Therese Mandel

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.

A striking phenomenon unique to the kingdom of plants is the regular arrangement of lateral organs around a central axis, known as phyllotaxis. Recent molecular-genetic experiments indicate that active transport of the plant hormone auxin is the key process regulating phyllotaxis. A conceptual model based on these experiments, introduced by Reinhardt et al. [Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T., Baltensperger, K., et al. (2003) Nature 426, 255-260], 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.

Expansins are extracellular proteins that increase plant cell wall extensibility in vitro. Beads loaded with purified expansin induced bulging on the leaf-generating organ, the apical meristem, of tomato plants. Some of these bulges underwent morphogenesis to produce leaflike structures, resulting in a reversal of the direction of phyllotaxis. Thus, expansin can induce tissue expansion in vivo, and localized control of tissue expansion may be sufficient to induce leaf formation. These results suggest a role for biophysical forces in the regulation of plant development.

Animal-mediated pollination is essential in plant reproductive biology and is often associated with pollination syndromes, sets of floral traits, such as color, scent, shape, or nectar content. Selection by pollinators is often considered a key factor in floral evolution and plant speciation. Our aim is the identification and characterization of the genetic changes that caused the evolution of divergent pollination syndromes in closely related plant species. We focus on ANTHOCYANIN2 (AN2), a well-defined myb-type transcription factor that is a major determinant of flower color variation between Petunia integrifolia and Petunia axillaris. Analysis of sequence variation in AN2 in wild P. axillaris accessions showed that loss-of-function alleles arose at least five times independently. DNA sequence analysis was complemented by functional assays for pollinator preference using genetic introgressions and transgenics. These results show that AN2 is a major determinant of pollinator attraction. Therefore, changes in a single gene cause a major shift in pollination biology and support the notion that the adaptation of a flowering plant to a new pollinator type may involve a limited number of genes of large effect. Gene identification and analysis of molecular evolution in combination with behavioral and ecological studies can ultimately unravel the evolutionary genetics of pollination syndromes.