Pavement cells, a living puzzle

Perhaps you enjoy solving jigsaw puzzles. Have you heard about living jigsaw puzzles? Imagine such a puzzle in which the individual pieces were not static but they were continuously changing. So, you will need to assemble it, at the same time as the pieces are growing and changing shape. This might sounds weird. But, actually among plant curiosities, there are some cells that have just this curious morphology resembling a jigsaw-like puzzle shape (left). These cells are called pavement cells and together with stomata coexist in the epidermis of leaves of many species.

They start their development as simple geometrical shapes, such as rectangles or hexagons and over time, they acquire their characteristic jigsaw-like shape, alternating with lobes (protrusions) and indentations. Then, the leaf is exactly like a puzzle which pieces are growing and changing shape over time: an alive puzzle!

How do they get their shape? This is a very intriguing question that continues puzzling plant scientists. On one hand, there is the question of patterning inside a cell, that is, how a cell creates the asymmetries that later on will become a lobe and indentation. Moreover, the decision to make lobes and indentations needs to be coordinated with their neighbours; otherwise, the whole puzzle will fall apart! This actually happen in some plant mutants whose cells fail to develop correct lobes and indentations, and as a consequence, their leaves have some holes in between.

Later, once these regions have been specified, the lobes and indentations develop. Then, the other side of the question on how they get their shapes is how these regions growth differentially to create lobes alternated with indentations. Elsner et al., 2012, studied the shape acquisition of these cells using the replica method. This technique consists of creating impressions of the epidermis during different days, so that the same cells are followed over time. It is like in order to know how the pieces of our hypothetical puzzle are changing shape, we decided to take pictures at different times. Interestingly, they found that the peculiar geometry of these cells could come about because different segments of the future pavement cells growth differentially and because they appear at different times. Then, it would be like if the sides of each of the pieces of our puzzle were growing differentially and were appearing at different times as well. How this is regulated remains a mystery.

Another fact that adds interest to our living-puzzle is that these cells get their jigsaw-like shape in a very stereotyped manner within the leaf. In Arabidopsis thaliana and Nicotiana bentamiana, cells acquire their shape first at the tip of the leaf and over time, cells at the base also show a jigsaw-like shape. So, the pieces of our puzzle are getting their shape first at one extreme and, over time, towards the other extreme. This situation resembles a famous picture by the Dutch painter M.C. Escher, called Metamorphosis (above), where the pieces are more complex towards one extreme. Enigmatic questions around the spatial development of pavement cells are: how is this pattern of cell morphogenesis from the tip to the base controlled? Is it similar in other species? Is this important for overall leaf shape?

Another puzzling question is what are they for. Perhaps the interdigitating pattern helps the leaves to be more resistant to breakage. Perhaps they increase the contact area with neighbours and cells can communicate faster. These possibilities are, of course, just speculations.

A very interesting observation is that these cells have quite different jigsaw-shape depending on the plant species. In fact, the pavement cells of several plants range from simple pieces to a very complex pieces, varying in their degree (or amplitude) of their lobes, the spacing (periodicity) between them, the elongation, etcetera (right). Just as there are jigsaw puzzles with different degree of difficulty!

Although a changing jigsaw puzzle sounds a lot of fun, at the moment it is just an idea. What we have are the pavement cells, our living puzzles, whose shape embrace very interesting questions to continue puzzling us for a while!