Control of Leaf and Vein Development by Auxin

Leaves are the main photosynthetic organs of vascular plants and show considerable diversity in their geometries, ranging from simple spoonlike forms to complex shapes with individual leaflets, as in compound leaves. Leaf vascular tissues, which act as conduits of both nutrients and signaling information, are organized in networks of different architectures that usually mirror the surrounding leaf shape. Understanding the processes that endow leaves and vein networks with ordered and closely aligned shapes has captured the attention of biologists and mathematicians since antiquity. Recent work has suggested that the growth regulator auxin has a key role in both initiation and elaboration of final morphology of both leaves and vascular networks. A key feature of auxin action is the existence of feedback loops through which auxin regulates its own transport. These feedbacks may facilitate the iterative generation of basic modules that underlies morphogenesis of both leaves and vasculature.Leaf form and vascular patterns provide some of the most impressive examples of the complexity of biological shapes generated in nature. A common feature of the development of the leaf lamina and vein networks is the repeated use of basic modules. For example, the iterative emergence of marginal leaf-shape elements, such as serrations, lobes, and leaflets (Fig. 1A–D), and the arrangement of successive orders of branched veins result in different types of leaf geometries and vascular patterns, respectively. Intriguingly, there is also congruence of leaf shape and vein layouts, such that, at least superficially, the pattern of vasculature formation is well aligned with the final geometry of the leaf lamina. These observations raise the questions of (1) what are the specific signaling pathways that sculpt leaf shape and vascular patterns, (2) to what degree lamina growth and vascular development share common genetic control, and finally (3) how coordination between leaf and vascular development is achieved and impacts on generation of final leaf shape and vein arrangement. Over the past 15 years, genetic approaches have led to substantial increase in our understanding of leaf and vascular development, and have provided good evidence that regulated activity of the small indolic growth regulator auxin provides important spatial cues for both processes. Such roles of auxin in different facets of leaf and vascular development is the focus of our article.Open in a separate windowFigure 1.Axes of leaf asymmetry and diversity of leaf shape. (A) A simple, serrated leaf of the Columbia ecotype of Arabidopsis thaliana. The proximo–distal (P–D) and medio–lateral (M–L) axes are indicated in the image. The asterisk marks one marginal serration. (B) The lobed leaf of the Arabidopsis thaliana relative Arabidopsis lyrata. The asterisk depicts the position of one lobe. Lobes are deep serrations, so the definition of an outgrowth as a serration or lobe is somewhat arbitrary. (C) The dissected leaf of Cardamine hirsuta. The asterisk marks a lateral leaflet. Leaflets are clearly defined as distinct units of the same leaf, which connect with the rachis (R) via a structure called a petiolule (Pu). (D) The dissected leaf of the cultivated tomato. Tomato demonstrates additional orders of dissection with respect to Cardamine hirsuta leaf and produces both primary leaflets (black asterisk) and secondary leaflets (red asterisk). (E) Scanning electron micrograph of the shoot apex of tomato. The white asterisk marks a leaf primordium (1) initiating from the meristem. The adaxial (yellow) and abaxial (orange) domains are marked on the subsequent developing leaf (2). Tomato is a compound leaf plant where leaflets are formed from the leaf blade soon after leaf initiation (a developing leaflet is marked by an arrow in leaf 3). Images in panels A–D are leaf silhouettes. Scale bars: (A–D) 1 cm, (E) 100 µm.