Podostemaceae-the strange family of aquatic angiosperms
H. Y. Mohan Ram & Anita Sehgal
Mohan Ram HY & Sehgal A 1992. Podostemaceae-the strange family of aquatic angiosperms. Palaeobotanist 41 : 192-197_
Podostemaceae is a unique family of aquatic angiosperms. The vegetative body of the podostemads is represented by a thallus resembling that of an alga, lichen or a bryophyte, and lacking the conventional demarcation into stem, leaf and root. The podostemads invariably inhabit gushing mountain streams or falls and generally grow attached to rocks. They lack aerenchyma. Flower buds are initiated while submerged, but flowering and fruit development occurs when the water level subsides and the plants become exposed. Taxonomists believe that podostemads have affinities with Crassulaceae, Saxifragaceae and Hydrostachydaceae. Podostemaceae are termed an embryological family owing to the lack of antipodals, triple fusion, endosperm, the prevalence of single fertilization, and the presence of a pseudo-embryo sac. The wide range of phenotypic plasticity, morphological nature of the thallus as understood by developmental studies using in vitro cultures, and embryological features of the family are discussed. The origin, adaptation and affinities with closely related families have also been examined. Key-words- Taxonomy, Podostemaceae, Aquatic angiosperms, Embryology, Polymorphism.
H. Y. Mohan Ram, Department of Botany, University of Delhi, Delhi 110 007, India. Anita Sehgal, Department of Botany, Miranda House, University of Delhi, Delhi 110007, India_ mmr
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~ ~ ~Iqf\f ~ ~ ~I ~ ~ ~ ~ ~, ~ ~ ~I~ ~ -# \ft EVOLUfIONISTS believe that diversity and unity are waterfalls and in rapidly flOWing streams where only twin themes that characterize the tiving world. certain mosses' and algae survive. The family is Evolution is considered as a means to reconcile represented by 46 genera and 260 species (Cook, these contrasting, mutually exclusive phenomena 1974). However, Nagendran (1975) lists 49 genera (Savage, 1965). Two results of evolution are and 240 species. The members are restricted to adaptation and specialization. Adaptation refers to tropical and subtropical regions of the world. efficient interaction with environment and Twenty species are recorded from India, of which 18 specialization means occupying restricted niches. are endemic. Most of these are concentrated in the The Podostemaceae present a challenging task to Western Ghats, whereas a few occur in Meghalaya, study these phenomena. The podosternads grow attached to waterworn Essays In Evolutionary Pl2nt Biology rocks, boulders and wood pieces located under Edllors ,B. S. venkatachala, David L Dllcher II: Hari K. Maheshwari PubllsbBr' Blrbal Sahnl Institute of Palaeobotany, Lucknow MOHAN RAM & SEHGAL-PODOSTEMACEAE: STRANGE FAMILY OF AQUATIC ANGIOSPERMS 193 Madhya Pradesh, Orissa, Maharashtra and Goa Polypleurum stylosum, crustaceous in Hydrobryopsis (Vanak & Bhadbade, 1973). The populations of sessilis and thread-like in Indotristicba ramosissima. podosteniads, though localized, are dense indicating The ability of these plants to develop into their relative fitness. exceptional forms can perhaps be attribut~dto the Willis (1902) described Podostemaceae as absence of a rigid skeletal system (Sculthorpe, having "most varied morphological structure". Arber 1967). Podostemads have no conventional (1920) in her monumental work on water plants distinction into stem, root and leaf. The thallus bears referred to this group as "peculiar and anomalous". gum-secreting rhiwids which cement it to the Sculthorpe (1967) has remarked: "There is surely no substratum. The vertical section of a thallus of stranger and more provocative family of angiosperms Grillitbella shows no vasculature. The thallus cells than Podostemaceae". A combination of contain copious amount of silica granules, the characteristics that make them an unusual family significance of which is not known. Aerenchyma, so among angiosperms are: their thalloid growth habit, characteristic of the hydrophytes is absent in the perplexing polymorphism, marked structural Podostemaceae. The probable reason for this could reductionism, presence of unique embryological be the firm attachment of thalli to the substratum features, submersed vegetative and emersed which obviates the necessity for buoyancy. reproductive phase. Podostemads start their annual life cycle with Taxonomical and embryological accounts on the onset of monsoon. Their seeds are tiny. Podostemaceae are available (Tulasne, 1852; Vidyashankari (1988a) reported