[396] MORPHOLOGY OF ABNORMAL FLOWERS IN SOME ANGIOSPERMS
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1 [396] MORPHOLOGY OF ABNORMAL FLOWERS IN SOME ANGIOSPERMS I BY S. B. KAUSIK, M.SC. Central College, Bangalore With 5 figures in the text N the following study, a description is given of five cases of abnormalities of flowers. The abnormalities fall into two categories, viz. virescence and phyllody of the floral organs and petalody of the stamens. The two categories will be treated separately. VIRESCENCE AND PHYLLODY Tropaeolum majus (garden nasturtium). The phenomena of virescence and phyllody of the floral parts proceed regularly through a series of stages and culminate in the formation of an axial foliar shoot from the flower. The different stages are as follows: (i) The first sign of the abnormality of the flower is the shortening of the spur, which disappears completely by the time the petals are fully virescent, and the ovary becomes raised on a fleshy stalk, the "gynophore". The carpels are inflated and contain abnormal ovules (Fig. I a). Microtomed and stained serial sections of the ovary were examined for determining the nature of the abnormalities of the ovules. In these, the integuments are greatly enlarged as foliaceous structures, possessing all the characteristic features of the ordinary leaves, such as the stomata in the epidermis, a pigmented mesophyll with the palisade (on the inner surface of the integument) and the spongy tissues and well-developed vascular strands. These vascular strands are separated from a large tracheal mass at the chalazal region of the ovule, from which a strand passes also to the nucellus (Fig. I b). The nucellus, the apex of which is tapering into the micropyle, is small relatively to the size of the integuments. The embryo sac appears as a much reduced cavity, the traces of which may be
2 Fig. I. Tropaeolum majus. a, d, e and/, different stages in the transformation of the floral parts in the abnormal flowers; b, longitudinal section of ovary in a; 0, same showing only the ovary, E.S. embryo sac; g, the foliar shoot in place of ovary in the flower in/; /;, two stages in the phyllody of the anthers in the same flower; i, section of a foliaceous anther.
3 398 S. B. KAUSIK entirely lost a little later. It may be inferred from these observations, that the phenomenon of phyllody extends to the ovules at quite an early stage of their development, and that the growth of the integuments alone is emphasized (Fig, ic). The stamens are perfectly regular and the anthers contain normal pollen grains, (ii) The infiated carpels mentioned above open out into leaf-like structures and the traces of the ovules are lost (Fig, i d). The anthers, however, appear to be normal externally, but contain a very large percentage of sterile pollen grains. The other floral parts are approximately at the same stages of transformation as in (i). (iii) The carpels of the ovary are completely leaf-like and are borne on fairly long petioles springing from a common stalk, which corresponds to the fleshy gynophore of the previous stages (Fig, le). The anthers, while continuing to be normal externally, show a high degree of virescence with the development of the stomata and the chlorophyllous tissue. The anther locules are reduced to narrow spaces (Fig, ^i) and the pollen grains are all sterile. The petals are more leaf-like, both in contour as well as in venation, than in the preceding stages. (iv) An extreme stage of the abnormality of the flower is that where the ovary is replaced by a foliar shoot (Fig, if). The anthers begin to show all external features of phyllody, the bases of the anther lobes spreading out as green expansions (Fig, ih, i). The anthers are thus the last of the floral organs to become phyllodes, Trichosanthes anguina (snake gourd), The male flowers, where the petals are completely transformed into leaves, show various degrees of phyllody of the anthers, and the most complete stage is that of an extensive foliar shoot springing from the centre of the flower (Fig, 2e). The sinuous anthers pass successively through a series of changes, the anther loops loosening gradually and the connectives becoming flattened more and more to form leaf-like structures (Fig, 2c, d). The anther locules are correspondingly reduced and produce abnormal pollen grains. Fven in the early stages of the phyllody of the anthers, the stomium is absent and the endothecium loses its characteristic fibrillar nature. The chlorophyllous tissue which begins to develop at this stage with the formation of the stomata (Fig, 2c) becomes more conspicuous and extensive in succeeding stages of phyllody. The male flower seems to be always in advance of the female flower in so far as the formation of an axial foliar shoot is concerned, because the ovary is already degenerate even in the normal male flowers. In the female flower, on the other hand, the initial stages of
4 Morphology of Abnormal Flowers in some Angiosperms 399 Fig. 2. Trichosanthes anguina. a, early stage in the abnormality of a male flower, petals leaf-like but the anthers normal; b, another of same with section and part enlarged; c and d, stages in the phyllody of tlie anther with sections enlarged; e, male flower with a well-developed a.xial foliar shoot.
