Leaf Trichome Distribution Pattern in Arabidopsis Reveals Gene Expression Variation Associated with Environmental Adaptation

Abstract

Gene expression varies stochastically even in both heterogenous and homogeneous cell populations. This variation is not simply useless noise; rather, it is important for many biological processes. Unicellular organisms or cultured cell lines are useful for analyzing the variation in gene expression between cells; however, owing to technical challenges, the biological relevance of this variation in multicellular organisms such as higher plants remain unclear. Here, we addressed the biological relevance of this variation between cells by examining the genetic basis of trichome distribution patterns in Arabidopsis thaliana. The distribution pattern of a trichome on a leaf is stochastic and can be mathematically represented using Turing’s reaction-diffusion (RD) model. We analyzed simulations based on the RD model and found that the variability in the trichome distribution pattern increased with the increase in stochastic variation in a particular gene expression. Moreover, differences in heat-dependent variability of the trichome distribution pattern between the accessions showed a strong correlation with environmental factors to which each accession was adapted. Taken together, we successfully visualized variations in gene expression by quantifying the variability in the Arabidopsis trichome distribution pattern. Thus, our data provide evidence for the biological importance of variations in gene expression for environmental adaptation.

Using quantitative methods to understand leaf epidermal development

“…The point-pattern approximation that we refer uses the nearest neighbour distance (NND), where each individual trichome/stomate is considered as a point (Clark & Evans, 1954 ). Okamoto et al ( 2020 ) used the point–pattern approximation and a GL3pro:GL3-GFP reporter to monitor gene expression under control and heat treatments. They observed that the trichome patterning gene GL3 is expressed heterogeneously.…”

“…They observed that the trichome patterning gene GL3 is expressed heterogeneously. This finding suggested that the noise resulting from either the abundance of cellular components or environmental conditions may lead to variable patterns in a biological system (Okamoto et al, 2020 ). Therefore, to predict the regulatory pathways underlying the formation of a given pattern, this variability needs to be considered.…”

Cell identity specification in plants: lessons from flower development

“…The use of a dual reporter system in plants helped distinguish between extrinsic and intrinsic noise in Arabidopsis, and revealed that fluctuation in gene expression is coupled in neighboring cells in young leaves ( Araújo et al , 2017 ). The trichome distribution pattern also emerges stochastically, and the variability in the trichome distribution pattern correlated with stochastic cell to cell variation in GL3 expression ( Okamoto et al , 2020 ).…”

Quantitative plant biology—Old and new

“…Turing's article ' e chemical basis of morphogenesis' , inspired by the vision of D' Arcy ompson for a mathematical approach to biology ( ompson, 1917), has been highly influential in the field of biological pattern formation and the so-called Turing patterning is nowadays thought to explain phenomena ranging from asymmetric cell divisions, plant phyllotaxis, patterning of animal skin, bone, scale and feather patterns as well as ecosystem vegetation patterns (Turing, 1952). For plants, this range of processes has recently been further expanded to encompass plant vasculature cell wall patterning, pigment patterning of plant flowers and leaf trichome patterning (Nagashima et al, 2018;Jacobs et al, 2020, Ding et al, 2020, Okamoto et al, 2020).…”