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Spiral phyllotaxis in flax. Left: 11 days after germination, the phyllotactic pattern is characterized by 3 counter-clockwise parastichies (one represented in red) and 5 clockwise parastichies (3:5 phyllotaxis). 11 days later, as a result of the increase in the size of the apex, the phyllotactic pattern has shifted to 5:8. However, the original 3 parastichies are still evident (one represented in red). (modified from Williams, 1974).
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Plant architecture is characterized by a high degree of regularity. Leaves, flowers and floral organs are arranged in regular patterns, a phenomenon referred to as phyllotaxis. Regular phyllotaxis is found in virtually all higher plants, from mosses, over ferns, to gymnosperms and angiosperms. Due to its remarkable precision, its beauty and its acc...
Contexts in source publication
Context 1
... spiral phyllotaxis, organs are formed with a constant diver- gence angle, usually 137.5°, resulting in an ontogenetic spiral which runs in clockwise or counter-clockwise direction (Fig. 1B). In addition, secondary spirals, the contact parastichies, can be dis- cerned which run in both directions (Fig. 3). Curiously, the number of parastichies in each direction represents consecutive terms in the Fibonacci series (Steeves and Sussex, 1989). This series consists of terms that represent the sum of the previous two numbers (0, 1, 1, 2, 3, 5, 8, 13, 21, 34, 55, etc.). The number of contact parastichies depends on the relative size of the ...
Context 2
... to the large flower disc, the numbers can be as high as 34:55. In many plants, the diameter of the meristem increases during development. This results in a gradual shift from lower to higher phyllotactic numbers, for example in flax, the phyllotactic pattern of the seedling starts with 3:5 and undergoes a gradual shift to 5:8 phyllotaxis ( Fig. 3; Williams, 1975). Interestingly, the 3:5 pattern remains recognizable for some time, even after the 5:8 spirals are already clearly prominent (Fig. ...
Context 3
... results in a gradual shift from lower to higher phyllotactic numbers, for example in flax, the phyllotactic pattern of the seedling starts with 3:5 and undergoes a gradual shift to 5:8 phyllotaxis ( Fig. 3; Williams, 1975). Interestingly, the 3:5 pattern remains recognizable for some time, even after the 5:8 spirals are already clearly prominent (Fig. ...
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Citations
... Background Auxin, a pivotal phytohormone, plays a central role in orchestrating fundamental processes throughout plant development. Its multifaceted influence spans various developmental stages across the entirety of the plant life cycle [1][2][3][4][5][6]. The key players in the intricate pathway of auxin signaling are the auxin/indole-3-acetic acid (Aux/ IAA) genes. ...
Background
The auxin/indole-3-acetic acid (Aux/IAA) gene family is a crucial element of the auxin signaling pathway, significantly influencing plant growth and development. Hence, we conducted a comprehensive investigation of Aux/IAAs gene family using the Sp75 and Monoe-Viroflay genomes in spinach.
Results
A total of 24 definitive Aux/IAA genes were identified, exhibiting diverse attributes in terms of amino acid length, molecular weight, and isoelectric points. This diversity underscores potential specific roles within the family, such as growth regulation and stress response. Structural analysis revealed significant variations in gene length and molecular weight. These variations indicate distinct roles within the Aux/IAA gene family. Chromosomal distribution analysis exhibited a dispersed pattern, with chromosomes 4 and 1 hosting the highest and lowest numbers of Aux/IAA genes, respectively. Phylogenetic analysis grouped the identified genes into distinct clades, revealing potential evolutionary relationships. Notably, the phylogenetic tree highlighted specific gene clusters suggesting shared genetic ancestry and potential functional synergies within spinach. Expression analysis under NAA treatment unveiled gene-specific and time-dependent responses, with certain genes exhibiting distinct temporal expression patterns. Specifically, SpoIAA5 displayed a substantial increase at 2 h post-NAA treatment, while SpoIAA7 and SpoIAA9 demonstrated continuous rises, peaking at the 4-hour time point.
