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2Department of Biology, 3The Electron Microscopy Facility, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085-1699
Received for publication April 6, 1998. Accepted for publication December 18, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: heterostyly; incompatibility • Lythraceae; Lythrum salicaria • purple loosestrife; scanning electron microscopy; stigmatic papillae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In distyly, the stigma is positioned above or below the staminal whorl in the pin and thrum morphs, respectively (Ganders, 1979
). In tristyly, the stigma is positioned at one of the three levels, long, mid, and short, with the two whorls of stamens positioned reciprocally at the other two levels (Darwin, 1877
). The spatial separation of stigma and anthers helps to promote out-crossing among individuals of unlike morphs via insect-mediated pollination (Darwin, 1877
). Often this leads to the transfer of pollen from anthers of similar height to that of the pistil and is considered to be "legitimate" pollination (Darwin, 1877
).
Although the intrinsic features of heterostyly are the polymorphisms of the style and stamen lengths, heterostyly is also associated with other physiological and morphological differences among morphs (Mather and De Winton, 1941
; Dulberger, 1992
). Most heterostylous species examined demonstrate pollen heteromorphism (Dulberger, 1974
). Polymorphisms occur in pollen size (Darwin, 1877
; Dulberger, 1974
; Bir Bahadur, Bangaru Laxmi, and Rama Swamy, 1984a
, b
), color (Darwin, 1877
), exine sculpturing (Dulberger, 1981
, 1992
; Weber-El Ghobary, 1986
), anther size (Price and Barrett, 1982
; Glover and Barrett, 1983
), and pollen production (Ganders, 1979
).
Many heterostylous species demonstrate stigma polymorphism as well. In a few distylous species, such as Jepsonia parryi, Linum grandiflorum, and Linum pubescens, the receptive surface of the pin stigma is larger (Ornduff, 1970
; Dulberger, 1992
), while in others (for example, Amsinckia grandiflora, Primula malacoides, and Hedyotis caerulea) the thrum stigma is larger (Pandey and Troughton, 1974
; Ornduff, 1976
, 1980
). In some species, stigma color has also been documented to differ between morphs (Barrett, 1977
; Dulberger, 1987
). Other documented stigmatic polymorphisms include size and shape of the stigmatic papillae and the structure of the papilla wall (Baker, 1966
; Vuilleumier, 1967
; Dahlgren, 1970
; Dulberger, 1970
, 1975
, 1987
, 1992
; Ornduff, 1978
; Olesen, 1979
; Heslop-Harrison, Heslop-Harrison, and Shivanna, 1981
). Larger papillae are generally associated with long-styled flowers (Dulberger, 1974
). In Linium grandiflorum and L. pubescens, stigmatic papillae are longer in the pin compared to that in the thrum morph (Dulberger, 1987
). The stigma of the long morph in tristylous Lythrum junceum also bears larger papillae than in the mid and short morphs (Dulberger, 1970). However, thrum papillae also are reported to be larger than pin papillae in Anchusa officinalis and Reinwardtia indica (Schou and Philipp, 1984
; Bir Bahadur, Bangaru Laxmi, and Rama Swamy, 1984b
). Morph-specific differences in stigma size are closely linked to the size of the stigmatic papillae. The density of papillae on the stigma surface possibly is determined by the size of the papillae stemming from differential cell growth of underlying supporting tissue (Dulberger, 1992
) and also has been shown to be polymorphic in some heterostylous species (Darwin, 1877
; Dulberger, 1974
).