5 400 S. B. KAUSIK the formation of a foliar shoot would be the disappearance of the ovules on the placental ridges, which then are thrown into a number of folds (as seen in a transverse section). The folds of adjacent ridges fuse together and form a central axis which proliferates into a shoot. Allamanda grandiflora. With the transformation of the petals into phyllodes, the ovary is replaced by a fairly elongated axis, which bears terminally a pair of leaf-like structures, the carpels. The anthers, which are normal externally, become massive on account of an increase in the size of the connectives. The anther locules are reduced in size and contain a very few sterile pollen grains (Fig. 3 c). The wall of the locules contains the chlorophyllous tissue with stomata in the epidermis. The fibrillar nature of the endothecium is lost, while the stomium may persist to some extent. In one or two abnormal flowers, axillary buds were found in the axils of the petals (Fig. 36). The vascular strands for the buds are continuous with the main vascular strand that passes into the "gynophore" of the leafy carpels. The most interesting abnormality was seen in the ovaries of only two flowers. In these, the axis of the abnormal ovary bears distally two carpels, which separate and tend to grow out into two leaf-like structures (Fig. 3^). Higher up, the two carpels again meet, bear a number of ovules and form a short style and a large stigma. The ovary in these abnormal flowers is, therefore, an open one, and the ovules are clearly visible from the outside on account of the separation of the carpels at the base of the ovary. In one of the abnormal ovaries mentioned above there is a single terminal vegetative bud between the two carpels (Fig. 3?). The vascular supplies to this bud are in continuation with the vascular cylinder in the gynophore-hke axis below the level of the separation of the carpels. The vascular strands of the carpels are also connected on to this main cylinder. In the other abnormal ovary, there are two vegetative buds within the carpels (Fig. 3/, g). These two buds are derived by a splitting of the apical portion of the gynophore-like axis. The ovules which are borne on the partially opened semi-foliar carpels of these ovaries seem to develop normally (an ovule at the megaspore mother cell stage is represented in Fig. 3/t), but whether they continue to form fully developed embryo sacs must for the present remain an open question, as more material for study could not be procured.
6 Morphology of Abnormal Flowers in some Angiosperms 401 Fig, 3. Allamandagrandiflora. a,flowerwith a pair of "leaves" in the place of the ovary; b, longitudinal section of flower showing apparently normal anthers and an axillary vegetative bud; c, transverse section of anther in 6; d, two views of an abnormal (open) ovary; e, longitudinal section of an abnormal ovary with one vegetative bud terminally; /, same as above with two buds; g, same enlarged to show ovules; h, an ovule from above at the megaspore mother cell stage, PHVT. XXXVII. 5 26
7 402 S. B. KAUSIK PETALODY The phenomenon of petalody is described here in only one case. In the abnormal flowers of the yellow variety of Jasminum (Fig. 4 a), the sepals are fewer in number but larger in size than in the normal flowers. The ovary is perfectly normal and the only condition of abnormality is seen in the transformation of the anthers into petaloid structures (Fig. 46). The two anthers of a flower may show identical or different degrees of petalody. In the earlier stages, while one of the anther lobes of a stamen may be completely formed into a petal, the other lobe may remain perfectly normal and produce regular pollen grains (Fig. 41:). In advanced stages of petalody, the connective is broadened out and the anther locules are greatly reduced (Fig. 4^) or completely absent. In a solitary case of a flower showing petalody of the anthers, one of the petals contained a very small accessory flower in its axil. This accessory flower had only four petals, while the other floral organs were missing (Fig. 4«). The e.xact relationship of this flower to the parent flower could not be studied for want of more material, and a further search for similar instances was of no avail. Utricitlaria coertdea. While the author was engaged in a study of the development of the gametophytes and embryo in U. coerulea, a solitary case of an abnormal ovary was accidentally discovered during an examination of the slides. The massive placenta shows here a splitting into two portions, one immediately becoming leaf-like (Fig. 4/), while the other, after a second splitting a little later, forms a reduced placenta and a second leaf-like structure (Fig. 4^). The placenta bears a few ovules, which contain regularly developed complete embryo sacs (Fig. 4A). The apex of the placenta, which in the normal ovary is only slightly elevated, is here prolonged extremely and passes in the stylar canal which is thus blocked. Therefore, the pollen tubes may perhaps be prevented from entering the ovary through their usual channel in the style and the ovary may fail to set seeds in the abnormal flowers. Since externally there is absolutely no indication of the abnormahty, it is impossible to pick out the abnormal ovaries for study and hence a further detailed examination could not be undertaken.
