Self-organizing periodicity in development: organ positioning in plants

Abstract

Periodic patterns during development often occur spontaneously through a process of self-organization. While reaction-diffusion mechanisms are often invoked, other types of mechanisms that involve cell-cell interactions and mechanical buckling have also been identified. Phyllotaxis, or the positioning of plant organs, has emerged as an excellent model system to study the self-organization of periodic patterns. At the macro scale, the regular spacing of organs on the growing plant shoot gives rise to the typical spiral and whorled arrangements of plant organs found in nature. In turn, this spacing relies on complex patterns of cell polarity that involve feedback between a signaling molecule - the plant hormone auxin - and its polar, cell-to-cell transport. Here, we review recent progress in understanding phyllotaxis and plant cell polarity and highlight the development of new tools that can help address the remaining gaps in our understanding.

A sense of place, many times over ‐ pattern formation and evolution of repetitive morphological structures

“…Inside the main shoot, the repetitive deployment of the segmental phytomers depends on “phyllotaxis,” the process of periodic placement of plant lateral organs in regular intervals both around the central and apical‐basal axes of the shoot . Subsequent elongation of the phytomer then leads to the species‐specific spacing patterns observed between the individual segments.…”

“…Moreover, the fact that the eventual basal‐to‐apical 1D‐pattern of the shoot involves—in its inception—a two‐dimensional component, namely the circumferential positioning of lateral branches, has led to the consideration of different self‐organizing properties involved in the process. For example, inhibitory fields of leaf primordia have been proposed to affect spacing during phyllotactic patterning, and already Turing himself, and others, have argued that activator‐inhibitor pairs might underlie the patterning phenomenon of phyllotaxis . How exactly such interplay of positional information and self‐organizing principles is realized, however, and in which way the rate of apical‐basal growth as determined by the SAM affects this balance, is an area of active investigation using both theoretical and experimental approaches …”

“…61 Inside the main shoot, the repetitive deployment of the segmental phytomers depends on "phyllotaxis," the process of periodic placement of plant lateral organs in regular intervals both around the central and apical-basal axes of the shoot. 62 Subsequent elongation of the phytomer then leads to the species-specific spacing patterns observed between the individual segments. For the radial patterns circumscribing the shoot, lateral organ placement can occur in whorled, distichous (alternate), decussate (opposite) as well as spiral arrangements-the latter invoking the famous Fibonacci sequence.…”

“…For example, inhibitory fields of leaf primordia have been proposed to affect spacing during phyllotactic patterning, 64 and already Turing himself, and others, have argued that activator-inhibitor pairs might underlie the patterning phenomenon of phyllotaxis. 7,62,75,76 How exactly such interplay of positional information and self-organizing principles is realized, however, and in which way the rate of apical-basal growth as F I G U R E 2 Formation of repetitive morphological structures across kingdoms. A, In plants, apical-basal growth depends on a proliferative zone at the apex of the shoot called the "shoot apical meristem" (SAM).…”

“…Once progenitors leave the PFR, cell fate decision into either joint-or cartilage-forming cells instruct the digit segmentation pattern into individual "phalanges," potentially modulated by BMP inhibitors released from previously formed elements determined by the SAM affects this balance, is an area of active investigation using both theoretical and experimental approaches. 62,67,77…”