Botanica Pacifica. A journal of plant science and conservation 2023. 12(2):3-14
Article first published online: 11 JUN 2023 | DOI: 10.17581/bp.2023.12s01
When asymmetry mimics zygomorphy: flower development in Chamaelirium japonicum (Melanthiaceae, Liliales)
Margarita V. Remizowa 1
,
Alexey B. Shipunov 2† &
Dmitry D. Sokoloff 1 1 Lomonosov Moscow State University, Moscow, Russia
2 Kyoto University, University Museum, Kyoto, Japan
† - deceased
Pendent sessile flowers of Chamaelirium japonicum (Willd.) N. Tanaka appear zygomorpic, but they do not possess a bilateral symmetry. The flowers are subtended by a vestigial bract and lack a bracteole. The perianth consists of two small tepals on the abaxial side of the flower and four large tepals, none of which is median. Because the short tepals belong to different whorls, there is no symmetry plane. Despite the absence of a bracteole, the shape of the floral meristem before perianth inception resembles that of bracteolate monocot flowers. At early stages, all six tepals are equal in shape and size, and the flower is actinomorphic. The difference between the dorsal and ventral sides and the pendent nature of the flower become expressed during the gynoecium development. The absence of median organs allows to avoid collision of floral organs with the flower-subtending bract during flower curvature. Species of Chamaelirium reveal a set of different flower groundplans, which makes the genus a perfect model to investigate evolutionary changes in flower symmetry accompanied by differential tepal reduction.
Ремизова М.В., Шипунов А.Б., Соколов Д.Д. Асимметрия имитирует зигоморфию: развитие цветка у Chamaelirium japonicum (Melanthiaceae, Liliales). Поникшие сидячие цветки Chamaelirium japonicum (Willd.) N. Tanaka выглядят как зигоморфные, но в отличие от типичных зигоморфных цветков не имеют билатеральной симметрии. Цветки с почти неразличимой брактеей, но без брактеолы. Околоцветник состоит из двух маленьких и четырех крупных листочков околоцветника, ни один из которых не расположен медианно. Так как маленькие листочки околоцветника принадлежат разным кругам, через цветок невозможно провести плоскость симметрии. Несмотря на отсутствие брактеолы флоральная меристема перед заложением околоцветника имеет треугольную форму, как это характерно для цветков однодольных растений с брактеолой. На ранних стадиях развития все шесть листочков околоцветника одинаковы по форме и размерам, цветки актиноморфные. Различия в размере верхних и нижних листочков околоцветника и поникание цветка начинают проявляться во время заложения гинецея. Отсутствие органов в медианной плоскости позволяет облегчить поникание цветка и избежать их наложения на брактею. Цветки представителей Chamaelirium весьма разнообразны, что делает этот небольшой род прекрасным объектом для изучения смены типа симметрии цветка, сопровождающегося редукцией листочков околоцветника.
Keywords: Chamaelirium, flower development, asymmetry, zygomorphy, flower symmetry, tepal reduction, развитие цветка, асимметрия, зигоморфия, симметрия цветка, редукция листочков околоцветника
References
Averyanov, L.V. & N. Tanaka. 2014. New species of Chionographis (Melanthiaceae) from eastern Indochina. Taiwania 59:13-17.
Bukhari, G., J. Zhang, P.F. Stevens & W. Zhang. 2017. Evolution of the process underlying floral zygomorphy development in pentapetalous angiosperms. American Journal of Botany 104:1846-1856. CrossRef
Bull-Hereñu, K., P. dos Santos, J.F.G. Toni, J.H.L. El Ottra, P. Thaowetsuwan, J. Jeiter, L.P. Ronse De Craene & A. Iwamoto. 2022. Mechanical forces in floral development. Plants 11:661. CrossRef
Citerne, H., F. Jabbour, S. Nadot & C. Damerval. 2010. The evolution of floral symmetry. Advances in Botanical Research 54:85-137. CrossRef
Claßen-Bockhoff, R. 2016. The shoot concept of the flower: Still up to date? Flora 221:46-53. CrossRef
Claßen-Bockhoff, R. & K. Bull-Hereñu. 2013. Towards an ontogenetic understanding of inflorescence diversity. Annals of Botany 112:1523-1542. CrossRef
Cubas, P. 2004. Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:1175-1184. CrossRef
Dahlgren R.M.T., H.T. Clifford & P.F. Yeo. 1985. The families of the Monocotyledons: Structure, evolution, and taxonomy. Springer Science & Business Media, Berlin, 531 pp. CrossRef
Eichler, A.W. 1875. Blüthendiagramme. Engelmann, Leipzig, 357 ss.
