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Regulation of Phyllotaxis by Polar Auxin Transport

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Regulation of Phyllotaxis by Polar Auxin Transport articles Regulation of phyllotaxis by polar auxin transport Didier Reinhardt1*, Eva-Rachele Pesce1*, Pia Stieger1, Therese Mandel1, Kurt Baltensperger2, Malcolm Bennett3, Jan Traas4, Jir˘ı´ Friml5 & Cris Kuhlemeier1 1Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland 2Institute of Pharmacology, University of Bern, Friedbu¨hlstrasse 49, 3010 Bern, Switzerland 3School of Biosciences, University of Nottingham, Nottingham NG7 2RD, UK 4Laboratoire de Biologie Cellulaire, INRA, Route de Saint Cyr, 78026 Versailles cedex, France 5Zentrum fu¨r Molekularbiologie der Pflanzen, Universita¨tTu¨bingen, Auf der Morgenstelle 3, D-72076 Tu¨bingen, Germany * These authors contributed equally to this work ........................................................................................................................................................................................................................... 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. A major determinant of plant architecture is the arrangement of valid predictions about the transport and distribution of auxin leaves and flowers around the stem, known as phyllotaxis1. Leaves within the shoot apex, we studied the expression pattern and and flowers are formed by the shoot apical meristem in character- subcellular localization of the putative Arabidopsis influx and istic patterns such as alternate (distichous), opposite (decussate), efflux carriers, AUXINRESISTANT1(AUX1)22 and PIN- or—most frequently—spiral1,2. Spiral phyllotaxis has received much FORMED1 (PIN1)23. In addition, we performed micro-application attention from theoreticians because the divergence angle between of auxin to Arabidopsis meristems to address the role of auxin in successive leaves approaches the golden ratio of 137.58, and the phyllotaxis. spiral arrangements are characterized by the Fibonacci numbers1,3,4. Models of phyllotaxis explain the regular spacing of leaf primordia PIN1 expression and localization in Arabidopsis apices 5 with mechanisms based on “the first available space” , “biophysical In vegetative apices, PIN1 protein was detected in the epidermis and 6 forces” within the meristem , or “inhibitors of organogenesis” the vasculature of developing leaf primordia, as well as in the released from young leaf primordia3,7. Although mathematical meristem L1 layer and, at lower levels, in L2 (Fig. 1a). A marked modelling of phyllotactic mechanisms based on biophysical or induction at the meristem flank (Fig. 1a) corresponded with the site biochemical regulation can recreate phyllotactic patterns3,6,8, experi- of incipient and young leaf primordia (Fig. 1b). PIN1 signal in the mental support for such phyllotactic mechanisms is lacking. L1 and L2 layers was consistently localized to the apical side of the Auxin has been implicated in various aspects of plant develop- cells, that is, pointing to the meristem summit (Fig. 1c, arrowheads), 9–13 14,15 ment, including embryogenesis , root development , and vas- except for the cells close to the site of incipient leaf initiation (I1). In 16 cular differentiation . Recently, auxin has been shown to induce these cells, the signal pointed to I1 (Fig. 1c, arrows). At the summit leaf and flower formation at the shoot apical meristem (SAM)17.As itself, the signal was more diffuse than at the flank (Fig. 1c). In the a trigger of organ initiation, auxin could play a role in determining epidermis of young leaf primordia, PIN1 signal was restricted to organ position and thereby phyllotaxis18. the apical side of the cells (Fig. 1d, e), as in cotyledon primordia24.At An instructive role of a signal molecule implies regulated distri- the site of incipient organ formation, PIN1 protein in the inner cell bution in the tissue. This could be achieved by defined sources of the layers was first localized with no obvious direction of polarization signal, by regulated degradation, or by controlled transport of the (Fig. 1f), but at the time of primordium outgrowth, PIN1 was signal to certain sites in the tissue. Auxin has its own polar transport detected at the side of the cells that points to the centre of the leaf route consisting of specific influx and efflux carriers in the plasma primordia (Fig. 