Tiny plants make a huge impact
Paula Rudall from Kew’s Jodrell Laboratory describes how comparative studies on the micromorphology of tiny plants can help us better understand flowering plant evolution
Kew researchers are collaborating with scientists worldwide in a detailed study of Hydatellaceae, a family of tiny aquatic plants that occur in Australia, New Zealand and India. Although they are difficult to locate and tricky to examine closely, several factors make this family useful for evolutionary studies. Perhaps most importantly, they represent an early lineage of flowering plants and can therefore provide a window into their evolutionary past.
A close relationship between Hydatellaceae and water-lilies (including Nymphaea and Victoria) was discovered relatively recently, following DNA-based studies . Initially, because Hydatellaceae have linear leaves and look superficially grass-like, scientists thought they were closely related to grasses, and wrongly classified them as monocotyledons. Subsequent studies, many of them coordinated at Kew, have confirmed this dramatic reclassification.
From other analyses of both DNA and fossils, we know that the water-lily lineage is among the oldest living groups of flowering plants. Therefore, the inclusion of Hydatellaceae with the water-lilies places them close to the “root” of flowering plants and potentially gives them greater significance in understanding angiosperm evolution.
One caveat is that this relatively ancient family could have developed many unique features during its long evolutionary history, and may not even remotely resemble ancestral angiosperms. However, science depends on assessment of evidence from a wide range of sources. Their placement near the base of the angiosperm family tree means that Hydatellaceae could provide a much-needed yardstick for comparison with other flowering plants.
Our studies have demonstrated that there is a single genus of Hydatellaceae (Trithuria), rather than two genera, as previously thought . Some species are dioecious (bearing male and female reproductive structures on different plants), and remarkably, some of the dioecious species are sexually dimorphic. We found that plants traditionally known as Trithuria occidentalis and Hydatella dioica represent female and male individuals of the same biological species: two individuals of H. dioica (male plants) were still attached to the seeds that gave rise to them, and these both had the seed coat sculpturing that characterises T. occidentalis. This discovery highlights the importance of detailed comparative work, and demonstrates that some characters are unreliable in defining species or genera in this family.
As currently recognised, Trithuria consists of ten species in Australia, one in India and one in New Zealand. Our studies have allowed subdivision of the family into two subfamilies, a northern (tropical) subfamily from northern Australia and India and a southern (subtropical/temperate) subfamily from the southern part of mainland Australia, Tasmania and New Zealand . However, the geographical range and taxonomic diversity of Hydatellaceae could be underestimated: more species remain to be discovered .
These plants are so small that you need a hand-lens to see them properly. They are true flowering plants (angiosperms), but at first sight they appear more like mosses. They are dwarfed by surrounding vegetation, even by small herbs.
Hydatellaceae grow in seasonal wetlands, sometimes in shallow lakes or lake margins. Most species are annual plants that only appear at certain times of the year, when they produce many seeds that survive until the next growing season. Thus, even where they are abundant they can be very difficult to locate in their natural habitats. Field collection of some of the tropical species can be daunting, as man-eating crocodiles can lurk nearby!
A number of Hydatellaceae species are grown at Kew, and we use various different types of microscope to study many aspects of their structure. One strange feature soon caught our attention in Trithuria submersa and other species with bisexual flowers . Their flowers are “inside-out”, because the carpels (female organs) surround the stamens (male organs). In contrast, one of the primary characteristics of almost all other flowers is that the carpel zone is located in the centre, surrounded by the stamens. The stamens produce the pollen and the carpels bear the ovules. The genetic basis for the highly conserved pattern found in most flowers is increasingly well understood.
So, Trithuria submersa appears to have extremely unusual flowers. Could this mean that its reproductive units are not actually flowers? In all other respects they look like flowers: they have a radially whorled structure with a ring of sterile petal-like organs surrounding the stamens and carpels. In fact, current evidence remains ambivalent as to whether these “non-flowers” of Hydatellaceae should correctly be interpreted as flowers or inflorescences [6,7].
They could represent a structure in which typical floral patterning has been ‘lost’ during the course of evolution. Alternatively, given the phylogenetic placement of Hydatellaceae close to the base of the angiosperms, they could represent the sole survivor of an early experiment with floral patterning that differs from the pattern that rapidly became firmly established in all other flowering plants.
