Generation of Leaf Shape Through Early Patterns of Growth and Tissue Polarity

Abstract

A major challenge in biology is to understand how buds comprising a few cells can give rise to complex plant and animal appendages like leaves or limbs. We address this problem through a combination of time-lapse imaging, clonal analysis, and computational modeling. We arrive at a model that shows how leaf shape can arise through feedback between early patterns of oriented growth and tissue deformation. Experimental tests through partial leaf ablation support this model and allow reevaluation of previous experimental studies. Our model allows a range of observed leaf shapes to be generated and predicts observed clone patterns in different species. Thus, our experimentally validated model may underlie the development and evolution of diverse organ shapes.

Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo

“…In plants, several spatially distinct cellular organizing centers that coordinate and organize organ development programs have been identified (3,12,13), as have genes that promote cell expansion through the loosening of cell walls (8). However, efforts to uncover growth regulatory mechanisms in plants are complicated by asynchronous cell division, in addition to variable gradients of spatial differentiation across complex and dynamically growing organs such as roots, meristems, and leaves (3,14,15).…”

“…However, there are few studies that link genes directly with shape change in a mechanistic way (3)(4)(5). In plants, where cells do not move, nearly all shape change and morphogenesis occur through the tightly regulated control over the mechanical properties of the cell wall.…”

Size and shape—integration of morphometrics, mathematical modelling, developmental and evolutionary biology

“…Similar to modern weather forecasts, this allows for describing regulatory networks and interactions of systems that would otherwise be too complex to handle. Recent cornerstones of a successful integration of mathematical models into evolutionary and developmental studies about shape variation are the prediction of a link between dorsal-ventral patterning mechanisms and tissue polarity organizers for proper flower shape formation, for example (Green et al 2010;Sauret-Güeto et al 2013), or insights into how leaf shape is established (Bilsborough et al 2011;Kuchen et al 2012). Population level variation in teeth morphology and tooth type differences in seals have been translated into mathematical models to disentangle the stages of development and the respective signaling changes responsible for the observed shape changes (Salazar-Ciudad and Jernvall 2010).…”

On the evolution of developmental mechanisms: Divergent polarities in leaf growth as a case study

“…Since basipetal leaf growth has been observed in all the model plants studied so far, 1,[3][4][5] it was considered universal and has therefore served as a paradigm to explain and model leaf growth in several species. [6][7][8][9] However, our recent survey of 75 eudicots 10 revealed that basipetal growth is not universal and that at least 3 more distinct growth patterns exist in nature: (i) acropetal leaf growth where differentiation begins near the base and progresses toward the tip (opposite of basipetal growth); (ii) even or diffused growth where the cells begin to differentiate synchronously throughout the leaf; and (iii) bidirectional growth where differentiation begins from both extremities and progresses toward the middle of the leaf. Since all these growth patterns are essentially different forms of polar or differential growth, we used the law of simple allometry to classify the growth patterns as positive allometry (basipetal growth), negative allometry (acropetal growth), isometry (diffused/even growth) and complex allometry (bidirectional growth).…”

“…When the distal half of a leaf of the winter annual Arabidopsis thaliana was excised at an early growth stage under laboratory condition, the remaining basal half grew to nearly normal size, lending some credence to the hypothesis discussed above. 7,12 The growth polarity of individual leaflets is independent of the direction of their initiation on compound leaves…”