Journal of Ecology and Environment

The Ecological Society of Korea (한국생태학회)
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A rare duodichogamous flowering system in monoecious Toona sinensis (Meliaceae)

  • Lee, Hakbong (Department of Biology, Sungshin University) ;
  • Kang, Hyesoon (Department of Biology, Sungshin University) ;
  • Park, Wan-Geun (Department of Forest Resources, College of Forest and Environmental Sciences, Kangwon National University)
  • Received : 2018.01.29
  • Accepted : 2018.03.23
  • Published : 2018.04.30
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Abstract

Background: Duodichogamy is the rarest form of dichogamy in angiosperms, which is characterized by flowering in the sequence of male${\rightarrow}$female${\rightarrow}$male. Disentangling factors promoting duodichogamy require the discovery of more duodichogamous species in angiosperms. However, extremely limited information on duodichogamous species makes it difficult to make general conclusions. Given the inflorescence morphology and flowering characteristics, the Meliaceae family is highly likely to contain duodichogamous species. Methods: We selected 48 individuals from 20 populations in Korea and investigated their flower morphology, arrangement of flowers by sexual condition within inflorescences, and flowering phases and duration of male and female flowers of Toona sinensis (Meliaceae) for 5 years (2011-2015) to determine if the species shows duodichogamous flowering. Results: Toona sinensis belonging to Meliaceae possessed functionally unisexual flowers with rudimentary parts of the opposite sex. The floral organs in male were larger than those in female, except for ovary length and width. In dichasium, male flowers were observed on primary or lateral branches, whereas female flowers were borne only on lateral branches. Overall, individuals from six different populations flowered in the male${\rightarrow}$female${\rightarrow}$male sequence, thereby male is blooming far longer than female flowers at the level of individual trees (male vs. female = 17-20 days vs. 2-4 days). Conclusions: This is the first study to report a duodichogamously flowering species, T. sinensis, within Meliaceae. Several flowering characteristics observed from T. sinensis may be important clues used to discover additional duodichogamous Meliaceae species. Short flowering period and relatively small number of female flowers, which is analogous to reduced ovule numbers observed in other duodichogamous species, may intensify male-male competition in T. sinensis. This study contributed to narrowing down potential candidates of duodichogamy based on their geographic distributions and flowering time.