Cytochemical differences also have been identified between morphs on the stigma surface in some heterostylous species. Dulberger (1974)
reported polymorphism in the cytochemical structure of the papillae walls in the two morphs of some Linum species. In distylous members of Plumbaginaceae, the papillae of the pin and thrum morphs differ in the way the cuticle is attached to the cellulose layer (Dulberger, 1975
). Heslop-Harrison, Heslop-Harrison, and Shivanna (1981)
and Shivanna, Heslop-Harrison, and Heslop-Harrison (1981)
found differences in the stylar extracts surrounding the papilla cells of the distylous Primula. Athanasiou and Shore (1997)
also reported specific proteins in both the stigma/style and pollen in some species of the distylous Turneraceae family that may play a role in incompatibility. These fine structures of the stigma, including surface secretions, papillae size, shape, and distribution, have been suggested as contributing factors to self-incompatibility (Heslop-Harrison, 1990
). Such stigmatic polymorphism coupled with size, shape, and exine sculpturing of pollen grains in dimorphic Linum may serve as the basis for promoting legitimate pollinations through structural mechanisms analogous to a lock and key (Dulberger, 1981
). Darwin (1877)
also suggested that differences in the size and shape of the stigma surface can be part of heterostylous polymorphisms.
Although stigmatic polymorphism in heterostylous species are almost ubiquitous, studies on morph-specific morphological variation of stigma are limited (Dulberger, 1992
), and most studies on heterostyly are centered around their functions (Webb and Lloyd, 1986
; Barrett, 1992
, 1993
; Dulberger, 1992
). Even functionally, stigmas are very important structures in heterostylous species because morph-specific variation in stigma size can be a determinant of relative reproductive fitness of a particular morph (Dulberger, 1992
). For example, the bigger stigma of the pin morph of distylous species generally captures more pollen than the smaller thrum stigma (Ganders, 1979
). The nature and function of reciprocal herkogamy in the tristylous Lythrum salicaria have already been demonstrated by Darwin (1877)
, O'Neil (1992)
, Mal and Lovett-Doust (1997)
, and Mal, Lovett-Doust, and Lovett-Doust (1997)
. Darwin (1877)
also found that the long-styled morph of L. salicaria had a much larger stigma than either of the mid- or short-styled morphs, and observed that papillae lengths of the long stigma were considerably longer than those in the mid and short stigma. Thus, on a qualitative basis, the three flower morphs of L. salicaria differ in both size and nature of the stigmatic receptive surface. In this paper, we have undertaken a quantitative approach to elucidate the polymorphism of the stigma surface of L. salicaria, including size of stigma and the size, shape, and distribution of the stigmatic papillae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The seeds were germinated in a large flat in March 1997. Two hundred and one individual seedlings were then transplanted into 15 x 18 cm pots and grown in the greenhouse of Villanova University. Individual plants were identified and tagged for their style morphs upon flowering. We had 75 long-, 53 mid-, and 73 short-morph individuals. We sampled two mature and freshly opened flowers from each of those plants during 22–24 July 1997. Flowers in L. salicaria remain open for only 1 d (T. K. Mal, personal observation), and as we sampled at the same time of the day, it is assumed that the sampled flowers were at a comparable developmental stage. The flowers were dissected, and individual pistils were removed and preserved in 2.5% glutaraldehyde with 0.01% calcium chloride in 0.1 mol/L sodium phosphate buffer at pH 7.2 in separate microfuge tubes and stored at 4°C.
Scanning electron microscopy
Whole stigmas from each morph were removed from the pistils previously preserved in glutaraldehyde. Specimens were washed three times for 15 min each in 0.1 mol/L sodium phosphate buffer at pH 7.2, then transferred to 1% osmium tetroxide in 0.1 mol/L sodium phosphate buffer at pH 7.2 for 1 h at room temperature (Hayat, 1978
). Samples were washed three times in 0.1 mol/L sodium phosphate buffer at pH 7.2 at room temperature and dehydrated in a graded ethanol series, and then critical point dried (Hayat, 1978
) with a POLARON E3100 Critical Point Dryer (Fisons Instruments, East Sussex, UK) using three purges of liquid CO2, 30 min apart. Samples were coated with gold-palladium in a POLARON SC 7640 sputter coater and viewed with a HITACHI S-570 scanning electron microscope at 5 kV.
