Two MYB Proteins in a Self-Organizing Activator-Inhibitor System Produce Spotted Pigmentation Patterns

Abstract

Many organisms exhibit visually striking spotted or striped pigmentation patterns. Turing's reaction-diffusion model postulates that such periodic pigmentation patterns form when a local autocatalytic feedback loop and a long-range inhibitory feedback loop interact. At its simplest, this network only requires one self-activating activator that also activates a repressor, which inhibits the activator and diffuses to neighboring cells. However, the molecular activators and repressors fully fitting this versatile model remain elusive. Here, we characterize an R2R3-MYB activator and an R3-MYB repressor in monkeyflowers that correspond to Turing's model and explain how periodic anthocyanin spots form. Notably, disrupting this pattern impacts pollinator visitation. Thus, subtle changes in simple reaction-diffusion networks are likely essential contributors to the evolution of the remarkable diversity of periodic pigmentation patterns in flowers. MaintextPeriodic pigmentation patterns like the stripes of zebras, the spiral pigmentation of seashells, and the petal spots of many flowers have fascinated biologists and mathematicians for centuries. One proposed developmental explanation for how such periodic patterns form is Turing's reactiondiffusion model (1), in which dynamic and autonomous patterns are generated simply owing to the interaction of an activator and a repressor. The activator self-activates and activates the repressor, which then diffuses and inhibits the activator along the diffusion path. This mechanism amplifies initial cellular fluctuations into tissue-level spatial patterns (2-4). Computer simulations suggest that by tinkering with the diffusion constants and the kinetics of the activator-repressor interaction, this simple circuit can recapitulate the immense diversity of pigmentation patterns observed in nature (3). However, the molecular identities and dynamics of actual activator-repressor pairs that fulfill the classic Turing model for pigment patterning have remained elusive. Anthocyanin spots in flower petals provide an excellent empirical system to reveal the molecular basis for the formation and evolution of periodic pigmentation patterns. These patterns, which are highly diverse in the angiosperms even among different varieties of the same species (5,6), are known to serve as critical cues in plant-pollinator interactions (7-9); and the genetic network controlling anthocyanin pigment production is otherwise well described (10, 11).

Dynamic Changes of the Anthocyanin Biosynthesis Mechanism During the Development of Heading Chinese Cabbage (Brassica rapa L.) and Arabidopsis Under the Control of BrMYB2

“…A notable example is AtMYBL2, occurs in seeds or vegetative tissues, inhibits the upregulation of AtTT8 , AtPAP1 , and AtPAP2 ; moreover, AtTT8 is able to positively upregulate the AtMYBL2 gene ( Dubos et al, 2010 ; Matsui et al, 2010 ). Another classic case of interaction between negative repressors and positive regulators with the spatial patterning considered that these interactions happen in a local, autocatalytic feedback loop and a long-range inhibitory feedback loop: an R2R3-MYB activator and an R3-MYB repressor constitute a double “activator and suppressor” components reaction-diffusion system in monkey flower, and this system dynamically interacts with MlANbHLH1 to regulate the formation of dispersed anthocyanin spots in its petals ( Ding et al, 2020 ). In this process, activators promote color generation and repressors restrain color formation, and they meet and react, and thereby producing pigments diffusion ( Ding et al, 2020 ).…”

Effective range of non-cell autonomous activator and inhibitor peptides specifying plant stomatal patterning

“…Analogously, different features of a stomatal correlation function may correspond to specific genes or mechanisms in stomatal patterning. Our SPACE pipeline is not limited to the context of stomatal development; it could be utilized for quantitative analyses of phenotypic characteristics and mathematical constraint, and broadly to the study of spatial patterns of individual cell fate, such as floral spot patterning ( Ding et al, 2020 ).…”

Macroevolution of Flower Color Patterning: Biased Transition Rates and Correlated Evolution with Flower Size

“…Biased evolutionary transitions toward uniform coloration may have developmental or ecological underpinnings. First, evolving pattern often requires precise regulation of the domain of expression of pigments (e.g., via alterations to MYB transcription factor expression or their binding sites; Mol et al., 1998 ; Quattrocchio et al., 2006 ; Jiang and Rausher, 2018 ; Ding et al., 2020 ). Thus, expression of uniform petal coloration may require fewer modifications in fewer structural or regulatory elements of pigmentation pathways compared to the precise spatial regulation of pigment production required for the evolution of color patterning.…”