branches and were trapped inside of the bags in the CROSS, SELF, and BAG treatments. They germinated in a few days within the bags. We calculated the germination rate of these mature seeds trapped within the bags as an index of seed viability.
We compared ovary survivorship from stages I to IV, I to II, and II to IV between treatments by chi-square tests. Days required for fruit maturation to stages II, III, and IV (as an index of the speed of fruit maturation) and germination rate of mature seeds between treatments were also analyzed by unpaired Student's t tests and chi-square tests, respectively. However, because of the small sample size, we pooled the data of the three trees and pooled and conducted the SELF and BAG treatments together (= SELF + BAG treatment, as the data for self-pollinated ovaries) when calculating the days required for fruit maturation and the germination rate. Analyzing fruits from SELF and BAG together is appropriate because fruit in BAG treatments should have originated from self-pollination. It is unlikely that the fruits in BAG treatment came from apomixis, because we did not observe multiple-embryo seeds, which are associated with apomixis in all the species of Dipterocarpaceae studied so far (Kaur et al., 1986
).
Pollen-tube growth
To examine self-incompatibility, we performed an additional pollination experiment in which we observed the germination and growth of pollen tubes. We cut off flowers from the trees and immediately hand-pollinated them with self- or cross-pollen in our laboratory (in the same manner as used for the SELF and CROSS treatments above, respectively). In total, 38 flowers were treated and fixed in FAA solution (formaldehyde, acetic acid, and 70% ethanol in the ratio 5 : 5 : 90 v/v/v) 6 h after hand pollination. We also fixed other sets of flowers at 2, 3, and 4 h after pollination manipulation, but the germination rates of pollen tubes were still low in the flowers fixed earlier than 6 h. Then we analyzed only the results from flowers fixed at 6 h after manipulation.
After fixation of the flowers, pollen tubes were visualized following the method of Shimizu and Okada (2000)
with some modifications. The fixed pistils were treated with 90%, 70%, and 40% ethanol for 20 min each in this order. After being washed with water, they were treated with 1 mol/L NaOH overnight. Then they were stained in 0.1% Aniline Blue (Schmid GMBH, Stuttgart, Baden-Württemberg, Germany) in 0.1% K3PO4 buffer (pH 12.4) overnight. The pistils were mounted in glycerol and split into halves longitudinally using a 25-gauge needle. The state of pollen grains and the pattern of elongation of pollen tubes were observed under a Axiophoto2 (Carl Zeiss, Jena, Thuringia, Germany) microscope with UV illumination to visualize the callose of pollen tubes. The number of pollen tubes in the style was counted at a position 1 mm distant from the tip of the pistil. We also observed whether the fastest pollen tube reached the base of the style.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Fruit-maturation rate
In both treatments, fruits grew slowly before stage II (1 cm in ovary diameter) and faster at the later stages. Fruits matured more quickly in CROSS treatments (Fig. 4) than in SELF + BAG treatments. Significantly fewer days were required for maturation to 1 cm and 2 cm ovary diameter in CROSS treatments (P < 0.05, unpaired Student's t test). The difference in required days became greater at later stages.
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Pollen tube growth
The stigma (tip of the pistil) of D. tempehes was covered with stigmatic exudate (Figs. 7 and 10). In both the SELF and CROSS treatments, pollen grains were deposited on the stigmatic exudate as under natural conditions. The average numbers of pollen grains that germinated in the stigmatic exudate per pistil were 27.4 and 27.9 in the CROSS and SELF treatments, respectively. The difference was not significant (P = 0.92 by unpaired Student's t test). The pollen tubes elongated in the exudate in random directions (Figs. 5 and 8). We could not find any evidence for a defect of elongation, such as a bulge or bursting at the tip of the pollen tubes. We also could not find strong fluorescence in pollen tubes that could be caused by cell death.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Early-acting self-incompatibility has typically been classified into two categories, depending on the reaction site of inhibition (de Nettancourt, 1977
; Seavey and Bawa, 1986
): inhibition of pollen germination and/or pollen tube elongation at the stigma (e.g., in Brassica [Takasaki et al., 2000]) and inhibition of pollen tube growth in the style (e.g., in Solanaceae [Newbigin, Anderson, and Clarke, 1993
]). However, the incompatibility seen in D. tempehes differs from these types. The inhibition of self-pollen tubes occurred at the border of the stigma and the style hollow.
