Why plants make puzzle cells, and how their shape emerges

Abstract

The shape and function of plant cells are often highly interdependent. The puzzle-shaped cells that appear in the epidermis of many plants are a striking example of a complex cell shape, however their functional benefit has remained elusive. We propose that these intricate forms provide an effective strategy to reduce mechanical stress in the cell wall of the epidermis. When tissue-level growth is isotropic, we hypothesize that lobes emerge at the cellular level to prevent formation of large isodiametric cells that would bulge under the stress produced by turgor pressure. Data from various plant organs and species support the relationship between lobes and growth isotropy, which we test with mutants where growth direction is perturbed. Using simulation models we show that a mechanism actively regulating cellular stress plausibly reproduces the development of epidermal cell shape. Together, our results suggest that mechanical stress is a key driver of cell-shape morphogenesis.

Of puzzles and pavements: a quantitative exploration of leaf epidermal cell shape

“…Leaf form is probably generated by complex growth patterns that we would be unable to detect with our sampling (Tsukaya, ; Kuchen et al ., ; Vlad et al ., ). However, in the Brassicaceae, a connection between growth direction, cell shape, and organ shape has recently been proposed (Sapala et al ., ). In addition, in the flowers of Saltugilia spp.…”

“…A second connection between cell shape and organ form that has been proposed is that the highly undulating cells characteristic of some eudicots are a consequence of cell expansion in all directions in the plane of the leaf lamina (Avery, ; Glover, ; Sapala et al ., ). In this case, one would expect large cells to have low solidity (more undulations); or highly anisotropic leaves to have cells with high solidity values (fewer undulations); or that highly anisotropic cells would have high solidity values (fewer undulations).…”

“…There are three long‐standing hypotheses in the field: (1) undulations may increase cell−cell contact between adjacent cells, allowing for more efficient chemical signalling (Galletti & Ingram, ); (2) undulating margins may increase epidermal integrity (think of a zipper) (Jacques et al ., ); and (3) undulations may help leaves flex (Sotiriou et al ., ). A fourth, more recent, hypothesis proposes that larger, isotropic, cells undulate to alleviate the stress caused by their own growth dynamics (Sapala et al ., ). This cell‐strength hypothesis was put forth on the basis of observations in species closely related to Arabidopsis, and therefore represents a much‐needed foray into nonmodel species (Sapala et al ., ).…”

“…A fourth, more recent, hypothesis proposes that larger, isotropic, cells undulate to alleviate the stress caused by their own growth dynamics (Sapala et al ., ). This cell‐strength hypothesis was put forth on the basis of observations in species closely related to Arabidopsis, and therefore represents a much‐needed foray into nonmodel species (Sapala et al ., ). However, a phylogenetic context is an important consideration for any experimental designs of this type.…”

Auxin promotion of seedling growth via ARF5 is dependent on the brassinosteroid‐regulated transcription factors BES1 and BEH4

“…Dominant iaa6/shy1‐1D and loss‐of‐function pif7 mutants exhibit short hypocotyl phenotypes (Kim, Soh, Kang, Furuya, & Nam, ; Li et al, ) (Figure d). LNG1 encodes a protein localized to cortical microtubules (cMT) (Drevensek et al, ) that was initially identified as a dominant mutant with exaggerated elongation of petioles via unidirectional cell elongation (Lee et al, ; Sapala et al, ).…”