Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs

Abstract

Development is remarkably reproducible, producing organs with the same size, shape, and function repeatedly from individual to individual. For example, every flower on the Antirrhinum stalk has the same snapping dragon mouth. This reproducibility has allowed taxonomists to classify plants and animals according to their morphology. Yet these reproducible organs are composed of highly variable cells. For example, neighboring cells grow at different rates in Arabidopsis leaves, sepals, and shoot apical meristems. This cellular variability occurs in normal, wild-type organisms, indicating that cellular heterogeneity (or diversity in a characteristic such as growth rate) is either actively maintained or, at a minimum, not entirely suppressed. In fact, cellular heterogeneity can contribute to producing invariant organs. Here, we focus on how plant organs are reproducibly created during development from these highly variable cells.

Growth dynamics of the Arabidopsis fruit is mediated by cell expansion

“…Interestingly, previous studies described endoreduplication as a morphogenetic factor supporting cell expansion during tomato fruit development (87,114). Thus, at the cellular scale, our results on cell expansion and associated endoreduplication are similar to previous analyses done on sepals and leaves (4,(86)(87)(88)(89)(90), organs evolutionarily and developmentally related to fruit (20)(21)(22)(23)(24)(25)115).…”

“…This results in doubling the nuclear DNA content each time, thereby producing cells with elevated nuclear genome content and higher ploidy status. In plants there exists an intimate correlation between ploidy level and cell size, particularly in epidermal systems (4,(86)(87)(88)(89)(90), and both endoreduplication and cell division coexist as alternative processes during morphogenesis. Their correct combination creates a range of cell sizes critical for leaf and sepal organogenesis (4,88,90,91).…”

A tension-adhesion feedback loop in plant epidermis

“…In other words, a cell would experience different tension level and orientation between a situation where it would be separated from its neighbors (typically, cell shape would be sufficient to prescribe a tensile stress pattern, as in [ Sampathkumar et al, 2014 ]) and a situation where it would still adhere to its neighbors (tensile stress could build up at the outer epidermal wall, to a magnitude higher than cell shape-derived stress, and with a pattern that would depend on tissue shape and differential growth, as in [ Hamant et al, 2008 ; Louveaux et al, 2016 ]). This opens exciting prospect for the future, as cell variability and growth heterogeneity is attracting increasing attention because of its, sometimes counterintuitive, instructive function in development ( Hong et al, 2018 ).…”

Les forces qui maintiennent l’ordre parmi les cellules

“…C'est la loi des grands nombres. Si les cellules d'un organe grandissaient de manière aléatoire et indépendante, la croissance de l'organe, qui intègre la croissance de toutes les cellules, deviendrait de moins en moins variable quand le nombre de cellules augmente [1]. Cependant, un tel scénario ne rend pas vraiment compte de la réalité, car les cellules communiquent entre elles et ne sont donc pas toutes indépendantes les unes des autres.…”