We suggest that this incompatibility reaction is not due to the absence of a component necessary for pollen germination or growth, nor to the existence of a substance interfering with the normal metabolism of the pollen grain or pollen tube, as has been previously suggested (de Nettancourt, 1977
). Neither pollen germination nor pollen tube growth were inhibited or interfered with in SELF treatments in D. tempehes. Rather, it appeared that only the guidance of pollen tubes to the style hollow was inhibited. Similar guidance defects have been reported in previous mutant studies (Wilhelmi and Preuss, 1996
; reviewed in Smyth, 1997
) and in a study of interspecies incompatibility (Shimizu and Okada, 2000
). Wilhelmi and Preuss (1996)
studied a mutant of Arabidopsis and suggested the inhibition of adhesion between pollen tubes and pistil tissues. Shimizu and Okada (2000)
studied the interspecies incompatibility in Brassicaceae and reported that there was a lack of directional guidance for pollen tubes to enter the ovules in ovaries. Either of these two models—a lack of adhesion substance or a lack of signal exchange for the directional guidance—can also explain the reaction of self-incompatibility in D. tempehes. The present results suggest that such a guidance defect contributes not only to interspecies incompatibility but also to intraspecies incompatibility. To our knowledge, D. tempehes is the first species in which a guidance defect is shown to cause self-incompatibility.
A late-acting mechanism
Most of the flower abortions occurred before ovary swelling. In that step, the difference in ovary survivorship was 10.0-fold between CROSS and SELF treatments using the pooled data for all three individuals (Table 1), which was much larger than the 2.2-fold difference caused by the pollen-tube guidance defect. Furthermore, we observed no inhibition of the elongation of self-pollen tubes in the style. There are two possible explanations for the discrepancy. The first is a threshold effect. Adhesion of a certain number of pollen grains is required for pollen germination in some species (reviewed by Hormaza and Herrero, 1994
). In other plants, first pollen tubes "pave the way" for later arriving tubes. Both mechanisms are considered to be controlled by maternal substance. In D. tempehes, there was considerable variation among flowers in the proportion of pollen tubes entering styles (Fig. 11). The relationship between the number of pollen tubes in the style and probability of the fertilization is unknown in this species. It is possible that the numbers of pollen tubes entering the styles are below a required threshold in most of the self-pollinated ovaries. The second possible explanation for low ovary survivorship in the SELF treatment is late-acting self-incompatibility (Seavey and Bawa, 1986
). Brewbaker (1957)
suggested that ovarian incompatibility was often associated with the hollow styles that characterize Dipterocarpus tempehes. The uniform abortion that occurred before ovary swelling is also consistent with late-acting self-incompatibility (Seavey and Bawa, 1986
). The relatively slow speed of fruit maturation before ovary swelling (Fig. 4) may be due to the incompatibility mechanism working before formation of a multicellular embryo.
Inbreeding depression and/or maternal selection
After ovary swelling, from stages II to IV, ovary survivorship was also higher in CROSS treatments (Table 1), although the difference between CROSS and SELF treatments was small compared to that between stages I and II. This selection probably occurred after fertilization and the formation of a multicellular embryo, since ovary swelling probably occurs only after fertilization in this species (ovaries >1 cm in diameter always had an embryo; T. Kenta, personal observation). Thus, we suggest the existence of either early-acting inbreeding depression (Wiens, 1984
; Wiens et al., 1989
) and/or late-acting maternal selection (Bookman, 1984
; Stephenson and Winsor, 1986
; Griffin, Moran and Fripp, 1987
; Kenrick and Knox, 1989
; Waser, 1993
). Based on the present results, we cannot distinguish between growth failure by deleterious recessives in self-pollinated ovaries and preferential maternal resource allocation to cross-pollinated ovaries. In addition, a 1.6-fold difference in germination rate between cross and self-pollinated seeds suggests the possibility of inbreeding depression at that stage, although the difference was not statistically significant.