Conclusions
These observations indicate a complex interplay of gene-specific and temporal regulation in response to auxin. Moreover, the comparison with other plant species emphasized both shared characteristics and unique features in Aux/IAA gene numbers, providing insights into the evolutionary dynamics of this gene family. This comprehensive characterization of Aux/IAA genes in spinach not only establishes the foundation for understanding their specific functions in spinach development but also provides a valuable resource for experimental validation and further exploration of their roles in the intricate network of auxin signaling pathways.
... For the past 25 years, many articles have been proposed supporting the biochemical research direction and stating that auxin (growth hormone) plays a dominant role in the morphogenesis of spiral patterns of phyllotaxis (Reinhardt, 2005;Jönsson et al., 2006). The observation of (Jean, 1994). ...
The mystery of the morphogenesis of phyllotaxis has been of concern for several generations of botanists and mathematicians. Of particular interest is the fact that the number of visible spirals is equal to the number from the Fibonacci series. The article proposes an analytical solution to two fundamental questions of phyllotaxis: what is the morphogenesis of patterns of spiral phyllotaxis? and why the number of visible spirals is equal to number from the Fibonacci series? The article contains videos illustrating the recursive dynamic model of spiral phyllotaxis morphogenesis.
... The regularity of plant architecture and morphology is a striking and mysterious phenomenon. The lateral organs, such as leaves, flowers, and floral organs, are arranged in regular patterns around a central axis (Reinhardt, 2005;Traas, 2013;Bartlett and Thompson, 2014). Leaves and flowers arise from the meristem in stereotypical patterns, known as phyllotaxis, which are related to the divergence angle between successive organs, most commonly approximating 137.5° (Smith et al., 2006;Okabe, 2012). ...
... Leaves and flowers arise from the meristem in stereotypical patterns, known as phyllotaxis, which are related to the divergence angle between successive organs, most commonly approximating 137.5° (Smith et al., 2006;Okabe, 2012). The floral organs also exhibit a characteristically symmetrical arrangement, with their number, position, and shape being precisely regulated (Reinhardt, 2005;Thomson and Wellmer, 2019). arf3 mutants exhibit obvious abnormalities in phyllotactic patterning, floral organ patterning, floral organ number, the patterning of abaxial tissues, and the establishment of apical and basal boundaries in primordia (Figures 3A, B, G-J; see section 4 for details). ...
... Although many mathematical, physical, and chemical models have been proposed to explain the mechanism of phyllotactic pattern formation, the regular initiation of organs and their spatial and temporal positioning is the basis for the formation of phyllotactic patterns from a developmental biology perspective (Reinhardt, 2005;Smith et al., 2006;Traas, 2013;Bergeron and Reutenauer, 2019). The phytohormone auxin plays a critical role in establishing phyllotactic patterns by promoting organ initiation (Prasad et al., 2011;Bhatia et al., 2016). ...
The key phytohormone auxin is involved in practically every aspect of plant growth and development. Auxin regulates these processes by controlling gene expression through functionally distinct AUXIN RESPONSE FACTORs (ARFs). As a noncanonical ARF, ARF3/ETTIN (ETT) mediates auxin responses to orchestrate multiple developmental processes during the reproductive phase. The arf3 mutation has pleiotropic effects on reproductive development, causing abnormalities in meristem homeostasis, floral determinacy, phyllotaxy, floral organ patterning, gynoecium morphogenesis, ovule development, and self-incompatibility. The importance of ARF3 is also reflected in its precise regulation at the transcriptional, posttranscriptional, translational, and epigenetic levels. Recent studies have shown that ARF3 controls dynamic shoot apical meristem (SAM) maintenance in a non-cell autonomous manner. Here, we summarize the hierarchical regulatory mechanisms by which ARF3 is regulated and the diverse roles of ARF3 regulating developmental processes during the reproductive phase.
