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

Stabilization and variation of floral structures are indispensable for plant reproduction and evolution; however, the developmental mechanism regulating their structural robustness is largely unknown. To investigate this mechanism, we examined positional arrangement (aestivation) of excessively produced perianth organs (tepals) of six- and seven-tepaled (lobed) flowers in six Anemone species (Ranunculaceae). We found that the tepal arrangement that occurred in nature varied intraspecifically between spiral and whorled arrangements. Moreover, among the studied species, variation was commonly limited to three types, including whorls, despite five geometrically possible arrangements in six-tepaled flowers and two types among six possibilities in seven-tepaled flowers. A spiral arrangement, on the other hand, was unique to five-tepaled flowers. A spiral phyllotaxis model with stochasticity on initiating excessive primordia accounted for these limited variations in arrangement in cases when the divergence angle between preexisting primordia was less than 144°. Moreover, interspecific differences in the frequency of the observed arrangements were explained by the change of model parameters that represent meristematic growth and differential organ growth. These findings suggest that the phyllotaxis parameters are responsible for not only intraspecific stability but interspecific difference of floral structure. Decreasing arrangements from six-tepaled to seven-tepaled Anemone flowers demonstrate that the stabilization occurs as development proceeds to increase the component (organ) number, in contrast from the intuition that the variation will be larger due to increasing number of possible states (arrangements).