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References

  1. Acevedo-Rodriguez, P. (1993). Systematics of Serjania (Sapindaceae) part 1: A revision of Serjania sect. Platycoccus. Memoirs of the New York Botanical Garden, 67, 1-93.
  2. Acevedo-Rodriguez, P. (2003). Melicocceae (Sapindaceae): Melicoccus and Talisia. In Flora Neotropica Monograph 87. New York: The New York Botanical Garden.
  3. Bahadur, K. N. (1987). Monograph on the genus Toona (Meliaceae). Dehra Dun: M/s Bishen Singh.
  4. Barrett, S. C. H. (2002). Sexual interference of the floral kind. Heredity, 88, 154-159. https://doi.org/10.1038/sj.hdy.6800020
  5. Bawa, K. S. (1977). The reproductive biology of Cupania guatemalensis Radlk. (Sapindaceae). Evolution, 31, 52-63. https://doi.org/10.1111/j.1558-5646.1977.tb00981.x
  6. Bawa, K. S., & Beach, J. H. (1981). Evolution of sexual systems in flowering plants. Annals of the Missouri Botanical Garden, 68, 254-274. https://doi.org/10.2307/2398798
  7. Borges, R. M., Somnathan, H., & Mali, S. (1997). Alternations of sexes in a deciduous tree: Temporal dioecy in Bridelia retusa. Current Science, 72, 940- 944.
  8. Christenhusz, M. J. M., & Byng, J. W. (2016). The number of known plants species in the world and its annual increase. Phytotaxa, 261, 201-217. https://doi.org/10.11646/phytotaxa.261.3.1
  9. Cruden, R. W. (1988). Temporal dioecism: Systematic breadth, associated traits, and temporal patterns. Botanical Gazette, 149, 1-15. https://doi.org/10.1086/337684
  10. de Jong, P. C. (1976). Flowering and sex expression in Acer L.: A biosynthetic study. Meded. Landbouwhogeschool Wageningen, 76, 1-201.
  11. de Lima, H. A., Somner, G. V., & Giulietti, A. M. (2016). Duodichogamy and sex lability in Sapindaceae: The case of Paullinia weinmanniifolia. Plant Systematics and Evolution, 302, 109-120. https://doi.org/10.1007/s00606-015-1247-5
  12. Edmonds, J. M. (1993). The potential value of Toona species (Meliaceae) as multipurpose and plantation trees in Southeast Asia. The Commonwealth Forestry Review, 72, 181-186.
  13. Edmonds, J. M., & Staniforth, M. (1998). Plate 348. Toona sinensis. Curtis's Botanical Magazine, 15, 186-193. https://doi.org/10.1111/1467-8748.00169
  14. eFloras. (2017). Missouri Botanical Garden, St. Louis, MO and Harvard University Herbaria, Cambridge, MA. Available from http://www.efloras.org. Accessed 12 March 2017.
  15. Godley, E. J. (1955). Monoecy and incompatibility. Nature, 176, 1176-1177.
  16. Gouvea, C. F., Dornelas, M. C., & Rodriguez, A. P. M. (2008). Floral development in the tribe Cedreleae (Meliaceae, Sub-family Swietenioideae): Cedrela and Toona. Annals of Botany, 101, 39-48.
  17. Hagman, M. (1975). Incompatibility in forest trees. Proceedings of the Royal Society B-Biological Sciences, 188, 313-326. https://doi.org/10.1098/rspb.1975.0022
  18. Harder, L. D., Barrett, S. C. H., & Cole, W. W. (2000). The mating consequences of sexual segregation within inflorescences of flowering plants. Proceedings of the Royal Society B-Biological Sciences, 267, 315-320. https://doi.org/10.1098/rspb.2000.1002
  19. Jaynes, R. A. (1975). Chestnuts. In J. Janick & J. Moore (Eds.), Advances in fruit breeding (pp. 490-503). West Lafayette: Purdue University Press.
  20. Khan, K. S. (1929). Pollination and fruit formation in litchi (Nephelium litchi, Camb). The Agricultural Journal of India, 24, 183-187.
  21. Kjohl, M., Nielsen, A., & Stenseth, N. C. (2011). Potential effects of climate change on crop pollination. Rome: Food and Agriculture Organization of the United Nations (FAO).
  22. Lamb, F. B. (1960). An approach to mahogany tree improvement. Caribbean Forester, 21, 12-20.
  23. Li, Y., Luo, S., & Zhang, D. (2014). Fly pollination and duodichogamy in Bridelia stipularis and Cleistanthus sumatranus (Phyllanthaceae). Plant Species Biology, 29, 85-92. https://doi.org/10.1111/j.1442-1984.2012.00390.x
  24. Lloyd, D. G., & Webb, C. J. (1986). The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. New Zealand Journal of Botany, 24, 135-162. https://doi.org/10.1080/0028825X.1986.10409725
  25. Luo, S., Zhang, D., & Renner, S. S. (2007). Duodichogamy and androdioecy in the Chinese Phyllanthaceae Bridelia tomentosa. American Journal of Botany, 94, 260-265. https://doi.org/10.3732/ajb.94.2.260
  26. Muellner, A. N., Pennington, T. D., & Chase, M. W. (2009). Molecular phylogenetics of Neotropical Cedreleae (mahogany family, Meliaceae) based on nuclear and plastid DNA sequences reveal multiple origins of "Cedrela odorata". Molecular Phylogenetics and Evolution, 52, 461-469. https://doi.org/10.1016/j.ympev.2009.03.025
  27. Pennington, T. D., & Muellner, A. N. (2010). A monograph of Cedrela (Meliaceae). Milborne Port: DH Books.
  28. Pennington, T. D., & Styles, B. T. (1975). A generic monograph of the Meliaceae. Blumea, 22, 419-540.
  29. Pramono, A. A., Palupi, E. R., Siregar, I. Z., & Kusmana, C. (2016). Characteristics of Surian flower, fruit and seed productions (Toona sinensis (A. Juss.) M. Roem.) in Sumedang, West Java. Tropical Life Sciences Research, 27, 77-91.
  30. Renner, S. S. (2014). The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany, 101, 1588-1596. https://doi.org/10.3732/ajb.1400196
  31. Routley, M. B., & Husband, B. C. (2003). The effect of protandry on siring success in Chamerion angustifolium (Onagraceae) with different inflorescence sizes. Evolution, 57, 240-248. https://doi.org/10.1111/j.0014-3820.2003.tb00259.x
  32. Sargent, R. D., Mandegar, M. A., & Otto, S. P. (2006). A model of the evolution of dichogamy incorporating sex-ratio selection, anther-stigma interference, and inbreeding depression. Evolution, 60, 934-944. https://doi.org/10.1111/j.0014-3820.2006.tb01172.x
  33. Snyder, J. M., & Richards, J. H. (2005). Floral phenology and compatibility of sawgrass, Cladium jamaicense (Cyperaceae). American Journal of Botany, 92, 736-743. https://doi.org/10.3732/ajb.92.4.736
  34. Stout, A. B. (1928). Dichogamy in flowering plants. Bulletin of the Torrey Botanical Club, 55, 141-153. https://doi.org/10.2307/2480605
  35. Styles, B. T. (1972). The flower biology of the Meliaceae and its bearing on tree breeding. Silvae Genetica, 21, 175-182.
  36. Subba Reddi, C., Reddi, E. U. B., Reddi, N. S., & Reddi, P. S. (1983). Reproductive ecology of Sapindus emarginatus Vahl. (Sapindaceae). Proceedings of the Indian National Science Academy, 49, 57-72.
  37. The Angiosperm Phylogeny Group. (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1-20. https://doi.org/10.1111/boj.12385
  38. The Tree of Sex Consortium. (2014). Tree of sex: a database of sexual systems. Available from https://doi.org/10.5061/dryad.v1908. Accessed 11 August 2017.
  39. Troup, R. S. (1921). The silviculture of Indian trees (Vol. 1). Oxford: Clarendon Press.
  40. Weberling, F. (1992). Morphology of flowers and inflorescences. Cambridge: Cambridge University Press.
  41. Wyatt, R. (1983). Pollinator-plant interactions and the evolution of breeding systems. In L. Real (Ed.), Pollination biology (pp. 51-95). New York: Academic Press.
  42. Zapata, T. R., & Arroyo, M. T. K. (1978). Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica, 10, 221-230. https://doi.org/10.2307/2387907

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