Developmental stochasticity and variation in floral phyllotaxis

Abstract

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.

Beyond Fibonacci patterns and the golden angle: phyllotactic variations and their cellular origin

“…In particular we highlight patterns "outside" Fibonacci patterns and the evolutionary origins of phyllotaxis. Three review articles discussing general aspects (Yin 2021), stochasticities (Kitazawa 2021), and symmetries (Yonekura and Sugiyama 2021); and three original research articles focusing on pattern regeneration (Zhang et al 2021b), a new system for studying phyllotactic transitions (Zagórska-Marek et al 2021), and the origin of phyllotaxis (Kamamoto et al 2021), are included in this special issue.…”

“…Phyllotaxis is not an exception to such stochasticity. Kitazawa (2021) reviewed the developing fields connecting developmental stochasticity, phenotypic variation, and evolutionary diversification, with an aim to understand the diversity of floral phyllotaxis. Three categories of variation in vegetative and inflorescence phyllotaxis were suggested: fluctuations around the mean divergence angle, transitions between regular patterns, and temporal deviations from regular patterns called permutations.…”