The breeding system
The result of much higher fruit sets (flower survivorship from stage I to IV) in the CROSS than in the SELF treatment (Table 1) indicates that D. tempehes has a strong self-rejection system. But this system was not perfect, because some fruit set was also observed in SELF. This result is consistent with the previous reports on other dipterocarps (Chan, 1981
; Sakai et al., 1999a
). The extremely low fruit set in the BAG treatment (Table 1) indicates the necessity of pollinators. In spite of the existence of effective pollinators, the result of higher fruit sets in CROSS than CONTROL proves that there was some degree of pollen limitation for fruiting under natural conditions. This pollen limitation caused a 2.8–5.1-fold difference in fruit set. Higher fruit set in CROSS might have been due to the exclusion of predators by the bag in CROSS treatment: in the CONTROL treatment, flowers were vulnerable to low survivorship due to predation. However, considering the low predation rate before fruit maturation (12.4%; T. Kenta, unpublished data), the difference in fruit set cannot be fully explained by predation exclusion.
In the self-rejection process of D. tempehes, we found early-acting self-incompatibility and inbreeding depression and/or maternal selection. Threshold effects in the number of pollen tubes for the fertilization or late-acting self-incompatibility were also implied. Thus we suggest that multiple processes determine the outcrossing rate of D. tempehes.
Dipterocarpus tempehes has relatively weak early-acting self-incompatibility caused by the unique pollen-tube guidance defect. On the other hand, many flowers were aborted at later stages. This seems to produce wastage of resource allocated to aborted flowers. Why, then, does Dipterocarpus tempehes not have strong self-incompatibility at an early stage? The flowering habit of D. tempehes and general flowering within the community are probably related to the advantages of this self-rejection system. In lowland dipterocarp forests, the interval between general flowering is highly variable (Ashton, Givinish, and Appanah, 1988
; Appanah, 1993
; Sakai et al., 1999b
), and the synchrony of flowering within the population fluctuates between years. Pollinator population sizes also fluctuate due to fluctuation in the flowering of the plant community (Nagamitsu, 1998
; Itioka et al., in press
). On the other hand, D. tempehes flowers relatively frequently compared to the typical general flowering interval (T. Kenta et al., unpublished data). Thus, D. tempehes should experience variation in pollinator availability and pollination efficiency. Although the pollen limitation in D. tempehes detected in this study suggests that pollination efficiency is critical for this species, the strength of pollen limitation may change depending on the synchrony of flowering within the population and availability of the pollinator.
We suggest several adaptive significances of the weak early-acting self-incompatibility related with such an uncertain pollination efficiency. First, it would allow some fruiting when pollination efficiency is low. On the other hand, without some early-acting self-incompatibility, the flower abortion at later stage and resource wastage would increase. Second, if this species has a late-acting self-incompatibility mechanism, although this is not verified in this paper, a combination of the weak early-acting self-incompatibility and late-acting self-incompatibility would permit some flexibility in the choice of pollen parents. Seavey and Bawa (1986)
pointed out that a late-acting self-incompatibility permits the maternal parent to evaluate the performance of pollen genotypes over a longer period and allows some flexibility in the choice of pollen parents in relation to resource availability, which is important in the face of variable pollen parentage and resource uncertainty. The same idea could be applied to species, like D. tempehes, with uncertain pollination efficiency. The partial early-acting self-incompatibility caused by the pollen guidance defect would preserve some flexibility in the choice of pollen parents and resource allocation.
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FOOTNOTES |
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5 Author for reprint requests (kenta{at}ecology.kyoto-u.ac.jp
).
6 These authors contributed equally to this work.
7 Present address: Research Institute for Humanity and Nature, Sakyo, Kyoto 606-8502 Japan.
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