Digital images were captured at 100x magnification from five places on each stigma: one in the center and four others selected from each of the four imaginary quarters of each stigma (see Fig. 1). Images were captured using a Sun IPC Workstation running PGT IMIX software (Version 8.0; Princeton Gamma Tech, Rocky Hill, New Jersey) and transferred to an IBM-compatible personal computer via a Local Area Network. Each stigma image was processed with Image PC imaging software (Scion Corporation, Frederick, Maryland) calibrated with a SEM standard image (Structure Probe, Inc., West Chester, Pennsylvania). The diameter of each stigma was measured as the mean of two separate measurements taken cross-wise on each stigma (Fig. 1). The density of papillae was measured by counting the number of papillae within five circular areas with a fixed diameter of 372.5 µm, one in each of the five captured images from a stigma (Figs. 1–2). These observations were used to calculate the density of papillae per square millimetre. The total number of papillae per stigma was estimated as the average number of papillae divided by the circular area times the stigmatic area calculated from its diameter. We used one stigma from each individual plant for this analysis.
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Statistical analyses
Statistical analyses were executed using SYSTAT (Wilkinson, 1996
), and SAS (1990)
. Multivariate hierarchic analysis of variance was carried out to test the effects of morphs, individual plants, and stigmatic quarters on the structure of papillae. The effect of morph was tested over the individuals within a morph, and the effect of individuals was tested over the stigmatic quarters of individuals within a morph (Sokal and Rohlf, 1995
). Univariate analyses were conducted to test the effect of morph on density of papillae, total number of papillae per stigma, and stigma diameter.
A discriminant function analysis (Tabachnick and Fidell, 1996
) was also carried out to find out the relative importance of different descriptors of papillae structure (i.e., length of papilla and diameter of papilla at the apex, neck, and base) to categorize individuals into three flower morphs. To avoid pseudoreplication, we used mean values for each plant of each descriptor in this analysis (Hurlbert, 1984
). No outliers were detected through Mahalanobis distance measures, and no transformation was needed to achieve homogeneity of variance–covariance matrices (Tabachnick and Fidell, 1996
; Wilkinson, 1996
). We have also conducted analyses of variance on two canonical discriminant functions to test the effect of morphs. Depending on the discriminant score of this analysis, we can determine group memberships of newly observed stigma samples whose style morphs are not known (Given Harper, Juliano, and Thompson, 1993
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Dulberger (1992)
documented the pin stigma to be twice as large as the thrum stigma in species of Linum. Ornduff (1970)
also found the pin stigma to be greater than the thrum stigma in Jepsonia parryi. On the other hand, Ornduff (1976
, 1980
), Gill and Kyauka (1977)
, Pandey and Troughton (1974)
, and Bir Bahadur, Bangaru Laxmi, and Rama Swamy (1984b)
found larger stigma in the pins than in the thrums in other distylous species. In tristylous L. salicaria, stigma diameter in the long morph is significantly larger than in the mid and short morphs; stigma diameter is not significantly different between the mid and short morphs. In contrast, stigma width and height in the short morph were significantly greater than in the long and mid morphs in another tristylous member of Lythraceae family, Decodon verticillatus (Eckert and Barrett, 1994
). Thus, while in many distylous and tristylous taxa including L. salicaria, stigma size increases with style length, many other members (e.g., Amsinckia grandiflora, Primula malacoides, Hedyotis caerulea, and Decodon verticillatus) demonstrate the opposite trend (Pandey and Troughton, 1974
; Ornduff, 1976
, 1980
; Eckert and Barrett, 1994
).