Endress, P.K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge, 530 pp.
Endress, P.K. 1995. Major evolutionary traits of monocot flowers. In: Monocotyledons: Systematics and evolution (P.J. Rudall, P.J. Cribb, D.F. Cutler & C.J. Humphries, eds), pp. 43-79, Royal Botanic Gardens, Kew, London.
Endress, P.K. 1999. Symmetry in flowers: diversity and evolution. International Journal of Plant Sciences 160: S3-S23. CrossRef
Endress, P.K. 2001. Evolution of floral symmetry. Current Opinion in Plant Biology 4:86-91. CrossRef
Endress, P.K. 2006. Angiosperm floral evolution: morphological developmental framework. Advances in Botanical Research 44: 1-61. CrossRef
Endress, P.K. 2008. The Whole and the Parts: relationships between floral architecture and floral organ shape, and their repercussions on the interpretation of fragmentary floral fossils. Annals of the Missouri Botanical Garden 95:101-120. CrossRef
Endress, P.K. 2011. Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98:370-396. CrossRef
Endress, P.K. 2012. The immense diversity of floral monosymmetry and asymmetry across angiosperms. The Botanical Review 78: 345-397. CrossRef
Engler, A. 1888. Liliaceae. In: Die Natürlichen Planzenfamilien. II, 5, (A. Engler, K. Prantl, eds.), ss. 10-91, Engelmann, Leipzig.
Leins, P. & C. Erbar. 2010. Flower and fruit. Morphology, ontogeny, phylogeny, function and ecology. Schweizerbart science publishers, Stuttgart, 439 pp.
Hoshino, Y., T. Igarashi, M. Ohshima, K. Shinoda, N. Murata, A. Kanno & M. Nakano. 2014. Characterization of CYCLOIDEA-like genes in controlling floral zygomorphy in the monocotyledon Alstroemeria. Scientia Horticulturae 169:6-13. CrossRef
Huang, Y.-F., R.-H. Jiang, D.-X. Nong & W.-B. Xu. 2011. Chionographis shiwandashanensis sp. nov. (Melanthiaceae) from southern Guangxi, China. Nordic Journal of Botany 29:605-607. CrossRef
Jabbour, F., S. Nadot & C. Damerval. 2009. Evolution of floral symmetry: a state of the art. Comptes Rendus Biologies 332:219-231. CrossRef
Liu, Z.-C., L. Feng, L. Wang & W.-B. Liao. 2018. Chamaelirium viridiflorum (Melanthiaceae), a new species from Jiangxi, China. Phytotaxa 357:126-132. CrossRef
Maki, M. 1993a. Floral sex ratio variation in hermaphrodites of gynodioecious Chionographis japonica var. kurohimensis Ajima et Satomi (Liliaceae). Journal of Plant Research 106:181-186. CrossRef
Maki, M. 1993b. Outcrossing and fecundity advantage of females in gynodioecious Chionographis japonica var. kurohimensis (Liliaceae). American Journal of Botany 80:629-634. CrossRef
Maki, M. 1996. Differences in plant size and flower production between hermaphrodites and females of two gynodioecious Chionographis (Liliaceae). Canadian Journal of Botany 74:150-153. CrossRef
Maki, M. & M. Masuda. 1994. Spatial genetic structure within two populations of a self-incompatible perennial Chionographis japonica var. japonica (Liliaceae). Journal of Plant Research 107:283-287. CrossRef
Neal, P.R., A. Dafni & M. Giurfa. 1998. Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annual Review of Ecology and Systematics 29(1):345-373. CrossRef
Neinhuis, C. & P.L. Ibisch. 1998. Corsiaceae. In: The families and genera of vascular plants. Monocotyledons: Lilianae (except Orchidaceae) (K. Kubitzki, ed.), pp. 198-201, Springer, Berlin, Heidelberg. CrossRef
Preston, J.C. & L.C. Hileman 2009. Developmental genetics of floral symmetry evolution. Trends in Plant Science 14:147-154. CrossRef
Qin, Y., F. Tan, Y. S. Huang & Y. Liu. 2023. Chamaelirium jiuwanshanense (Melanthiaceae), a new dioecious species from Guangxi, China. Taiwania 68:97-100.
