Development of reproductive structures in the sole Indian species of Hydatellaceae, Trithuria konkanensis, and its morphological differences from Australian taxa
Dmitry D. Sokoloff A , Margarita V. Remizowa A , Shrirang R. Yadav B and Paula J. Rudall C DA Department of Higher Plants, Biological Faculty, Moscow State University, 119991 Moscow, Russia.
B Shivaji University, Vidyanagar, Kolhapur 416 004, India.
C Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK.
D Corresponding author. Email: p.rudall@kew.org
Australian Systematic Botany 23(4) 217-228 https://doi.org/10.1071/SB10015
Submitted: 30 March 2010 Accepted: 21 May 2010 Published: 31 August 2010
Abstract
The current paper presents new morphological and developmental data on the sole Indian species of Hydatellaceae, T. konkanensis Yadav & Janarthanam, and explores its morphological differences from Australian members of the family. On the basis of morphology and ecology, T. konkanensis appears to be closely related to T. lanterna, a species from tropical northern Australia that resembles T. konkanensis more closely than does any other Australian taxon. However, fruits are dehiscent in T. lanterna and indehiscent in T. konkanensis. Developmental data on T. konkanensis are significant for interpreting the reproductive units in Hydatellaceae. In T. konkanensis, each reproductive unit consists of two bract-like phyllomes, several carpels and a single central stamen that is initiated before the carpels. The earliest-formed carpels are those closest to the stamen; the latest-formed carpels are closest to the phyllomes. Despite their apparently whorled arrangement, the phyllomes are initiated sequentially. The spatial arrangement of the earliest-initiated carpels makes it unlikely that the phyllomes subtend any axillary structures. So far, there is no robust direct evidence in favour of a multiaxial (pseudanthial) morphological interpretation of bisexual reproductive units of Hydatellaceae. No evidence for dichogamy is present in bisexual reproductive units of either Indian or Australian Hydatellaceae, a feature that contrasts with the common presence of protogyny in flowers of other early divergent extant angiosperms.
Additional keywords: flower, fruit, homology, Hydatellaceae, inflorescence, morphology, Nymphaeales, seed.
Acknowledgements
We are grateful to Richard Bateman, Terry Macfarlane and two anonymous reviewers for helpful discussion and comments. M. V. R. and D. D. S. acknowledge support from the President of Russia grant no. MD-2644.2009.4, RFBR grant no. 09-04-01155 and the Ministry of Education and Science of Russia.
Ambrose BA,
Espinosa-Matías S,
Vázquez-Santana S,
Vergara-Silva F,
Martínez E,
Márquez-Guzmán J, Alvarez-Buylla ER
(2006) Comparative floral developmental series of the Mexican triurids support a euanthial interpretation for the unusual floral structures of Lacandonia schismatica (Lacandoniaceae). American Journal of Botany 93, 15–35.
| Crossref | GoogleScholarGoogle Scholar |
[verified May 2010].
Joshi VC, Janarthanam MK
(2004) The diversity of life-form type, habitat preference and phenology of the endemics in the Goa region of the Western Ghats, India. Journal of Biogeography 31, 1227–1237.
| Crossref | GoogleScholarGoogle Scholar |
Meeuse ADJ
(1972) Sixty-five years of theories of the multiaxial flower. Acta Biotheoretica 21, 167–202.
| Crossref | GoogleScholarGoogle Scholar |
Remizowa MV,
Sokoloff DD,
Macfarlane TD,
Yadav SR,
Prychid CJ, Rudall PJ
(2008) Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific level. Grana 47, 81–100.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ
(2008) Fascicles and filamentous structures: comparative ontogeny of morphological novelties in Triuridaceae. International Journal of Plant Sciences 169, 1023–1037.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ, Bateman RM
(2006) Morphological phylogenetic analysis of Pandanales: testing contrasting hypotheses of floral evolution. Systematic Botany 31, 223–238.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ, Bateman RM
(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.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ,
Sokoloff DD,
Remizowa MV,
Conran JG,
Davis JI,
Macfarlane TD, Stevenson DW
(2007) Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early-divergent angiosperm lineage. American Journal of Botany 94, 1073–1092.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ,
Remizowa MV,
Beer AS,
Bradshaw E,
Stevenson DW,
Macfarlane TD,
Tuckett RE,
Yadav SR, Sokoloff DD
(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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rudall PJ,
Eldridge T,
Tratt J,
Ramsay MM,
Tuckett RE,
Smith SY,
Collinson ME,
Remizowa MV, Sokoloff DD
(2009a) Seed fertilization, development, and germination in Hydatellaceae (Nymphaeales): implications for endosperm evolution in early angiosperms. American Journal of Botany 96, 1581–1593.