that 1,236,100 seeds Maheshwari, 1955; Chopra & Mukkada, 1966; of Grilli/bella bookerlana weigh one gram. The Takhtajan, 1966; Battaglia, 1971; Nagendran, 1975; number of seeds per fruit varies from 2-8 in Cronquist, 1988). Nevertheless, the amount of Farmerla (Arekal & Nagendran, 1974) to 240 ± 25 in unknown information is vast, probably because of Polypleurum stylosum (Mohan Ram & Sehgal, the obscurity and inaccessibility of material for unpublished). study. Swollen rivers dissuade botanists to make In the taxa investigated by us, I.e., Dalzellta field investigations, especially during the period of zeylanica, Grilli/bella bookerlana (Vidyashankari, seedling establishment in nature. According to 1988a, b), Hydrobryopsis sessilis, Indotrtsttcba Pannier (1960) "the reason for the lack of research ramosissima, Polypleurum stylosum, Zeylanidtum on this interesting group of plants is undoubtedly licbenoides, the embryo shows two large cotyledons due to impossibility of maintaining them alive out of and a highly reduced primary axis without a their natural habitat for any period of time". recognizable division into radicle and plumule. During imbibition the seeds secrete mucilage. On SEED GERMINATION, THAllUS germination, the expanding cotyledons break open DEVELOPMENT AND the seed coat and emerge out of it. The radicle fails MORPHOLOGY AND FLOWERING to develop a root. Instead it forms several unicellular rhiwids which secrete gum. In Grtllttbella the gum It is difficult to collect seedlings in nature and has been shown to be a polysaccharide unless a comparative account of germination in the (Vidyashankari, 1988a). The cotyledons continue to family is carried out, the true nature of the plant elongate and reflex. A plumule is organized post body will remain enigmatic. Nagendran (1975) was germinally and the first leaf-like structure appears the first to germinate the seeds of nine taxa under one week after germination. The number of leaf-like laboratory conditions. However, he was unable to structures formed by the plumule varies from keep the seedlings growing beyond a few days. species to species (unpublished work) after which Our research group at the University of Delhi the plumular activity ceases. Further development has successfully developed a simple and occurs by the transfer of meristematic activity to the reproducible technique of raising podostemads from hypocotyledonary portion. A small protuberance is seeds to mature plants in axenic cultures formed, which develops into a dorsiventral, (Vidyashankari, 1988a, b; Vidyashankari & Mohan branched chlorophyllous thallus, typical of the Ram, 1987; Mohan Ram & Sehgal, unpublished). It is respective species. In Polypleurum stylosum, thallus envisaged to investigate the ultrastructure and has also been observed to arise in a few instances development of the different phases of their life from the cotyledons and leaf-like structures in the cycle. In the taxa investigated by us, the plant body seedling. After expansion the thallus also bears leaf is thalloid and bewilderingly polymorphic. It is star like structures (Vidyashankari, 1988a)/secondary like in Dalzellia zeylanica, cup- or funnel-like in shoots (Willis, 1902) along the margins and rhizoids Grillitbella bookeriana, ribbon-shaped in on the ventral surface. The ontogeny of these has not 194 THE PAlAEOBOTANIST been worked out in detail. The morphological Table I-Relationships between Podostemoideae and nature of the thallus is also a maHer of dispute. Tristichoideae" Nagendran (1975) believes that it represents a stem DissimIlarities whereas Tulasne (1852), Warming (1891), Willis CHARACfERS llHSTlCHOIDEAE PODOSTEMOIDEAE (1902) and Engler (1930) argue for its root origin. The work done by Vidyashankari and Mohan Ram Flowers Trimerous Dimerous (1987) on Grifjithella hookeriana and by us on Perianth Present Absent Spathe Absent Present Polypleurum stylosum suggests that the thallus Stamens 1·25 Many (l or 2 in Indian originates as an extension of the hypocotyledonary raxa) region of a young seedling. Staminodes Absent Present Flower buds are initiated when the plants are Pollen Monads Dyads submerged and the water level is 25-40 cm above the Ovary Tricarpellary Bicarpellary Ovules Many, bitegmic Few to many, bitegmic thalli. With the falling of the water level in the river, Pseudo-embryo Organized after Arises before the thalli become exposed to the aerial sac fertilization fertilization environmenL The leaf-like structures/secondary Embryo Plumule Plumule nor shoots gradually are replaced by reproductive shoots differentiated (?) differentiated in the subsequent