Remizowa, M.V., P.J. Rudall, V.V. Choob & D.D. Sokoloff 2013a. Racemose inflorescences of monocots: structural and morphogenetic interaction at the flower/inflorescence level. Annals of Botany 112:1553-1566. CrossRef
Remizowa, M.V., D.D. Sokoloff & P.J. Rudall 2013b. Patterns of bract reduction in racemose inflorescences of early-divergent monocots. In: Early events in monocot evolution (P. Wilkin & S.J. Mayo, eds), pp. 185-207. Cambridge University Press, Cambridge. CrossRef
Remizowa, M., D. Sokoloff & P. Rudall 2006. Patterns of floral structure and orientation in Japonolirion, Narthecium, and Tofieldia. Aliso 22: 159-171. CrossRef
Reyes, E., H. Sauquet & S. Nadot 2016. Perianth symmetry changed at least 199 times in angiosperm evolution. Taxon 65:945-964. CrossRef
Ronse De Craene, L.P. 2010. Floral diagrams. An aid to understanding flower morphology and evolution. Cambridge University Press, Cambridge, 441 pp. CrossRef
Ronse De Craene, L. 2018. Understanding the role of floral development in the evolution of angiosperm flowers: clarifications from a historical and physico-dynamic perspective. Journal of Plant Research 131:367-393. CrossRef
Ronse De Craene, L.P. 2022. Floral diagrams. An aid to understanding flower morphology and evolution. Second edition. Cambridge University Press, Cambridge, 534 pp. CrossRef
Rudall, P.J. & R.M. Bateman 2004. Evolution of zygomorphy in monocot flowers: iterative patterns and developmental constraints. New Phytologist 162:25-44. CrossRef
Rudall, P.J. & A. Eastman. 2002. The questionable affinities of Corsia (Corsiaceae): evidence from floral anatomy and pollen morphology. Botanical Journal of the Linnean Society 138:315-324. CrossRef
Sokoloff, D.D., G.V. Degtjareva, P.K. Endress, M.V. Remizowa, T.H. Samigullin & C.M. Valiejo-Roman 2007. Inflorescence and early flower development in Loteae (Leguminosae) in a phylogenetic and taxonomic context. International Journal of Plant Sciences 168:801-833. CrossRef
Takhtajan, A. 2009. Flowering plants. Springer Science & Business Media, New York, 906 pp. CrossRef
Tamura, M.N. 1998. Melanthiaceae. In: The families and genera of vascular plants. Monocotyledons: Lilianae (except Orchidaceae) (K. Kubitzki, ed.), pp. 369-380, Springer, Berlin, Heidelberg. CrossRef
Tanaka, N. 2003. New status and combinations for Japanese taxa of Chionographis (Melanthiaceae). Novon 13:212-215. CrossRef
Tanaka, N. 2013. A new species of Chionographis (Melanthiaceae) from Japan. Journal of Japanese Botany 88:30-35.
Tanaka, N. 2017a. A synopsis of the genus Chamaelirium (Melanthiaceae) with a new infrageneric classification including Chionographis. Taiwania 62:157-167.
Tanaka, N. 2017b. Diversity in fruit and seed characters of Chamaelirium and Chionographis (Melanthiaceae). Taiwania 62:67-74.
Tong, Y., Y. Li, G. Guo, K. Dai, Y. Zeng & C. He. 2020. Chamaelirium shimentaiense (Melanthiaceae), a new species from Guangdong, China. Nordic Journal of Botany 38:e02634. CrossRef
Tucker, S.C. 1975. Floral development in Saururus cernuus (Saururaceae): 1. Floral initiation and stamen development. American Journal of Botany 62: 993-1007. CrossRef
Tucker, S.C. 1981. Inflorescence and floral development in Houttuynia cordata (Saururaceae). American Journal of Botany 68:1017-1032. CrossRef
Walch, J.-P. & S. Blaise. 2022. Mathematical modeling the influence of bracteoles on sepal arrangement. Flora 295:e152138. CrossRef
Westerkamp, C. & R. Claßen-Bockhoff. 2007. Bilabiate flowers: the ultimate response to bees? Annals of Botany 100: 361-374. CrossRef
Wu, L., Y. Tong, R.-Y. Yan & Q.-R. Liu. 2016. Chionographis nanlingensis (Melanthiaceae), a new species from China. Pakistan Journal of Botany 48:601-606.
|
|