| Crossref | GoogleScholarGoogle Scholar |
Rudall PJ,
Remizowa MV,
Prenner G,
Prychid CJ,
Tuckett RE, Sokoloff DD
(2009b) Nonflowers 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.
| Crossref | GoogleScholarGoogle Scholar |
Saarela JM,
Rai HS,
Doyle JA,
Endress PK,
Mathews S,
Marchant AD,
Briggs BG, Graham SW
(2007) Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446, 312–315.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sokoloff DD, Timonin AC
(2007) Morphological and molecular data on the origin of angiosperms: on a way to a synthesis. Journal of General Biology 68, 83–97.
| PubMed |
Sokoloff DD,
Remizowa MV,
Macfarlane TD, Rudall PJ
(2008a) 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.
| Crossref | GoogleScholarGoogle Scholar |
Sokoloff DD,
Remizowa MV,
Macfarlane TD,
Tuckett RE,
Ramsay MM,
Beer AS,
Yadav SR, Rudall PJ
(2008b) Seedling diversity in Hydatellaceae: implications for the evolution of angiosperm cotyledons. Annals of Botany 101, 153–164.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sokoloff DD,
Remizowa MV,
Briggs BG, Rudall PJ
(2009a) Shoot architecture and branching pattern in perennial Hydatellaceae. International Journal of Plant Sciences 170, 869–884.
| Crossref | GoogleScholarGoogle Scholar |
Sokoloff DD,
Remizowa MV,
Linder HP, Rudall PJ
(2009b) Morphology and development of the gynoecium in Centrolepidaceae: the most remarkable range of variation in Poales. American Journal of Botany 96, 1925–1940.
| Crossref | GoogleScholarGoogle Scholar |
Tillich HJ,
Tuckett RE, Facher E
(2007) Do Hydatellaceae belong to the monocotyledons or basal angiosperms? Evidence from seedling morphology. Willdenowia 37, 399–406.
| Crossref | GoogleScholarGoogle Scholar |
Tratt J,
Prychid CJ,
Behnke H-D, Rudall PJ
(2009) Starch-accumulating (S-type) sieve-element plastids in Hydatellaceae: implications for plastid evolution in flowering plants. Protoplasma 237, 19–26.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yadav SR, Janarthanam MK
(1994) Hydatellaceae: a new family to Indian flora with a new species. Rheedea 4, 17–20.
Yadav SR, Janarthanam MK
(1995)
Trithuria konkanensis (Hydatellaceae), eine neue Art aus Indien. Aqua-Planta 3, 91–97.
Appendix 1
Identification key of Trithuria species with bisexual reproductive units
1. Fruits lacking longitudinal ribs. Fruit surface with dense and well recognisable papillae ..........T. cowieana (N Australia)
Fruits with three longitudinal ribs. Fruit surface lacking papillae ..........2
2. Seeds smooth, covered by firm cuticle. Seedlings lacking a cotyledonary sheath, with cotyledon represented by a haustorium only ..........3
Mature seeds clearly sculptured, honeycombed when dry, with individual exotesta cells well recognisable from the surface. Seedlings possessing a bilobed cotyledonary sheath to which a haustorium is attached ..........4
3. Fruits indehiscent. Reproductive units always possessing two bract-like phyllomes. Longest stigmatic hairs longer than 3 mm ..........T. konkanensis (India)
Dry mature fruits dehiscing by separating three longitudinal ribs. Reproductive units possessing 2–4 bract-like phyllomes. Longest stigmatic hairs usually not exceeding 3 mm ..........T. lanterna (N Australia)
4. Reproductive units typically possessing four (rarely three or up to seven, very rarely two) acute or apiculate bract-like phyllomes. Reproductive units typically borne on distinct, often long peduncles. (Less frequently, reproductive units almost sessile, but such plants were not collected from Western Australia, where the next species occurs.) ..........T. submersa (SW, S and SE Australia, Tasmania)
Reproductive units possessing two (very rarely four) acuminate bract-like phyllomes. Reproductive units virtually sessile (or very rarely possessing long peduncles) ..........T. bibracteata (SW Australia)