growth of the exposed thalli. Similarities There are no studies on the mechanism of Embryo sac Apinagia type Apinagia, Podostemum pollination. Fruit development occurs above water. Podostemum type and Polypleurum What factors initiate flowering in nature is not type understood. Nevertheless, we have been able to Fertilization induce flowering under in vitro conditions by Single Si-ngle (only syngamy) (only syngamy) subjecting the plants of Polypleurum stylosutn and Endosperm Absent Absent Indotristicha ramosissima to stress. The signals Embryogeny Solanad type Solanad type responsible for induction need further investigation. Embryonal Present Present haustorium EMBRYOLOGICAL FEATURES "Reproduced from Nagendran (1975). The Podostemaceae are recognized as an the ancestOrs of Podostemaceae must have been embryological family because of the several land plants. He presumed that they might have taken remarkable features not known in such combination to water at one time and undergone whole of the in any other angiosperm family. Among the notable evolution in water. It was a riddle for Willis to characteristics are lack of antipodals, absence of account for the origin of diverse morphological double, fertilization and endosperm, presence of a forms within the family under what he considered pseudo-embryo sac and Single fertilization (Razi, most uniform conditions proVided by running water. 1949; Maheshwari, 1955; Mukkada, 1962, 1969; He explained it as cumulative mutations without Chopra & Mukkada, 1966; Kapil, 1970; Battaglia, natural selection. He believed that the thallus had no 1971; Mukkada & Chopra, 1973; Nagendran, 1975; adaptive significance to the plant and that Nagendran & Arekal, 1976; Arekal & Nagendran, Podostemaceae may have a continuum of genotypes 1974, 1975a, b, 1977a, b; Nagendran et al., 1981). with more specialized to less specialized forms. Though syngamy is normal, the fate of the second Tristichoideae are believed to be represented by male gamete is disputed (Mukkada, 1962; Walia, three genera, whereas Podostemoideae include the 1965; Chopra & Mukkada, 1966). others. Members of the family Tristichoideae are The family Podostemaceae has been divided simple, less-specialized and more Widespread into two subfamilies-Tristichoideae and (Willis, 1902). They have greater tOlerance to Podostemoideae. Table 1 presents similarities and environmental fluctuations and therefore occupy dissimilarities between the Podostemoideae and more trophiC niches. The structure of Indotristicha Tristichoideae regarding floral and embryological ramosissima has been described in detail by features (Nagendran, 1975). It is apparent that there Rutishauser and Huber (unpublished)·. According are two distinct lines of evolution within the family. to them, the plant has creeping roots with several . rhizoids on the ventral surface. It bears (a) ORIGIN AND EVOLUTION secondary and tertiary roots with a root cap, (b) The origin and evolution of the Podostemaceae "This work has since appeared in Plant Systematics and are perpleXing questions. Willis (1915) believed thaI Evolution 1991, 178: 195-223. MOHAN RAM & SEHGAL-PODOSTEMACEAE: STRANGE FAM1LY OF AQUATIC ANGIOSPEIU,,1S 195 holdfasts, and (c) floating shoots with flowers at the (Szafer, 1952) from West Carpathian mountains. The tips. Several ramuli are produced on the shoots. It is latter has unisexual flowers, 3 sepals united in the in the tribe Tristichoideae that one finds the middle, 3 free petals, 6 free stamens. Female flowers transition from regular erect branches to prostrate, are not known. Stomata are present. flat and dorsiventral thalli. The trend towards As only fragmentary information is available on dorsiventrality continues in the tribe the fossil Podostemaceae, it is difficult to throw any Podostemoideae and even permeates the most light on the affinities of podostemads. When Aublet conservative organ, i.e., flower (with the loss of discovered Mourera jluviatilis in 1775, he placed it some stamens and obliquity of gynoecium and seed) with the monocots. In 1815, Richard described (Willis, 1902). In contrast to Tristichoideae, Podostemon ceratophyllum and raised it to the rank Podostemoideae are highly specialized and of a family, viz., Podostemeae, although he still consequently occupy narrow niches. The seemingly considered this group to have monocotyledonous simple structure of Podostemaceae appears to be a affinities. Subsequently it was placed among the case of reduction. dicotyledons by Lindley (1847). Bentham and Hooker (1880) placed this family in Multiovulatae AFFINITIES Aquaticae of Monochlamydeae. Rendle (1925), Takhtajan (1966) and Cronquist (1988) have To the best of our knowledge, two fossil records grouped it under Rosales, Rosidae (Magnoliatae) of Podostemaceae are available from the Tertiary and Rosidae (Magnoliopsida), respectively. The Period in Europe. These are: (i) Podostemonopsis pioneering works of Gardner (1847), Tulasne tertiaria (Weyland, 1937) from Siebengebirge on the (1849), Warming (1901) and Willis (1902) have river Rhine, and (ii) Podostemonites corollatus contributed immensely to the understanding of the Table 2-Embryological relationship with related famlUes· CHARACfER PODOSTEMACEAE HYDROSTACHYDACEAE SAXIFRAGACEAE CRASSULACEAE Anther wall 4 or 5 layered - 4 layered 5 layered Anther tapetum Secretory Secretory Secretory or amoeboid Secretory \ Microsporogenesis Simultaneous or Simultaneous Simultaneous Simultaneous successive Pollen grains Monads or dyads, Compound, Monads or Monads shed shed at 2-celled permanent in tetrads at 2-celled stage tetrads stage Gynoecium 2 or 3 carpellary, Bicarpellary, 2-5 carpellary Apocarpous ovary syncarpous syncarpous ovary syncarpous, 2 or 3 locular unilocular 2·5 locular Ovules Many, tenuinucellate Many, tenuinucellate Many, crassinucellate Numerous on marginal bitegmic, on axile unitegmic. anatropous or tenuinucellate placenta, anatropous placenta on parietal placenta bitegmic/unitegmic crassinucellate. on axile placenta bitegmic Megaspore tetrad No linear tetrad Linear [j near/bisporic Linear/T-shaped! formed isobilateral Embryo sac Bisporic, Apinagia Polygonum type Polygonum type Polygonum type development Podostemum/Poly- and Allium type pleurum type, mature embryo sac 4 or 5 nucleate Antipodal cells Absent (2 in Dicraea ?) Present Present Present Pseudo-embryo sac Present Absent Absent Absent Embryogeny Solanad. suspensor Onagrad type- Caryophyllad Caryophyllad haustoria present Capsella variation, type, Sedum type, suspensor suspensor variation haustorium absent haustorium absent ·Modified after Nagendran (1975). 196 THE PAlAEOBOTANIST Indian Podostemads. Battaglia E 1971. The embryo sac of Podostemaceae-an inter Taxonomists have held various views pretation. Caryologia 24 : 403-420. Bentham G & Hooker JD 1880. Genera Plantarum 3 : 105-115. concerning the relationships of the Podostemaceae London. with other angiosperm families. For example, Chopra RN & Mukkada AJ 1966. Gametogenesis and pseudo Podostemaceae have been related to Saxifragaceae embryo sac in Indotristicba ramosissima (Wight) Van Royen. (Warming, 1888; Engler, 1930); Crassulaceae Pbytomorpbology 16 : 182-188. (Hutchinson, 1959); Hydrostachydaceae Cook CDK 1974. Water plants of tbe world. W. Junk b, v. Publi (Subramanyam, 1962). The embryological features of shers, The Hague. Cronquist A 1988. The evolution and classificatton of flowering families related to Podostemaceae are presented in plants. The New York Botanical Garden, New York. Table 2. Engler A 1930. Podostemaceae. In Engler A & ?rant! K (edltors) On the basis of embryological studies Die naturltcben Pflanzenfamtlten: 18. : 1-68. Leipzig. Maheshwari (1945) had observed that the Gardner G 1847. Observations on the structure and affinities of Podostemaceae are much reduced apetalous the plants belonging to the natural order Podostemaceae. Calcutta Univ. j. nat. Hist. 7 : 165·189. derivatives of the Crassulaceae. Hutchinson J 1959. The families of flowering plants. I. Ed. 2. Thorough study is needed to understand and Clarendon Press, Oxford. interpret the wide range of morphological and Kapil RN 1970. Podostemaceae. Bull. Indian natn. Sci. Acad. 41 : physiological variability of the family. Because of 104-109. their endemic nature and habitat specialization, the undley J 1847. The vegetable kingdom (Ed. 2) : 482-483. London. Maheshwari P 1945. The place of angiosperm embryology in podostemads are vulnerable to anthropogenic research and teaching. j. Indian bot. Soc. ·24: 25-41. changes in the environment. There is justifiable Maheshwari SC 1955. The occurrence of bisporic embryo sacs in need to conserve their biodiversity. Methods for angiosperms-a critical review. Pbytomorpbology 5 : 67 -99. their in vitro cultivation have been developed by our Mukkada AJ 1962. Morphological and embryological studies on some Indian Podostemaceae. Pb. D: Tbesis, University group, which makes their ex situ conservation and of Delhi. study a possibility. Mukkada AJ 1969. Some aspects of the morphology, embryology and biology of Terniola zeylanica (Gardner) Tulasne. New ACKNOWLEDGEMENTS Pbytol. 68 : 1145-1158. Mukkada AJ & Chopra RN 1973. 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