Following the discovery that Hydatellaceae belongs to a basal angiosperm lineage, our knowledge of many aspects of the taxonomy, comparative and evolutionary morphology, and ecology of the family has increased exponentially. Nevertheless, several important issues remain to be studied. We are investigating other aspects of morphological evolution in this interesting family, such as the structure of the pollen and stigma [8,9], ovules , fruits and seeds [11,12,13] and seedlings [14,15,] including the remarkable range of cotyledon diversity. The potential impact of these studies is to provide us with a broader understanding of what the ancestral angiosperms could have looked like. Ultimately, this knowledge is crucially important in understanding how flowering plants evolved.
- Paula -
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2. Sokoloff D.D., M.V. Remizowa, T.D. Macfarlane and P.J. Rudall. (2008). Classification of the early-divergent angiosperm family Hydatellaceae: one genus instead of two, four new species, and sexual dimorphism in dioecious taxa. Taxon 57: 179–200.
3. Iles W.J.D., P.J. Rudall, D.D. Sokoloff, M.V. Remizowa, T.D. Macfarlane, M.B. Logacheva and S.W. Graham. (2012). Molecular phylogenetics of Hydatellaceae (Nymphaeales): sexual-system homoplasy and a new sectional classification. American Journal of Botany 99: 663–676.
4. Sokoloff D.D., M.V. Remizowa, T.D. Macfarlane, S.R. Yadav and P.J. Rudall. (2011). Hydatellaceae: a historical review of systematics and ecology. Rheedea 21: 115−138.
5. Rudall P.J., D.D. Sokoloff, M. V. Remizowa, J.G. Conran, J.I. Davis, T.D. Macfarlane and D.W. Stevenson. (2007). Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early-divergent angiosperm lineage. American Journal of Botany 94: 1073–1092.
6. Rudall P.J., M.V. Remizowa, G. Prenner, C.J. Prychid, R.E. Tuckett and D.D. Sokoloff. (2009). Non-flowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae, and its bearing on the origin of the flower. American Journal of Botany 96: 67–82.
7. Rudall P.J. and R.M. Bateman. (2010). Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Philosophical Transactions of the Royal Society B 365: 397–409.
8. Remizowa M.V., D.D. Sokoloff, T.D. Macfarlane, S.R. Yadav, C.J. Prychid and P.J. Rudall. (2008). Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific level. Grana 47: 81–100.
9. Prychid C.J., D.D. Sokoloff, M.V. Remizowa, R.E. Tuckett RE, S.R. Yadav and P.J. Rudall. (2011). Unique stigmatic hairs and pollen-tube growth within the stigmatic cell wall in the early-divergent angiosperm family Hydatellaceae. Annals of Botany 108: 599–608.
10. Rudall P.J., M.V. Remizowa, A. Beer, E. Bradshaw, D.W. Stevenson, T.D. Macfarlane, R.E. Tuckett, S.R. Yadav, D.D. Sokoloff. (2008). Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Annals of Botany 101: 941–956.
11. Rudall P.J., T. Eldridge, J. Tratt, S.Y. Smith, M.M. Ramsay, R.E. Tuckett, M.E. Collinson, M.V. Remizowa and D.D. Sokoloff. (2009). Seed fertilization, development and germination in Hydatellaceae (Nymphaeales): implications for endosperm evolution in early angiosperms. American Journal of Botany 96: 1581–1593.
12. Tuckett R.E., D.J. Merritt, P.J. Rudall, F. Hay, S.D. Hopper, C.C. Baskin, J.M. Baskin, J. Tratt and K.W. Dixon. (2010). A new type of specialised morphophysiological dormancy and seed storage behaviour in Hydatellaceae, an early-divergent angiosperm family. Annals of Botany 105: 1053–1061.
13. Sokoloff D.D., M.V. Remizowa, T.D. Macfarlane, J.G. Conran, S.R. Yadav and P.J. Rudall. (2013a). Comparative fruit structure in Hydatellaceae (Nymphaeales) reveals specialized pericarp dehiscence in some early-divergent angiosperms with ascidiate carpels. Taxon 62: 40–61.
14. Sokoloff D.D., M.V. Remizowa, T.D. Macfarlane, R.E. Tuckett, M.M. Ramsay, A.S. Beer, S.R. Yadav and P.J. Rudall. (2008). Seedling diversity in Hydatellaceae: implications for the evolution of angiosperm cotyledons. Annals of Botany 101:153–164.
15. Sokoloff D.D., M.V. Remizowa, A.S. Beer, S.R. Yadav, T.D. Macfarlane, M.M. Ramsay and P.J. Rudall. (2013b). Impact of spatial constraints during seed germination on the evolution of angiosperm cotyledons: a case study from tropical Hydatellaceae (Nymphaeales). American Journal of Botany 100: 824–843.