... These zones are generated by asymmetric distribution of PIN1, such that PIN1 is preferentially located to membranes adjacent to cells with the highest auxin concentration, moving auxin up the concentration gradient to produce auxin maxima and deplete surrounding cells of auxin (Vernoux et al., 2000;Benková et al., 2003;Heisler et al., 2005;Vernoux et al., 2011;O'Connor et al., 2014). Thus, in this model, a lack of auxin is the inhibitory signal and prevents formation of primordia directly adja-cent to one another (Reinhardt et al., 2003;Reinhardt, 2005). The control of this PIN1 distribution is dependent on an ARF, MONOPTEROS (MP), with PIN1 polarity tracking MP activity, which is in turn determined by auxin distribution, suggesting a feedback loop in which high levels of auxin induce MP-mediated auxin signalling leading to increased transport of auxin towards those cells (Hardtke and Berleth, 1998;Bhatia et al., 2016). ...
Shoot branching plasticity relies on integration of diverse signals to regulate the activity of buds, which is partially mediated through auxin transport by PINs and the regulation thereof. Whilst PIN behaviour has been well characterised, the mechanisms by which PINs sense and respond to auxin, strigolactone and cytokinin remain unknown. In this thesis I investigate the regulation of PIN polarity in response to these hormones, presenting evidence of an age-dependent aspect to PIN1 behaviour. I then demonstrate that NPA-sensitive auxin flux or auxin concentration are insufficient to explain PIN1 behaviour and attempt to identify a mechanism by which PIN1 senses and responds to auxin at a sub-cellular level. Following this, I demonstrate the requirement of the central region of the PIN1 hydrophilic loop to confer strigolactone sensitivity and characterise the effect of the loss of this response on plant phenotypes and bud growth dynamics. Finally, I demonstrate cross-species differences in PIN hormone responses. As a whole, this work advances our understanding of hormonal control of auxin transport in the shoot and the way in which this affects shoot architecture.
... Leaf primordia are initiated from the PZ, where cells become responsive to differentiation. Leaf primordia in the PZ are generated in a temporally and spatially controlled manner; this process is referred to as phyllotaxy 34 . The SAM is anatomically divided into three well-defined cell layers: The epidermal (L1) and subepidermal (L2) layers, known as the tunica, and an inner layer (L3) that is referred to as the corpus 32,35 . ...
Leaves provide energy for plants, and consequently for animals, through photosynthesis. Despite their important functions, plant leaf developmental processes and their underlying mechanisms have not been well characterized. Here, we provide a holistic description of leaf developmental processes that is centered on cytokinins and their signaling functions. Cytokinins maintain the growth potential (pluripotency) of shoot apical meristems, which provide stem cells for the generation of leaf primordia during the initial stage of leaf formation; cytokinins and auxins, as well as their interaction, determine the phyllotaxis pattern. The activities of cytokinins in various regions of the leaf, especially at the margins, collectively determine the final leaf morphology (e.g., simple or compound). The area of a leaf is generally determined by the number and size of the cells in the leaf. Cytokinins promote cell division and increase cell expansion during the proliferation and expansion stages of leaf cell development, respectively. During leaf senescence, cytokinins reduce sugar accumulation, increase chlorophyll synthesis, and prolong the leaf photosynthetic period. We also briefly describe the roles of other hormones, including auxin and ethylene, during the whole leaf developmental process. In this study, we review the regulatory roles of cytokinins in various leaf developmental stages, with a focus on cytokinin metabolism and signal transduction processes, in order to shed light on the molecular mechanisms underlying leaf development.
... Directional asymmetry was determined in studied populations of P. avium (Table 4). The left-right symmetry of leaves could be related to auxin transport processes during the origination of leaf primordia in plants with a spiral organization of meristems (Reinhardt 2005;Chitwood et al. 2012). ...
