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

Abstract

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).Electronic supplementary materialThe online version of this article (10.1007/s10265-018-1025-x) contains supplementary material, which is available to authorized users.

Perianth Phyllotaxis Is Polymorphic in the Basal Eudicot Anemone and Eranthis Species

“…In line with a previous report (Kitazawa and Fujimoto, 2018), we confirmed that the aestivations of 5-to 7-lobed flowers were constrained to several types including the trimerous double-whorl and the spirals, despite considerable intraspecific variation of tepal numbers in Anemone species ( Supplementary Table 2) (Yule, 1902;Fujimoto, 2014, 2016a), even when there was a two-fold increase in the sample size ( Figures 2B-D, Supplementary Table 1). Therefore, we explored the constrained coexistence of whorled and spiral flowers in populations with more than 7 and <5 tepals, in four Anemone and one Eranthis species (sections Positional Arrangement of Perianth Organs and Plant Samples).…”

“…× hybrida W, and A. hepatica, and second for A. × hybrida PP and E. pinnatifida (EAIEIA and EAIAEI ranked first, respectively, for the last two species; Figure 2C), in line with the results of a previous report (Kitazawa and Fujimoto, 2018). In addition, in several populations, the 6-tepaled aestivation exhibited a reproducible difference from the above-mentioned average of total populations.…”

Developmental Flower and Rhizome Morphology in Nuphar (Nymphaeales): An Interplay of Chaos and Stability

“…Another character is the order of organ initiation. A third character (Kitazawa and Fujimoto, 2018;Fujimoto and Kitazawa, 2020) is the pattern of overlapping between margins of adjacent organs (aestivation). Quincuncial aestivation normally correlates with sequential sepal initiation in angiosperms.…”

Mathematical model studies of the comprehensive generation of major and minor phyllotactic patterns in plants with a predominant focus on orixate phyllotaxis

“…Smith et al assumed in their mathematical model that the inhibitory power of each primordium decays exponentially with age and stated that this decay promoted phyllotactic pattern formation de novo, as well as pattern transition, and allowed the maintenance of patterns for wider ranges of parameters [9]. A DC1-based model equipped with a primordial age-dependent change in the inhibitory power was also used to investigate floral organ arrangement [35, 36]. In these studies, however, temporal changes in the inhibitory power were examined under limited ranges of parameters focusing on particular aspects of phyllotactic patterning, and the possibility of the generation of minor patterns, such as orixate phyllotaxis, was not addressed.…”