Besides the polymorphism of stigmatic size, heterostylous species often demonstrate polymorphism of stigmatic surface including size and shape of the papillae. In distylous species, pin stigmas bear cob-like papillae, while thrum stigmas bear papillate papillae (Baker, 1948
, 1966
; Dulberger, 1975
). We found the stigmatic papillae in L. salicaria to be shaped like bowling pins in all three morphs, however, we also found that they differ in size. Length and diameters at the apex, neck, and base were significantly greater in the long morph than those in the mid followed by the short morph. We also wanted to predict to which morph an individual plant belongs from the papillae dimensions. A canonical scores plot easily separates the long morph from the mid and short morphs (Fig. 15). However, the canonical scores of the mid and short morphs show considerable overlap. Dulberger (1970)
also reported larger papillae in the long stigma compared to those in the mid and short stigmas, the latter being equal in size in L. junceum. In D. verticillatus, however, short papillae were found to be larger than the mid, which in turn were larger than the long papillae (Eckert and Barrett, 1994
). Similarly, in distylous species such as Pemphis acidula (Gill and Kyauka, 1977
), Anchusa officinalis (Schou and Philipp, 1984
), Reinwardtia indica (Bir Bahadur, Bangaru Laxmi, and Rama Swamy, 1984b
), thrum papillae were found to be larger than the pin papillae. Other distylous species demonstrate larger papillae in the pin morph than in the thrums (Dulberger, 1974
). Such morphological variation in stigmatic papillae may also be associated with variation in size, shape, and exine structure of pollen grains (Dulberger, 1992
). Polymorphisms of stigmatic papillae and pollen can lead to a close correlation between the morphology of stigmatic papillae and pollen grains involving legitimate pollinations (Dulberger, 1981
).
Information on the distribution and density of papillae is rather limited. In members of Plumbaginaceae (for example, Plumbago capensis, Plumbago europea, and Ceratostigma willmottianum), papillae are distributed in clusters on the stigmas (Dahlgren, 1918
, 1923
, 1970
; Dulberger, 1975
, 1987
). Number of clusters and number of papillae per cluster were found to differ between the two morphs. Pin stigmas generally have larger and less numerous clusters than thrum stigmas (Dulberger, 1992
). In L. salicaria, we found that the density of papillae per square millimetre of stigma surface was significantly greater in the mid and short morphs than in the long morph (Table 1; Fig. 14). These polymorphisms may indicate the presence of a pollen recognition system leading to differential adherence of specific pollen on the specific stigmas as has been noted in many distylous species (Dulberger, 1975
).
Although the density and size of papillae differ across morphs, the estimated number of papillae per stigma does not. This suggests that pollen capture efficiency may not differ across the morphs even when the stigma size differs. Increased stigma size in the long morph may only be a consequence of housing the same number of larger papillae. O'Neil (1992)
recorded transfer of pollen among the three morphs of L. salicaria using dye transfer methods. Long stigmas received dye more frequently than the mid stigmas followed by the short stigmas (O'Neil, 1992
). Fluorescent dye was used as the surrogate pollen, and thus the issue of pollen size polymorphism and absolute number of pollen per stigma could not be addressed (O'Neil, 1992
). Ornduff (1975)
reported average total pollen loads on stigmas of L. junceum to be 246, 231, and 223 pollen grains in the long, mid, and short morphs, respectively. Mulcahy and Caporello (1970)
estimated pollen flow in intact and emasculated flowers of L. salicaria. In intact flowers of L. salicaria, the pollen loads per stigma were 2087 in the longs, 3795 in the mids, and 1696 in the short morphs (Mulcahy and Caporello, 1970
). However, estimated pollen loads (pollen brought into the emasculated flowers, corrected for contamination) were 381, 482, and 384 pollen grains per stigma of long, mid, and short morphs, respectively. Total pollen loads in another tristylous species, Pontederia cordata, were 232.6, 265.1, and 180 in the long, mid, and short stigmas, respectively (Barrett and Glover, 1985
). Ganders (1979)
also reviewed stigmatic pollen loads of distylous species. The pollen loads of pin stigmas are much greater than the thrums in species of Primula, Jepsonia, and Lithospermum (Ganders, 1979
). These observations clearly indicate that pollen flow in heterostylous species is largely asymmetric. This asymmetric pollen flow may be caused by the size differences of stigmatic receptive areas (Dulberger, 1992
), differential pollen production among anther whorls (Dulberger, 1992
), and accessibility of pollinators to stigmas (Ågren, 1996
; Ågren and Ericson, 1996
). Even if the pollen capture efficiency of stigmas of each morph in L. salicaria were the same, morph-specific floral morphology could influence the efficacy of pollen transfer by pollinators (Barrett and Glover, 1985
).