Leaf shape variations and developmental instability were examined for the first time in natural populations of Prunus avium (L.) L. in the central Balkan region (Bosnia and Herzegovina) at different elevational points, from 230 to 1177 m. above sea level. Geometric morphometric tools were applied to assess the variability of leaf shapes and sizes, while a fluctuating asymmetry leaf index was used as a measure of leaf developmental instability. According to the results of canonical variate analysis for the symmetric component of shape variation and hierarchical analysis of variance for centroid size, the studied populations could be partially differentiated into three groups. The co-variation between leaf form (shape and size) and climate variables was significant, estimated by two-block partial least square analysis. Climate variables (the sum of precipitation in May and the De Martonne aridity index) mostly influenced leaf shape and size. A population situated at the highest elevation had the highest value for fluctuating asymmetry leaf index, which was an indication of developmental instability. High natural variability and interpopulation differences were observed for all studied leaf traits (leaf shape, centroid size, fluctuating asymmetry leaf index, leaf area, leaf length and width, petiole length). For well-known traditional morphometric measures (leaf area, leaf length, leaf width, and petiole length) in accordance with previous studies, intrapopulation variability was greater than interpopulation variability. For centroid size and the fluctuating asymmetry leaf index (measures used in geometric morphometrics) variability was higher among populations than within them. This indicates that geometric morphometrics could give new insights into infra-specific variability.
... The phenomenon of regular and periodic patterning of leaves (or other lateral organs) is called phyllotaxis and has drawn the attention of researchers for centuries (e.g., Jean, 1994;Adler, Barabé & Jean, 1997;Reinhardt, 2005;Kuhlemeier, 2007). In the plant kingdom, two major types of leaf arrangements, whorled and spiral (helical) (Zagórska-Marek, 1985;Zagórska-Marek, 1994), are recognised. ...
... A special whorled leaf arrangement, called decussate phyllotaxis, occurs when two leaves are formed per whorl. This is a common pattern in, for example, the families Lamiaceae and Caryophyllaceae (Rutishauser, 1998;Reinhardt, 2005;Gola & Banasiak, 2016). Another modification of whorled phyllotaxis is distichy, whereby only one leaf is initiated per whorl, but the next leaf is displaced the half distance around the stem, i.e., 180 • , with respect to the previous leaf. ...
The selection and validation of proper distinguishing characters are of crucial importance
in taxonomic revisions. The modern classifications of orchids utilize the molecular tools, but still the selection and identification of the material used in these studies is for the most part related to general species morphology. One of the vegetative characters quoted in orchid manuals is leaf arrangement. However, phyllotactic diversity and ontogenetic changeability have not been analysed in detail in reference to particular taxonomic groups. Therefore, we evaluated the usefulness of leaf arrangements in the taxonomy of the genus Epipactis Zinn, 1757. Typical leaf arrangements in shoots of this genus are described as distichous or spiral. However, in the course of field research and screening of herbarium materials, we indisputably disproved the presence of distichous phyllotaxis in the species Epipactis purpurata Sm. and confirmed the spiral Fibonacci pattern as the dominant leaf arrangement.
In addition, detailed analyses revealed the presence of atypical decussate phyllotaxis in this species, as well as demonstrated the ontogenetic formation of pseudowhorls. These findings confirm ontogenetic variability and plasticity in E. purpurata. Our results are discussed in the context of their significance in delimitations of complex taxa within the genus Epipactis.
... Floral organ development includes not only the meristematic signals of the ABC(DE) network which indicate the correct place where a tissue or organ will differentiate from the FM, but also changes in cell proliferation leading to the growth of floral organ primordia. This program initiates in response to meristematic signals and interacts with the organ identity genes (Reinhardt, 2005;Dornelas et al., 2011;Wellmer et al., 2014). As a result, each organ primordia grows initially by cell division and, subsequently, by cell expansion until it acquires its final size and shape (Anastasiou and Lenhard, 2007;Bögre et al., 2008). ...
