Stochastic occurrence of trimery from pentamery in floral phyllotaxis of Anemone (Ranunculaceae)

Abstract

Merosity, indicating the basic number of floral organs such as sepals and petals, has been constrained to specific and stable numbers during the evolution of angiosperms. The ancestral flower is considered to have a spiral arrangement of perianth organs, as in phyllotaxis, the arrangement of leaves. How has the ancestral spiral evolved into flowers with specific merosities? To address this question, we studied perianth organ arrangement in the Anemone genus of the basal eudicot family Ranunculaceae, because various merosities are found in this genus. In three species, A. flaccida, A. scabiosa, and A. nikoensis that are normally pentamerous, we found positional arrangement of the excessive sixth perianth organ indicating the possibility of a transition from pentamerous to trimerous arrangement. Arrangement was intraspecifically stochastic, but constrained to three of five types, where trimerous arrangement was the most frequent in all species except for a form of A. scabiosa. The rank of frequency of the other two types was species-dependent. We connect these observations with classical theories of spiral phyllotaxis. The phyllotaxis model for initiation of the sixth organ showed that the three arrangements occur at a divergence angle <144°, indicating the spiral nature of floral phyllotaxis rather than a perfect penta-radial symmetry of 144°. The model further showed that selective occurrence of trimerous arrangement is mainly regulated by the organ growth rate. Differential organ growth as well as divergence angle may regulate transitions between pentamerous and trimerous flowers in intraspecific variation as well as in species evolution.

Spiral phyllotaxis underlies constrained variation in Anemone (Ranunculaceae) tepal arrangement

“…The arrangement of tepals was examined for flowers with five, six, and seven tepals, whereas the arrangement was not determined for flowers with more than seven tepals. Based on previous studies (Cunnell 1958 ; Kitazawa and Fujimoto 2016b ; Morgan 1874 ; Schoute 1935 ), we surmised the aestivation by positional arrangements of tepals in mature flowers by identifying the arrangement of each organ with neighboring organs as either external, internal, or alternating (Fig. 1 ).…”

“…For six-tepaled flowers derived from quincuncial, there are five aestivation types (Fig. 1 middle row; Kitazawa and Fujimoto 2016b ). Regarding flowers with seven tepals, since the arrangement type 6-II is radially symmetric, the resulting arrangement converge onto only the type 7-II (Fig.…”

“…These species are not separately clustered but rather scattered in the phylogenetic tree (Hoot et al 2012 ). Furthermore, trimerous-like arrangements can be stochastically found even in the species with pentamerous spiral flowers (Kitazawa and Fujimoto 2016b ; Ren et al 2010 ; Schöffel 1932 ). The development of some Anemone flowers indicates a transient pattern between spiral and trimerous whorls: first three tepal primordia arise sequentially, and then three tepal primordia initiate at once (Ren et al 2010 ).…”

“…Previously, we studied the variation in tepal arrangements of flowers with six tepals in wild populations of three Anemone species and found that variation was limited to three aestivation types, including trimerous double whorl type (floral diagram at the left end of middle row in Fig. 1 ), despite the option of five geometrically possible types (Kitazawa and Fujimoto 2016b ). To examine this limited variation associated with the increasing number of tepals, we analyzed the position of the seventh as well as the sixth tepals of Anemone in both wild populations and a floral phyllotaxis model.…”

Phyllotaxis and related topics

“…Entirely different is the chaos observed in acacias, which results from the insertion of additional meristematic structures among primordia already set in a regular phyllotactic pattern. The phenomenon of additive plant organs is analyzed by Kitazawa and Fujimoto [13]. They show how meristic variation in the perianth of the Japanese species of Anemone leads to the formation of different floral phenotypes, a species-specific trait.…”