In L. salicaria, the ratios of stigma diameters in the three morphs (i.e., L/S:M/S:S/S) are 1.43:1.07:1, while those of the papillae lengths are 1.44:1.08:1. Mal (1998)
recently measured the length of epidermal cells of styles and stamens in the three style morphs. The ratios of the length of epidermal cells of styles were found to be 1.47:1.16:1. These three sets of ratios are almost identical, indicating that the developmental processes for intrinsic heterostylous character (i.e., differential style lengths) and ancillary heterostylous characters such as stigma diameter and papillae length are the same. Lewis (1949)
suggested that similar genetic control governs the papillae size and style lengths and that the elongation of stylar epidermal cells and stigmatic papillae are physiologically inseparable and their development follows a similar body plan. There are exceptions, however, in which larger stigma and papillae have been documented in the thrum or short morphs (see Dulberger, 1992
; Eckert and Barrett, 1994
), indicating that they are physiologically independent and separate characters (Dulberger, 1992
). The ratios of length and diameter of pollen from long, mid, and short stamens of L. salicaria, calculated from Bir Bahadur, Bangaru Laxmi, and Rama Swamy (1984a)
were 1.47:1.12:1 and 1.47:1.07:1, respectively. In another tristylous species, L. junceum, the ratios of length of stigmatic papillae and pollen diameter were found to be 1.51:1.04:1 and 1.72:1.11:1, respectively (Dulberger, 1970
). These again suggest that the genetic control that manipulates style lengths, stigma diameter, and papillae lengths also controls pollen size. The shape and structure of polymorphisms of papillae and pollen grains may play a significant role in incompatibility mechanisms (Dulberger, 1975
), and the pollen size polymorphism in L. salicaria may be correlated with papillae polymorphism.
Incompatibility in the stigma operates at least at three levels: (a) adhesion of specific pollen to specific stigma, (b) pollen hydration, and (c) pollen tube growth within the stigma (Ghosh and Shivanna, 1982
). Dulberger (1975)
suggested that stigmatic papillae and pollen polymorphisms are involved in incompatibility mechanisms particularly at the pollen adhesion stage. Complimentarity has been demonstrated between pollen exine structure and the shape of stigmatic papillae in many distylous species (Dulberger, 1992
). In Limonium meyeri, Limonium sinuatum, Limonium oleifolium, and Limonium gracum type B pollen (from the thrum morph) do not adhere to thrum stigmas that are papillate (Dulberger, 1975
). Pollen and stigma dimorphisms in Goniolimon tataricum and Acantholimon glumaceum have also been suggested to play a role in incompatibility (Baker, 1966
; Schill, Baumm, and Wolter, 1985
; Dulberger, 1992
).
In summary, the present paper demonstrates that (1) the average diameter of the long-morph stigma is significantly larger than the mid- and short-morph stigmas; (2) the stigmatic papillae are significantly larger in the long morph than in the mid morph followed by the short morph; (3) the density of papillae in the mid and short stigmas is greater than in the long stigma; (4) the estimated number of papillae per stigma is similar in all three morphs; and (5) the long morph can be easily identified from the mid and short morphs by its papillae dimensions. In a subsequent paper, we will present a quantitative analysis of pollen polymorphism from the same individuals and will also attempt to establish a correlation between stigma surface polymorphism with those of the pollen. The stigma polymorphism coupled with those of pollen may play a functional role in facilitating legitimate pollinations.
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FOOTNOTES |
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4 Author for correspondence, current address: Department of Biological, Geological and Environmental Sciences, Cleveland State University, 2399 Euclid Avenue, Cleveland, Ohio 44115-2403, (phone: (216) 687-2444, FAX: (216) 687-6972, mal{at}biology.csuohio.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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———, and L. Ericson. 1996 Population structure and morph-specific fitness differences in tristylous Lythrum salicaria. Evolution 50: 126–139.
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} = 0.017 and 0.0004 for P = 0.05 and 0.001, respectively; *** P < 0.001
