Correction to: Developmental stochasticity and variation in floral phyllotaxis

A correction to this paper has been published: https://doi.org/10.1007/s10265-021-01307-2

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.

Recurrent requirement for the m6A-ECT2/ECT3/ECT4 axis in the control of cell proliferation during plant organogenesis

ABSTRACTmRNA methylation at the N6-position of adenosine (m6A) enables multiple layers of post-transcriptional gene control, often via RNA-binding proteins that use a YT521-B homology (YTH) domain for specific m6A recognition. In Arabidopsis, normal leaf morphogenesis and rate of leaf formation require m6A and the YTH-domain proteins ECT2, ECT3 and ECT4. In this study, we show that ect2/ect3 and ect2/ect3/ect4 mutants also exhibit slow root and stem growth, slow flower formation, defective directionality of root growth, and aberrant flower and fruit morphology. In all cases, the m6A-binding site of ECT proteins is required for in vivo function. We also demonstrate that both m6A methyltransferase mutants and ect2/ect3/ect4 exhibit aberrant floral phyllotaxis. Consistent with the delayed organogenesis phenotypes, we observe particularly high expression of ECT2, ECT3 and ECT4 in rapidly dividing cells of organ primordia. Accordingly, ect2/ect3/ect4 mutants exhibit decreased rates of cell division in leaf and vascular primordia. Thus, the m6A-ECT2/ECT3/ECT4 axis is employed as a recurrent module to stimulate plant organogenesis, at least in part by enabling rapid cellular proliferation.

Cecilanthus polymerus, a novel multiparted flower from the mid-Cretaceous Rocky Point locality, Maryland

A flower from the early Cenomanian of northeastern Maryland, Cecilanthus polymerus gen. et sp. nov., is described using SEM and synchrotron X-ray microtomography. The flower has >20 strap-shaped tepals, ca. 50 spatulate stamens with embedded adaxial pollen sacs and possibly H-valvate dehiscence, and ca. 100 more-or-less plicate carpels. Floral phyllotaxis is whorled, with >10 parts per whorl, but slightly irregular. Pollen and ovules are not preserved, but locule shape suggests that the carpels are uniovulate. Similar characters occur in extant Magnoliales and the basal ANITA grade, but never in combination. In an attempt to resolve these ambiguities, we performed morphological phylogenetic analyses, with the arrangement of extant taxa constrained to trees based primarily on molecular data. With anther dehiscence and ovule number treated as unknown, Cecilanthus has several most-parsimonious positions: nested in Nymphaeales, nested in Magnoliales, sister to Laurales, and sister to Chloranthaceae. However, scoring anther dehiscence as H-valvate and ovule number as = 1, increases support for a position in Magnoliales. Cecilanthus demonstrates that the early radiation of angiosperms produced floral morphotypes unlike those in any surviving taxa, and it illustrates the value of characters such as pollen morphology and seed anatomy for phylogenetic placement of floral mesofossils.

Floral organogenesis in Urophysa rockii, a rediscovered endangered and rare species of Ranunculaceae

Urophysa is an Asian endemic genus in the Ranunculaceae, but data on floral organogenesis, which would be a useful complement to molecular data in clarifying the relationship with closely related taxa (Aquilegia and Semiaquilegia) in Ranunculaceae, are completely lacking. We used scanning electron microscopy and light microscopy to study the floral development of Urophysa rockii Ulbrich, a recently rediscovered species in this genus. The sepals are initiated spirally, whereas other organs are nonsimultaneously whorled; the floral phyllotaxis is whorled. Primordia of the sepals are lunular and truncate, but those of the petals and stamens are hemispherical and rounded. After sepal initiation, there is a delay in development, but the initiation of petals and stamens is continuous. The developmental sequence of the microspores in the stamens is centrifugal, although the stamens are initiated centripetally. The early developmental stages of the staminodes are similar to those of the stamens, although much smaller, so they may be phylogenetically homologous organs. The carpel primordia are lunular in shape and plicate. The mature ovule is anatropous and bitegmic. Urophysa shows similar floral development features as Aquilegia and Semiaquilegia, although with some differences, which supports the relationship inferred by DNA sequence data.

Stochastic occurrence of trimery from pentamery in floral phyllotaxis of Anemone (Ranunculaceae)

Merosity, indicating the basic number of floral organs such as sepals and petals, has been constrained to specific and stable numbers during the evolution of angiosperms. The ancestral flower is considered to have a spiral arrangement of perianth organs, as in phyllotaxis, the arrangement of leaves. How has the ancestral spiral evolved into flowers with specific merosities? To address this question, we studied perianth organ arrangement in the <em>Anemone</em> genus of the basal eudicot family Ranunculaceae, because various merosities are found in this genus. In three species, <em>A. flaccida</em>, <em>A. scabiosa</em>, and <em>A. nikoensis</em> that are normally pentamerous, we found positional arrangement of the excessive sixth perianth organ indicating the possibility of a transition from pentamerous to trimerous arrangement. Arrangement was intraspecifically stochastic, but constrained to three of five types, where trimerous arrangement was the most frequent in all species except for a form of <em>A. scabiosa</em>. The rank of frequency of the other two types was species-dependent. We connect these observations with classical theories of spiral phyllotaxis. The phyllotaxis model for initiation of the sixth organ showed that the three arrangements occur at a divergence angle &lt;144°, indicating the spiral nature of floral phyllotaxis rather than a perfect penta-radial symmetry of 144°. The model further showed that selective occurrence of trimerous arrangement is mainly regulated by the organ growth rate. Differential organ growth as well as divergence angle may regulate transitions between pentamerous and trimerous flowers in intraspecific variation as well as in species evolution.

Geometric parameters of the apical meristem and the quality of phyllotactic patterns in Magnolia flowers

The ratio of primordium size to the meristem size (<em>P/M </em>ratio) is regarded by some geometrical models of phyllotaxis as the parameter, which determines the quality of spiral and whorled patterns of lateral organ arrangement. This assumption was tested on floral meristems in four genets representing four <em>Magnolia </em>taxa: <em>M. </em>× <em>salicifolia</em>, <em>M. stellata</em>, <em>M. denudata </em>and <em>M. acuminata</em>. In successive zones of <em>Magnolia </em>flower, lateral organs are initiated in specific phyllotactic patterns and at specific values of the meristem and primordia sizes. The elements of perianth, usually positioned in three trimerous whorls, are initiated as large primordia on relatively small meristem. The switch in the identity of primordia, from tepals to stamens is accompanied by an abrupt increase in the size of the meristem and decrease in the primordia size. Small values of <em>P/M </em>ratio and frequent occurrence of qualitative transformations of phyllotaxis contribute to the exceptionally rich spectrum of spiral patterns in androecium zone. New spiral patterns emerge when bigger primordia of carpels are initiated on the meristem, which at the same time starts diminishing in size either abruptly (<em>M. </em>× <em>salicifolia</em>, <em>M. stellata</em>, <em>M. acuminata</em>) or slowly (<em>M. denudata</em>). Spiral patterns identified in gynoecia have lower numbers of parastichies than the patterns of androecia and occur in frequencies specific for the genet. Although noted ranges of the meristem and primordia sizes, justify the occurrence of phyllotactic patterns observed in successive zones of <em>Magnolia </em>flower, they do not explain genet-specific frequencies of the patterns observed in gynoecium zone. The lack of straightforward relationship between frequency of the patterns and <em>P/M </em>ratio in gynoecium suggests that more complex geometrical factors or factors of non-geometrical nature are engaged in determination of <em>Magnolia </em>floral phyllotaxis.