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

Kitazawa, Miho S.; Fujimoto, Koichi

doi:10.3389/fevo.2020.00070

Cited by 8 publications

(6 citation statements)

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“…The appearance of mature flowers and their development can differ, exemplified by rapid spiral initiation in calyx whorls in core eudicot species (Endress and Doyle 2007 ). Mathematical modelling studies have shown that the post-meristematic modification of an organ by repulsive interaction between organs enables concentric arrangement following spiral initiation and stabilizes the organ number in each circle (Kitazawa and Fujimoto 2015 , 2020 ). This result suggests that interaction among organs, which is affected by the determinate nature of flowers and the growth control of each organ, can be crucial to ensure robust organ positioning.…”

Section: Floral Phyllotaxis and Developmentmentioning

confidence: 99%

“…Another perspective, not considered in the approach of Sauquet et al ( 2017 ), is the coexistence of multiple states and the possibility that the ancestral state is polymorphic (Sauquet et al 2018 ). Recently, we reported the coexistence of spirals and whorls in the perianth phyllotaxis at maturity in Anemone and Eranthis (Ranunculaceae) flowers (Kitazawa and Fujimoto 2020 ). Studies on phyllotaxis variations suggest that such variations are common in nature, and variable phenotypes can be generated from a single developmental system, with inevitable existence of stochasticity in biological processes.…”

Section: Floral Evo-devo and Stochasticitymentioning

confidence: 99%

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Developmental stochasticity and variation in floral phyllotaxis

Kitazawa

2021

J Plant Res

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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.

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Section: Floral Phyllotaxis and Developmentmentioning

confidence: 99%

Section: Floral Evo-devo and Stochasticitymentioning

confidence: 99%

Developmental stochasticity and variation in floral phyllotaxis

Kitazawa

2021

J Plant Res

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“…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.…”

Section: Resultsmentioning

confidence: 99%

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

Remizowa

Sokoloff

2020

Front. Cell Dev. Biol.

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European species of Nuphar are among the most accessible members of the basal angiosperm grade, but detailed studies using scanning electron microscopy are lacking. We provide such data and discuss them in the evolutionary context. Dorsiventral monopodial rhizomes of Nuphar bear foliage leaves and non-axillary reproductive units (RUs) arranged in a Fibonacci spiral. The direction of the phyllotaxis spiral is established in seedlings apparently environmentally and maintained through all rhizome branching events. The RUs can be located on dorsal, ventral or lateral side of the rhizome. There is no seasonality in timing of their initiation. The RUs usually form pairs in positions N and N + 2 along the ontogenetic spiral. New rhizomes appear on lateral sides of the mother rhizome. A lateral rhizome is subtended by a foliage leaf (N) and is accompanied by a RU in the position N + 2. We hypothesize a two-step process of regulation of RU/branch initiation, with the second step possibly involving environmental factors such as gravitropism. Each RU has a short stalk, 1-2 scale-like phyllomes and a long-pedicellate flower. We support a theory that the flower is lateral to the RU axis. The five sepals initiate successively and form two whorls as 3 + 2. The sepal arrangement is not 'intermediate' between whorled and spiral. Mechanisms of phyllotaxis establishment differ between flowers and lateral rhizomes. Petal, stamen and carpel numbers are not precisely fixed. Petals are smaller than sepals and form a whorl. They appear first in the sectors of the outer whorl sepals. The stamen arrangement is whorled to chaotic. The merism of the androecium tends to be the same as in the corolla. Flowers with odd numbers of stamen orthostichies are found. These are interpreted as having a non-integer merism of the androecium (e.g., 14.5). Carpels form a whorl in N. lutea and normally alternate with inner whorl stamens. Sterile second whorl carpel(s) are found in some flowers of N. pumila.

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“…Exterior tepals are typically initiated earlier during the floral development in many clades of plant species, including Anemone and Arabidopsis (Smyth et al, 1990;Ren et al, 2010). At present, tepal arrangements are identified manually (Endress, 2010;Ronse De Craene, 2010;Vislobokov et al, 2014;Kitazawa and Fujimoto, 2018;Kitazawa and Fujimoto, 2020). The visual examination of a large number of flower images is extremely labor intensive; moreover, judging these images unless one is a specialist is difficult.…”

Section: Introductionmentioning

confidence: 99%

Image recognition-based petal arrangement estimation

Nakatani,

Utsumi,

Fujimoto

et al. 2024

Front. Plant Sci.

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Flowers exhibit morphological diversity in the number and positional arrangement of their floral organs, such as petals. The petal arrangements of blooming flowers are represented by the overlap position relation between neighboring petals, an indicator of the floral developmental process; however, only specialists are capable of the petal arrangement identification. Therefore, we propose a method to support the estimation of the arrangement of the perianth organs, including petals and tepals, using image recognition techniques. The problem for realizing the method is that it is not possible to prepare a large number of image datasets: we cannot apply the latest machine learning based image processing methods, which require a large number of images. Therefore, we describe the tepal arrangement as a sequence of interior-exterior patterns of tepal overlap in the image, and estimate the tepal arrangement by matching the pattern with the known patterns. We also use methods that require less or no training data to implement the method: the fine-tuned YOLO v5 model for flower detection, GrubCut for flower segmentation, the Harris corner detector for tepal overlap detection, MAML-based interior-exterior estimation, and circular permutation matching for tepal arrangement estimation. Experimental results showed good accuracy when flower detection, segmentation, overlap location estimation, interior-exterior estimation, and circle permutation matching-based tepal arrangement estimation were evaluated independently. However, the accuracy decreased when they were integrated. Therefore, we developed a user interface for manual correction of the position of overlap estimation and interior-exterior pattern estimation, which ensures the quality of tepal arrangement estimation.

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

Abstract: We thank the Kuwagata family, S. Maeda and K. Horibe for their support in field work.

Cited by 8 publications

References 49 publications

Developmental stochasticity and variation in floral phyllotaxis

Developmental stochasticity and variation in floral phyllotaxis

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

Image recognition-based petal arrangement estimation

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