Pavement cells, a living puzzle

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Pavement cells in Arabidopsis thaliana.

Pavement cells in Arabidopsis thaliana.

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.

Facade decorated showing an Escher's design from Metamorphosis II.

Facade dec­or­ated show­ing an Escher’s design from Metamorphosis II. Photo Luis García (Zaqarbal) / Wikipedia

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?

Pavement cells in different species

Pavement cells in dif­fer­ent spe­cies. First row shows a leaf impres­sion of Arabidopsis thali­ana (left) and a banana plant (right). In the second row, there is a leaf impres­sion of an orange (left) and another of an avo­cado leaf (right). Finally, on the third row, there is an impres­sion of leaf epi­dermis of a crassu­laceae (right) and a maize leaf (left).

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!

Yara Sánchez-Corrales.

Yara E. Sanchez-Corrales is a plant scientist at the John Innes Centre, where she researches leaf development.

2 Responses

  1. xiaowei says:

    the fant­astic model for cell com­mu­nic­a­tion research

  2. Audrey Berrie says:

    Excuse me, but I think the “third row” of your illus­tra­tion should be “crassulaceae(left) and a maize leaf (right).
    See your quote below:
    “Finally, on the third row, there is an impres­sion of leaf epi­dermis of a crassu­laceae (right) and a maize leaf (left).”

    Its pretty obvi­ous that each spe­cies has genes for a par­tic­u­lar epi­dermal cell shape, whether a dicot or a mono­cot. Try look­ing at the dif­fer­ent stages of growth of the epi­dermal cells, to see how their shape devel­ops, in dif­fer­ent parts of the leaf, from base to apex. Which grows faster, the tip or the base?
    Might the total length of the mature cell out­line (its peri­meter) be an import­ant factor in its ratio to the volume of the cell? like sur­face area of an animal in rela­tion to its volume? just a jig­saw puzzle thought!