The regular arrangement of leaves around a plant's stem, called phyllotaxis, has for centuries attracted the attention of philosophers, mathematicians and natural scientists; however, to date, studies of phyllotaxis have been largely theoretical. Leaves and flowers are formed from the shoot apical meristem, triggered by the plant hormone auxin. Auxin is transported through plant tissues by specific cellular influx and efflux carrier proteins. Here we show that proteins involved in auxin transport regulate phyllotaxis. Our data indicate that auxin is transported upwards into the meristem through the epidermis and the outermost meristem cell layer. Existing leaf primordia act as sinks, redistributing auxin and creating its heterogeneous distribution in the meristem. Auxin accumulation occurs only at certain minimal distances from existing primordia, defining the position of future primordia. This model for phyllotaxis accounts for its reiterative nature, as well as its regularity and stability.

, provides an intuitively plausible interpretation of the data, but raises questions of whether the proposed mechanism is, in fact, capable of producing the observed temporal and spatial patterns, is robust, can start de novo, and can account for phyllotactic transitions, such as the frequently observed transition from decussate to spiral phyllotaxis. To answer these questions, we created a computer simulation model based on data described previously or in this paper and reasonable hypotheses. The model reproduces, within the standard error, the divergence angles measured in Arabidopsis seedlings and the effects of selected experimental manipulations. It also reproduces distichous, decussate, and tricussate patterns. The model thus offers a plausible link between molecular mechanisms of morphogenesis and the geometry of phyllotaxis.active transport ͉ auxin ͉ PIN ͉ polarity ͉ computer simulation W ithin the variety of phyllotactic patterns found in nature, the most intriguing and, at the same time, the most prevalent is the spiral phyllotactic pattern characterized by the arrangement of organs into conspicuous spirals (parastichies), where the numbers of parastichies are consecutive elements of the Fibonacci series. This pattern is related to the divergence angle between organs approximating the golden angle of 137.5°. In the entire world of developmental biology, phyllotaxis is perhaps the most striking example of a phenomenon that can only be described by using quantitative notions of geometry.The regularity and mathematical properties of spiral phyllotaxis have attracted the attention of biologists and mathematicians since the early 19th century. They proposed conceptual, mathematical, and computational models, which elucidated the geometric properties of spiral phyllotactic arrangements (1) and the emergence of phyllotactic patterns during plant development. This latter category of models was pioneered by Hofmeister (2) and Snow and Snow (3), who hypothesized that the creation of new primordia is inhibited by the proximity of older primordia. New primordia, therefore, can be formed only at a certain minimal distance from the old ones. This general hypothesis has subsequently been refined into a number of computational models, postulating and exploring different types of inhibitory mechanisms such as geometric spacing (4), physical forces (5, 6), and chemical signals (7,8).In the absence of molecular data, the proposed mechanisms were more or less abstract. Recent experiments, however, provided an insight into the molecular processes involved in phyllotaxis, pointing to the central role of active transport of the plant hormone auxin. When shoot apices were cultivated in the presence of auxin transport inhibitors, the induction of lateral organs was blocked, and the apices grew vigorously as radially symmetric structures. Application of the natural auxin indole-3-acetic acid (IAA) to such pin-shaped meristems induced lateral primordia, with the size and position depending on the concentration and the position o...