8 Morphology of Abnormal Flowers in some Angiosperms 403 Fig. 4. a-e, Jasminum. a, flower with petalody of stamens; b, longitudinal section of same; c and d, sections of the two petaloid stamens at different stages; e, accessory flower, f-h, Utyiciilaria coeriilea. / and g, longitudinal section of abnormal ovary at different planes to show the leaf-like structures formed by the splitting of the placenta and a few ovules; /;, one ovule of above enlarged to show the completely developed normal embryo sac. 26-2
9 404 S. B. KAUSIK VASCULAR ANATOMY OF THE ABNORMAL FLOWERS During the course of this study, it was thought that an examination of the vascular anatomy of the abnormal flowers would perhaps throw some light on the nature of these abnormalities, and the following account is therefore included. In all cases the vascular strands that enter the different floral parts are similar to those in normal flowers. In Tropaeolum majus, after the formation of the vascular supplies to the sepals and the stamens, three large strands pass into the base of the ovary, where each splits into an inner and an outer portion (Fig, 5), The inner portion runs in the axis of the ovary and is exhausted below the stj'le. The outer portion splits into a number of small strands which run in the ovary wall. The separation of these smaller strands is similar to the formation of a number of strands in the ordinary leaves. In the anthers also, with progressive phyllody, the number of strands increases from one in the very early stages, to several later on (Fig, 51), In the female flowers of Trichosanthes anguina showing phyllody, the ovary has three larger outer strands and a group of smaller inner ones arranged triradiately (Fig, 5), Later on, these smaller strands spht further and are gradually lost, while the three outer larger ones increase in size (F"ig, 5/, m), and when the foliar axis is formed by the fusion of the placental ridges become more or less continuous to form a ring, which closely resembles the vascular structure of the ordinary vegetative axis. In the peculiar abnormal ovary of Allamanda grandiflora, the vascular strands are numerous and form a ring in the gynophorelike stalk of the ovary (Fig, 59), When the carpels separate the entire ring divides into two halves, which pass into the two carpels (Fig. 5?-), Higher up the number of strands in each carpel is reduced to three, one median dorsal and two lateral ventrals. The median dorsal strand disappears in the style and the lateral ventrals fuse and give rise to a stylar strand (Fig, 5«). This strand is greatly expanded in the stigma. The separation of the carpellary strands is similar to the separation of a leaf strand in the vegetative portions of the plant. The only difference perhaps is, that while in the case of a leaf a single large trace is separated from a well-developed continuous vascular ring of the vegetative axis, in the case of the ovary a number of smaller strands are separated to supply the carpels.
10 Morphology of Abnormal Flowers in some Angiosperms 405 TROPAEOLUM V Fig. 5. The vascular structures in the various abnormal flowers. At a is shown the vascular strands in a longitudinal section of a normal flower of Tropaeolum majus for comparison. The numbers in each series indicate transverse sections at successively higher levels.
