The puzzling puzzle

Sometimes we humans tend to prefer style over substance, as you might observe in any clothes shop. On the other hand, plants are down-to-earth living beings that do not appreciate fashion and aesthetics. Their whole structure has been molded through time by evolution so that the shape of their components mirrors their specific functions (something that is less likely in the clothing industry). For example, the different types of cells present on the surface of a leaf look very different. The curved shape of guard cells allows them to form an adjustable pore on the leaf surface, while trichome cells have an elongated shape in order to protect the leaf blade from frost, heat and herbivores. Their shapes make sense. But there is a third type of cell on the leaf surface: pavement cells, which look more or less like this:

A pavement cell from Arabidopsis thaliana. Picture from Ashley Pridgeon.

What mysteries lie within the shape of a pavement cell? Why aren’t they as boring to look at as the square tiles on our pavements? What is the function of those undulating margins? Are they just trying to be more cool and fashionable than the other plant cells?

There are some different theories about the function of pavement cell shape. It is possible that it is needed to increase epidermal integrity by locking the cells together like pieces of a puzzle, or it could help to ease the mechanical stress caused by their huge size, or increase flexibility of the whole leaf. Up until now, our idea of what a pavement cell looks like was based on model species such as Arabidopsis, rice and maize. But Roza Vofely, together with a group of researchers from University of Cambridge, University of Massachusetts and University of California at Los Angeles, recently published a paper in New Phytologist in which they collected leaves from 278 different plants to study the shape of their pavement cells. The plants were selected from a broad variety of taxa, so that they would be representative of vascular plants. Pavement cell shape was then described using the width-to-length ratio (Aspect Ratio), as well as a measure of cell margin undulation (Solidity).

From Figure 2 from Vofely et al., 2018. (b) An illustration of cell solidity (S) calculated as the ratio of cell area to the convex hull area and its results from four representative cells with constant AR; (c) An illustration of AR calculation as the ratio of maximal width to maximal length and its results from four representative cells with constant solidity value.

They found out that apparently being a sinuous leaf pavement cell is not popular in all plant groups. There is an amazing range of pavement cell shapes, and not all of them have highly undulating margins. This variety seems to be linked to evolution, as similar forms often appear in groups of related plants, so that highly wavy cell borders are common in fern cells, while Monocots and Gymnosperms tend to have long and thin cells, with more straight margins. Maize is not in line with its Monocot buddies, because its cells have a highly undulating margin. The same happens with Arabidopsis, which is more wavy than the average Eudicot. So it turned out that the model plants that we have been using up until now to study pavement cell shape are really not that representative, but rather a bit odd, and more studies on other species will be needed.

Figure 1 from Vofely et al., 2018. Epidermal peel images, leaf or leaflet outlines, and segmented cells for a small subset of sampled taxa.

Puzzled about the meaning of this diversity, the researchers tried to see if it is linked to leaf shape. This seems to be the case in Ferns, Gymnosperms and Monocots, in which long and thin cells correspond to long and thin leaves, but in Eudicots they found no link between pavement cell shape and leaf shape.

This dataset did not confirm the hypothesis that pavement cells need undulating margins because of their large size, as there was no correlation between cell area and cell solidity. The authors also did not find any correlation between leaf area and cell margin undulation, which means that bigger leaves do not seem to need more undulating pavement cells to avoid falling apart. Even if these hypotheses do not explain the variability found in vascular plants, they might still be important in specific cases, but as the authors elegantly put it “In the evolutionary optimization of function […] there are likely to be many different solutions to functional problems, and sometimes undulations count and sometimes they do not”. Which, less elegantly, means that it depends.

Even if the function of pavement cell shape is still a mystery, we are now a bit less clueless. We can start from the idea that phylogenesis is likely to be a pretty important factor to consider when comparing the epidermal cell shape of two different species. Second, the fact that phylogenesis influences cell shape gives us some hints to where a common patterning machinery might be present or absent. Therefore “the molecular mechanisms that generate cell shape have both been conserved in some cases and diversified in others”. So, well, I guess it depends.

We do not have the answers to the puzzle yet, but we do have a treasure map to help us find them. And one certainty: pavement cells look quite cool.

Zoe Nemec Venza

Featured image from Ashley Pridgeon

References:

Vőfély, R. V., Gallagher, J., Pisano, G. D., Bartlett, M. and Braybrook, S. A. (2019) Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape. New Phytologist 221: 540-552. doi: 10.1111/nph.15461

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Zoe Nemec Venza

Zoe Nemec Venza is a Sainsbury PhD student at the University of Bristol, in Jill Harrison’s lab, funded by the Gatsby Charitable Foundation. She graduated from her Masters degree at the Universita’ di Pisa, with Francesco Licausi. Her research interests are mostly located in the broad field of plant development. She is particularly fascinated by how cell identity is established and by how developmental pathways changed during evolution. Zoe completed an internship at the New Phytologist Trust during summer 2018.