Leaves originate from the shoot apical meristem, a small mound of undifferentiated tissue at the tip of the stem. Leaf formation begins with the selection of a group of founder cells in the so-called peripheral zone at the flank of the meristem, followed by the initiation of local growth and finally morphogenesis of the resulting bulge into a differentiated leaf. Whereas the mechanisms controlling the switch between meristem propagation and leaf initiation are being identified by genetic and molecular analyses, the radial positioning of leaves, known as phyllotaxis, remains poorly understood. Hormones, especially auxin and gibberellin, are known to influence phyllotaxis, but their specific role in the determination of organ position is not clear. We show that inhibition of polar auxin transport blocks leaf formation at the vegetative tomato meristem, resulting in pinlike naked stems with an intact meristem at the tip. Microapplication of the natural auxin indole-3-acetic acid (IAA) to the apex of such pins restores leaf formation. Similarly, exogenous IAA induces flower formation on Arabidopsis pin-formed1-1 inflorescence apices, which are blocked in flower formation because of a mutation in a putative auxin transport protein. Our results show that auxin is required for and sufficient to induce organogenesis both in the vegetative tomato meristem and in the Arabidopsis inflorescence meristem. In this study, organogenesis always strictly coincided with the site of IAA application in the radial dimension, whereas in the apical-basal dimension, organ formation always occurred at a fixed distance from the summit of the meristem. We propose that auxin determines the radial position and the size of lateral organs but not the apical-basal position or the identity of the induced structures. INTRODUCTIONLeaf primordia develop in regular patterns from the shoot apical meristem. In the majority of flowering plants, the leaves are arranged in spirals, with the divergence angle between successive leaves approaching the Fibonacci angle of 137.5 Њ , the so-called golden ratio (Steeves and Sussex, 1989;Lyndon, 1990Lyndon, , 1998Jean, 1994). Molecular and genetic analyses have recently identified various genes that regulate meristem development and leaf formation. Some of these genes encode transcription factors of the homeobox class (Vollbrecht et al., 1991;Long et al., 1996;Kerstetter et al., 1997; Taylor, 1997;Mayer et al., 1998), whereas others, such as clavata1 , clavata3, and zwille, appear to be involved in cell-to-cell signaling Moussian et al., 1998;Fletcher et al., 1999; Trotochaud et al., 1999). Current models postulate that these genes control the balance between meristem self-propagation and the production of organogenic tissue.Whereas genetic analyses provide us with an ever more detailed description of meristem maintenance and propagation, the molecular nature of the mechanisms that trigger leaf initiation and ensure that leaves form at the proper angles relative to each other remains to be established. In many m...

Strigolactones were originally identified as stimulators of the germination of root-parasitic weeds 1 that pose a serious threat to resource-limited agriculture 2 . They are mostly exuded from roots and function as signalling compounds in the initiation of arbuscular mycorrhizae 3 , which are plant-fungus symbionts with a global effect on carbon and phosphate cycling 4 . Recently, strigolactones were established to be phytohormones that regulate plant shoot architecture by inhibiting the outgrowth of axillary buds 5,6 . Despite their importance, it is not known how strigolactones are transported. ATP-binding cassette (ABC) transporters, however, are known to have functions in phytohormone translocation [7][8][9] . Here we show that the Petunia hybrida ABC transporter PDR1 has a key role in regulating the development of arbuscular mycorrhizae and axillary branches, by functioning as a cellular strigolactone exporter. P. hybrida pdr1 mutants are defective in strigolactone exudation from their roots, resulting in reduced symbiotic interactions. Above ground, pdr1 mutants have an enhanced branching phenotype, which is indicative of impaired strigolactone allocation. Overexpression of Petunia axillaris PDR1 in Arabidopsis thaliana results in increased tolerance to high concentrations of a synthetic strigolactone, consistent with increased export of strigolactones from the roots. PDR1 is the first known component in strigolactone transport, providing new opportunities for investigating and manipulating strigolactone-dependent processes.Strigolactones are a new class of carotenoid-derived 10 phytohormone in land plants. In addition to their role in shoot branching, strigolactones are exuded into the rhizosphere under phosphorus-limiting conditions 5 and act as growth stimulants of arbuscular mycorrhizal fungi 3 . To identify efflux carriers of arbuscular-mycorrhiza-promoting factors such as strigolactones, we used a degenerate primer approach ( Supplementary Fig. 2a) to isolate full-size PDR-type transporters (also known as ABC subtype G (ABCG) transporters) of P. hybrida that are abundant in phosphate-starved or mycorrhizal roots. The rationale behind the focus on these transporters, of which there are 15 in Arabidopsis 11 , 23 in Oryza sativa (rice) 11 and 23 putative factors in Solanum lycopersicum (tomato) ( Supplementary Fig. 3a), was that they are plasma membrane proteins often found in roots 12 , they are implicated in below-ground plantmicrobe interactions 13,14 , and they have affinities for compounds that are structurally related to strigolactones 8,9,15 . Of six primary candidates, only P. hybrida PDR1 had increased expression in roots that were subjected to either phosphate starvation (Fig. 1a) or colonization by the arbuscular mycorrhizal fungus Glomus intraradices (Fig. 1b). Furthermore, PDR1 transcript levels increased in response to treatment with the synthetic strigolactone analogue GR24 or the auxin analogue 1-naphthaleneacetic acid (NAA) (Fig. 1c). Auxin has been shown to upregulate strigolactone-bi...