Floral organogenesis requires coordinated interactions between genes specifying floral organ identity and those regulating growth and size of developing floral organs. With the aim to isolate regulatory genes linking both developmental processes (i.e., floral organ identity and growth) in the tomato model species, a novel mutant altered in the formation of floral organs was further characterized. Under normal growth conditions, floral organ primordia of mutant plants were correctly initiated, however, they were unable to complete their development impeding the formation of mature and fertile flowers. Thus, the growth of floral buds was blocked at an early stage of development; therefore, we named this mutant as unfinished flower development (ufd). Genetic analysis performed in a segregating population of 543 plants showed that the abnormal phenotype was controlled by a single recessive mutation. Global gene expression analysis confirmed that several MADS-box genes regulating floral identity as well as other genes participating in cell division and different hormonal pathways were affected in their expression patterns in ufd mutant plants. Moreover, ufd mutant inflorescences showed higher hormone contents, particularly ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and strigol compared to wild type. Such results indicate that UFD may have a key function as positive regulator of the development of floral primordia once they have been initiated in the four floral whorls. This function should be performed by affecting the expression of floral organ identity and growth genes, together with hormonal signaling pathways.
... Phyllotaxis primarily arises at the shoot apical meristem, a specialized tissue containing a stem cell niche and located at the tip of growing shoots. Rooted in early works of pioneers such as (Bonnet, 1754;Braun, 1831;Bravais and Bravais, 1837) and after decades of research, the idea that phyllotactic patterns emerge from simple physical or bio-chemical lateral inhibitions between successive organs produced at the meristem has become largely prevalent, (Adler et al., 1997;Jean, 1995;Kuhlemeier, 2007;Pennybacker et al., 2015;Reinhardt, 2005). Microscopic observations and modeling led to propose that this self-organizing process relies on five basic principles: i) organs can form only close to the tip of growing shoots, ii) no organ can form at the very tip, iii) pre-existing organs prevent the formation of new organs in their vicinity (Hofmeister, 1868), forming altogether an inhibitory field that covers the organogenetic zone, iv) due to growth, organs are progressively moved away from the organogenetic zone, v) a new organ is formed as soon as the influence of the inhibitory field produced by the existing organs fades away at the growing tip, (Schoute, 1913;Snow and Snow, 1962;Turing, 1952). ...
Exploration of developmental mechanisms classically relies on analysis of pattern regularities. Whether disorders induced by biological noise may carry information on building principles of developmental systems is an important debated question. Here, we addressed theoretically this question using phyllotaxis, the geometric arrangement of plant aerial organs, as a model system. Phyllotaxis arises from reiterative organogenesis driven by lateral inhibitions at the shoot apex. Motivated by recurrent observations of disorders in phyllotaxis patterns, we revisited in depth the classical deterministic view of phyllotaxis. We developed a stochastic model of primordia initiation at the shoot apex, integrating locality and stochasticity in the patterning system. This stochastic model recapitulates phyllotactic patterns, both regular and irregular, and makes quantitative predictions on the nature of disorders arising from noise. We further show that disorders in phyllotaxis instruct us on the parameters governing phyllotaxis dynamics, thus that disorders can reveal biological watermarks of developmental systems.
... Recently, developments in molecular biology have revealed that auxin plays a crucial role in primordium formation [4,8,[13][14][15]17]. It has been shown in biological experiments that auxin induces leaf and flower primordia in the stem tip, thereby indicating that auxin acts as an activator for primordium formation in stem tip. ...
... Here we will explain the behavior of auxin in a shoot apex from the papers [4,8,[13][14][15]17]. Two distinct types of auxin transport are observed in a shoot apex. ...
Phyllotactic patterns in plants are well known to be related to the golden ratio. Actually, many mathematical models using the theoretical inhibitory effect were proposed to reproduce these phyllotactic patterns. In 1996, Douady and Couder introduced a model using magnetic repulsion and succeeded in reproducing phyllotactic patterns numerically. On the other hand, it was recently revealed in biological experiments that a plant hormone, auxin, regulates the phyllotactic formation as an activator (Reinhardt et al., Nature 426:255–260, 2003). Then, there arises a natural question as to how the inhibitory effect can be related to the auxin. In this paper, a reaction diffusion model is proposed by taking account of auxin behavior in plant tips. The relationship between Douady and Couder’s model and our model is shown by singular limit analysis. It also provides us with the potential function corresponding to the inhibitory effect, and the bifurcation diagram.