1g). This localization suggests accumulation of membrane19. Net auxin flux results from coordinated polar local- auxin in the centre of the young primordia. ization of the auxin efflux carrier in the auxin-conducting cells20. During primordium outgrowth, PIN1 became restricted to a This routing of auxin is responsible for basipetal auxin transport narrow file of cells that comprised 2–3 cells in width, corresponding from the young leaves towards the root. In the root tip, active polar presumably to the provascular strand, and the PIN1 signal in these transport generates an auxin maximum in the columella initials, cells became gradually localized to the basal end of the cells (Fig. 1h). which regulates meristem development and cell differentiation14,15. The gradual restriction to narrow cell files and the subcellular Furthermore, auxin efflux carriers mediate gravitropism by creating polarization of PIN1, first towards the centre and later towards asymmetric auxin distribution, thereby causing anisotropic the base of the leaf primordia, is suggestive of a canalization growth21. mechanism25. The canalization theory proposes that small local We have previously proposed that active auxin transport in differences in auxin concentration are amplified by a self- the shoot apex could generate patterned auxin distribution, reinforcing accumulation mechanism, resulting in local auxin thereby determining the pattern of organ formation. To allow elevation and auxin depletion in the surrounding tissue. As a NATURE | VOL 426 | 20 NOVEMBER 2003 | www.nature.com/nature © 2003 Nature Publishing Group 255 articles consequence, the cells that experience high auxin levels are Organ formation in mutants with auxin-related defects restricted to narrow stripes that are determined to become auxin- The similar expression patterns of PIN1 in vegetative and floral conducting cell files25. apices suggest a comparable function of PIN1 and auxin in the In inflorescence apices, PIN1 expression followed a similar induction of leaves and flowers. However, pin1 mutants can form phyllotactic pattern as in vegetative meristems (Fig. 1i, compare leaves, although their size, shape, and position are aberrant27,28.To with Fig. 1b). Notably, PIN1 induction was already clearly visible in address the role of auxin in leaf formation, we treated young pin1 incipient flower primordia at the I3 stage, at least one plastochron plants with indole-3-acetic acid (IAA), resulting in the formation of earlier than the induction of the organ marker gene LEAFY (LFY)26 normal leaves (Fig. 2a). In addition, we crossed pin1 mutants with (Fig. 1j). PIN1 was detected in the vasculature of the inflorescence lfy mutants, which form leaves and axillary inflorescences instead of stem as well as in young flower primordia (Fig. 1k). In the flowers26. Treatment of pin-shaped apices of pin1;lfy double inflorescence meristem, the PIN1 signal was strongest in the L1 mutants with IAA resulted in the formation of leaves instead of layer, and lower in the interior layers with upregulation at the site of flowers (Fig. 2b). These leaves had abundant trichomes on their incipient organ formation (arrowhead in Fig. 1k). In young flower abaxial side (Fig. 2b), and formed pin-shaped lateral branches in primordia, PIN1 expression was elevated at the flank, at the site of their axils (not shown), indicating that they corresponded to cauline sepal induction (Fig. 1l), and later where the inner whorl organs leaves. Hence, IAA can trigger the initiation of rosette leaves, cauline were formed (Fig. 1m). leaves, and flowers17. Figure 1 Localization of the PIN1 protein in Arabidopsis apices. a, Median longitudinal inflorescence apex with PIN1 signal in the centres of flower primordia (P1–P8), and at the section through a vegetative apex. Note PIN1 signal (red) in the vasculature of leaf site of incipient flower formation (I1–I3). j, Section as in i hybridized with an antisense primordia and at the site of incipient organ formation (I1). b, Cross-section of an apex as in probe against LEAFY mRNA. k, Longitudinal section through an inflorescence apex. Note a. The outline of primordia (blue) is highlighted for clarity. Note PIN1 expression in young PIN1 signal in the vasculature, in the L1 layer of inflorescence and flower meristems, and primordia (P1,P2 and P3) and the developing central vein of older primordia (P4–P8).
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