Chloroplasts in plant cells show active glassy behavior under low-light conditions

Significance

How can immobile plants adapt to ever-changing light conditions? Intracellular chloroplast motion is a fast adaptation mechanism which has been studied for more than 150 y. However, the role of collective motion of these organelles remained elusive. We show that dim-light–adapted chloroplasts exhibit glass-like features. We develop a mathematical model uncovering that chloroplast dynamics are close to a glass transition, which enables chloroplasts to quickly switch to a fluid-like phase for efficient avoidance motion. Besides their biological relevance, the light-dependent dynamical phases of the colloidal-like chloroplasts in Elodea densa constitute an intriguing model system to facilitate and broaden future research perspectives on dense active and living matter.

Abstract

Plants have developed intricate mechanisms to adapt to changing light conditions. Besides phototropism and heliotropism (differential growth toward light and diurnal motion with respect to sunlight, respectively), chloroplast motion acts as a fast mechanism to change the intracellular structure of leaf cells. While chloroplasts move toward the sides of the plant cell to avoid strong light, they accumulate and spread out into a layer on the bottom of the cell at low light to increase the light absorption efficiency. Although the motion of chloroplasts has been studied for over a century, the collective organelle motion leading to light-adapting self-organized structures remains elusive. Here, we study the active motion of chloroplasts under dim-light conditions, leading to an accumulation in a densely packed quasi-2D layer. We observe burst-like rearrangements and show that these dynamics resemble systems close to the glass transition by tracking individual chloroplasts. Furthermore, we provide a minimal mathematical model to uncover relevant system parameters controlling the stability of the dense configuration of chloroplasts. Our study suggests that the meta-stable caging close to the glass transition in the chloroplast monolayer serves a physiological relevance: Chloroplasts remain in a spread-out configuration to increase the light uptake but can easily fluidize when the activity is increased to efficiently rearrange the structure toward an avoidance state. Our research opens questions about the role that dynamical phase transitions could play in self-organized intracellular responses of plant cells toward environmental cues.