11 4o6 S. B. KAUSIK DISCUSSION The abnormal features of flowers described here are regarded as reversions in which there is a reappearance of ancestral characters. The phenomenon of petalody may suggest that the members of the adjacent floral whorls show sometimes a certain amount of indefiniteness, namely, whether they should form one or the other floral part in the course of the evolution of the flower. The formation of an axial foliar shoot from the flower is an extreme case of the transformation of a flower, the initial stages m this being virescence and phyllody. But by reversions to an ancestral condition it is not even remotely suggested that the floral parts are in any sense metamorphosed foliar appendages as envisaged by Goethe so long ago. The different floral organs do not show the same degree of mutability, and from the examples cited in this paper it is evident to some extent that the outer two whorls, those of the calyx and the corolla, which are already more leaf-like (more particularly the whorl of the calyx) than the other two inner whorls even in the normal flowers, show the stages of transformation less strikingly than the androecium or the gynoecium. The least susceptible to phyllody is the androecium, for it is only after all the other floral parts are affected that it shows signs of transformation. In the earlier stages it is externally perfectly normal for all purposes, though in its contents, the pouen grains, a certain degree of sterility may set in. It becomes foliaceous only after the innermost whorl, that of the carpels, has proliferated into a foliar shoot. The floral organ that is affected earliest is the gynoecium, because the floral parts constituting it, the carpels, are the nearest placed to the growing point of the floral shoot and the latest formed lateral organs on the floral axis. The presence of a gynophore in the abnormal flowers of Argemone mexicana is stated by Joshi (1933) to be of phylogenetic importance, and he states that the development of this structure emphasizes the relation of the Papaveraceae to the Capparideae. On the other hand, a gynophore-like stalk is present in all instances of abnormality of the ovary mentioned in this paper, and this structure may be held to be of general occurrence in an ancestral condition of the ovary. Accessory flowers have been described in Nasturtium officinale by Halket (1932) and Arber (1931). The latter states that it is difficult to interpret the relation of the accessory flowers to the parent flower, but suggests that they cannot be described as axillary to the petals
12 Morphology of Abnormal Flowers in some Angiosperms 407 and that the petal plays the part of an axis rather than a leaf. The accessory flower in fasminum may be regarded as axillary to the petal, which is considered to be of the nature of a leaf. Similarly the presence of a vegetative bud between the floral axis and the petal in the abnormal flowers of AUamanda may indicate an identical morphological nature for the petals. The point of view from which the author regards the abnormahties here described is conveyed by the following statement of Worsdell (1915): " In very many cases the so-called ' freaks ' and ' monstrosities' represent reversions or harkings-back, in one form or another, to an ancestral condition, but this will alwaj^s take place in a way which is modified by the structure and idiosyncrasies of the organ which is undergoing change. For example, a vegetatively proliferated rose, whose floral organs change into green leaves and become vertically displaced owing to the elongation of the floral axis, tells us better than the facts of its ontogeny would, better than those of its anatomical structure, better even than any comparison of theflowerin its normal state with any other type of flower, that the flower has been derived in the past by congestion and abbreviation of an axis, and by the extreme reduction and modification of leafy sporophylls. But it would be absurd to suppose that the leafy shoots from which our flowers originally sprang in any sense resembled, save in the matter of possessing an elongated axis and leafy sporophylls, those into which our modern flowers so frequently proliferate. Under special conditions of nutriment and moisture, the older tendency to break the bonds which an adaptive evolution has placed upon the flower becomes manifested." ACKNOWLEDGEMENTS Some of the materials mentioned in this paper were very kindly passed on to the author by his colleagues. Prof. L. Narayana Rao, M.Sc, F.R.M.S., and Mr A. R. Gopalaiyengar, M.Sc, and considerable assistance in the preparation of microtome sections was rendered by Mr M. Ananthasamy Rao, B.Sc. To each of these sincere thanks are due; for the views expressed here the author alone is responsible. Finally, grateful acknowledgement is made to Dr M. A. Sampathkumaran, M.A., Ph.D. (Chic), University Professor of Botany, University of Mysore, for all facilities and kind encouragement during the course of this work.
13 S. B. KAUSIK REEERENCES ARBER, A. (1931), Studies in Floral Morphology, II. On some normal and abnormal Crucifers: with a discussion on Teratology and Atavism. New Phytol. 30, , HALKET, A. C, (1932). A note on the occurrence of abnormal flowers of Nasturtium officinale R.Br. New Phytol. 31, , JosHi, A, C. (1933). Some abnormal flowers of Argemone mexicana Linn, /, Ind. Bot. Soc. 12, MASTERS, M, T. (1886), Pflanzenteratologie. Leipzig. WoRSDELL, W, C. (1915). The Principles of Plant Teratology. London,
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