Romanesco broccoli grows in a geometric shape called a fractal. The central structure is a meristem that produces small primordial meristems that induce new meristems, which gives rise to the fractal shape. © INRA, LAUFS Patrick

Shaping up: how plants take form

Growth coordination at the cellular level

The growth of plant organs is not anarchic. It is determined by hormonal and mechanical signals that coordinate the direction and speed of growth.

By Pascale Mollier, translated by Teri Jones-Villeneuve
Updated on 02/10/2016
Published on 12/15/2015

Romanesco broccoli observed under a scanning electronic microscope. The central structure is a meristem that produces small primordial meristems that induce new meristems, which gives rise to the fractal shape. © INRA, LAUFS Patrick
Romanesco broccoli observed under a scanning electronic microscope. The central structure is a meristem that produces small primordial meristems that induce new meristems, which gives rise to the fractal shape © INRA, LAUFS Patrick

Meristems and primordia

Plant growth and development occurs via the meristems, undifferentiated cell masses from which new cells are continually formed. Meristematic cells, which conserve characteristics of pluripotent cells, are comparable to stem cells in mammals. Meristems are found at the tips of the stem, roots and leaf axils and all along the stem and roots. Trees, for example, have a layer of meristematic cells called a cambium that governs trunk thickness.

The initial growth trigger still unknown

The shoot apical meristem induces the formation of leaves and flowers according to a characteristic pattern for a given species. The formation of a new organ begins by the appearance of region of intense divisions on the sides of the meristem called a primordium. Organ growth is not anarchic, which implies some sort of coordination and communication between the primordial cells. Two main types of communication have been identified between these cells: hormonal and mechanical.

Hormonal coordination hormonale: local auxin gradients

. © INRA
© INRA

Diagram key: Model of the polar auxin transport role in the development of lateral organs at the shoot apical meristem. Auxin accumulates locally and triggers the formation of an initium (i3) that becomes a primordium (P2). The auxin is then evacuated by the provascular tissues (black arrows in P2).

Auxin plays a determining role in the initiation and growth of new organs. At the cellular level, it affects the mechanical properties of the plant cell wall and its extension during the cell’s growth. Localised auxin accumulation triggers the appearance of a primordium. Incidentally, a primordium can be produced by placing a drop of auxin on a meristem. These “wells” of auxin become stronger due to a special phenomenon in which cells near those rich in auxin accentuate the gradient by providing auxin to these cells. A leaf then develops, while nearby, the cells having lost their auxin can no longer multiply. As the stem grows, the auxin wells move further apart and more auxin gradients can form away from the first, which determines the space between leaves. Polar auxin transport is governed by the movement of auxin membrane transporters (1) from one side of a cell to the other. The exact mechanism that leads to specific localisation of these transporters is unknown (see Section 5).

Mechanical coordination: like an inflating balloon

See the video

Recent research at INRA has shed light on another type of interaction between growing cells within a primordium: the mechanical forces rising from the pressure cells exert on each other. In fact, the primordium resembles a bunch of balloons packed tightly next to each other. Each cell is like a balloon attempting to get expand at its own rhythm, but which is limited by its neighbours. The cell will eventually grow in the direction where the pressure is the least intense. It begins by re-routing the microtubules in its cytoskeleton to withstand the dominant tension by forming a ring, much like the way metal hoops are used to strengthen barrels. The cell then grows in a perpendicular direction to this ring (i.e., towards the outer edges of the “barrel”). “Modelling helps us better understand how a primordium grows because this growth depends on both the individual behaviour of each cell and their interactions with each other. As in any complex system, the whole is bigger than the sum of its parts, with emerging properties that are not always predictable,” explains Jan Traas, who has developed models to study this behaviour. Jan Traas’ and Olivier Hamant’s teams were pioneers in demonstrating this mechanical control of growth.

Interactions between hormonal and mechanical control

The two types of growth control can be linked into several interdependent feedback loops as a sort of organizational chart within the primordium:

Diagram of plant growth regulation. © INRA, Jan Traas
Diagram of plant growth regulation © INRA, Jan Traas

“We’ve been able to create high-quality virtual models of organ growth. But we don’t yet have a mechanical model that lets us predict how and where growth will happen by integrating the auxin pump system and the role of the cytoskeleton. To break down these mechanisms, we need to quantify the speed and direction of growth at the cellular level (3) and tie these measurements to differential gene expression. Then, we’ll be able to identify which genes are involved and their hierarchy. This is what we’re aiming for now, but we still have ten or twenty years ahead of us,” says Jan Traas.

Multiple genes involved

Following studies on mutants, researchers have been able to identify dozens of “leader” genes since the nineties that are involved in plant growth and development. These genes encode transcription factors and can command several other genes themselves, including genes responsible for remodelling the cell wall, which are the first to be called on for cell expansion. There are about a hundred of these genes. So far, few links have been established between the cell wall structure and the plant growth regulation network (see Section 4).

(1) Auxin transporters: Membrane proteins called PIN proteins (see Section 5).

(2) Cell wall growth occurs perpendicular to the microtubules (see Section 4).

(3) A recent article describes a methodology to do this using confocal microscopy combined with data processing. Nature Methods 2010.

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Plant Biology and Breeding
Associated Centre(s):
Auvergne Rhône-Alpes

References

Uyttewaal M., …, Hamant O. 2012. A katanin-dependent microtubule response to mechanical stress enhances growth gradients between neighboring cells in Arabidopsis. Cell 149, 439-451
Vernoux T., …, Traas J. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7: 508
Heisler, M., …, Traas, J, Meyerowitz, E. 2010. Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport. Plos Biol 8(10):e1000516
Hamant O., …, Traas J. 2008. Developmental patterning by mechanical signals inArabidopsis. Science, 322 (5908), 1650-1655

Shapes govern genes

New research has shown that the expression of the SHOOT MERISTEMLESS gene (STM, see Section 2), which is necessary to shoot apical meristem maintenance and therefore leaf formation, is stimulated and maintained in the curved area of the meristem, a region subject to high-pressure interactions between cells. Researchers have used micromechanical approaches to show that the physical forces are able to induce expression of the STM gene and that this mechanism is independent of growth hormones.

A direct means to track auxin

A method was recently developed by Téva Vernoux’s and Jan Traas’ teams that lets researchers track auxin in situ in cells using engineered fluorescent auxin sensors. This system, called DII-VENUS, was successfully used to visualise changes in auxin distribution during two development processes, the root gravitropic response and lateral organ production at the apical meristem. The system provides high-resolution spatio-temporal information about hormone distribution during plant growth and development.

Reference: Brunoud G et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature. 482(7383):103-6. DOI: 10.1038/nature10791.