Developmental stochasticity and variation in floral phyllotaxis

Floral phyllotaxis is a relatively robust phenotype; trimerous and pentamerous arrangements are widely observed in monocots and core eudicots. Conversely, it also shows variability in some angiosperm clades such as 'ANA' grade (Amborellales, Nymphaeales, and Austrobaileyales), magnoliids, and Ranunculales. Regardless of the phylogenetic relationship, however, phyllotactic pattern formation appears to be a common process. What are the causes of the variability in floral phyllotaxis and how has the variation of floral phyllotaxis contributed to floral diversity? In this review, I summarize recent progress in studies on two related fields to develop answers to these questions. First, it is known that molecular and cellular stochasticity are inevitably found in biological systems, including plant development. Organisms deal with molecular stochasticity in several ways, such as dampening noise through gene networks or maintaining function through cellular redundancy. Recent studies on molecular and cellular stochasticity suggest that stochasticity is not always detrimental to plants and that it is also essential in development. Second, studies on vegetative and inflorescence phyllotaxis have shown that plants often exhibit variability and flexibility in phenotypes. Three types of phyllotaxis variations are observed, namely, fluctuation around the mean, transition between regular patterns, and a transient irregular organ arrangement called permutation. Computer models have demonstrated that stochasticity in the phyllotactic pattern formation plays a role in pattern transitions and irregularities. Variations are also found in the number and positioning of floral organs, although it is not known whether such variations provide any functional advantages. Two ways of diversification may be involved in angiosperm floral evolution: precise regulation of organ position and identity that leads to further specialization of organs and organ redundancy that leads to flexibility in floral phyllotaxis.