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

Abstract

Most model plants used to study leaf growth share a common developmental mechanism, namely basipetal growth polarity, wherein the distal end differentiates first with progressively more proliferative cells toward the base. Therefore, this base-to-tip growth pattern has served as a paradigm to explain leaf growth and also formed the basis for several computational models. However, our recent report in The Plant Cell on the investigation of leaf growth in 75 eudicot species covering a wide range of eudicot families showed that leaves grow with divergent polarities in the proximo-distal axis or without any obvious polarity. This divergence in growth polarity is linked to the expression divergence of a conserved microRNA-transcription factor module. This study raises several questions on the evolutionary origin of leaf growth pattern, such as 'when and why in evolution did the divergent growth polarities arise?' and 'what were the molecular changes that led to this divergence?'. Here, we discuss a few of these questions in some detail.

Keywords: Compound leaf; Leaf development; evolution of growth pattern; growth allometry; micro RNA; polarity.

Figure 1.

Distribution of allometric growth patterns in 75 plant species sorted according to their growth habits, i.e., perennial or annual. The percentages within the circles indicate the fraction of total species belonging to a specific allomertry and the numbers inside the parentheses indicate the number of species.

Figure 2.

Schematic representation of growth polarities in simple and compound leaves. (A) Schematics showing the progression of cell proliferation arrest (yellow arrows) in simple leaves growing with different polarities. There is no directionality in cell division arrest in leaves growing evenly (the leaf schematic on the right). A similar schematic also appeared in our original Plant Cell article. (B) Schematic representation of the direction of leaflet formation and the growth gradient within individual leaflet on compound leaves. The black arrows indicate the direction of formation of leaflets; the yellow arrows indicate the direction of the progression of cell division arrest in individual leaflets; the red dots represent dividing cells. Note that there is no directional cell division arrest in the case of Cassia spectabilis since the cells throughout the individual leaflets exit cell proliferation simultaneously.