Plants use molecular mechanisms mediated by biomolecular condensates to integrate environmental cues with development

Abstract

This review highlights recent literature on biomolecular condensates in plant development and discusses challenges for fully dissecting their functional roles. Plant developmental biology has been inundated with descriptive examples of biomolecular condensate formation, but it is only recently that mechanistic understanding has been forthcoming. Here, we discuss recent examples of potential roles biomolecular condensates play at different stages of the plant life cycle. We group these examples based on putative molecular functions, including sequestering interacting components, enhancing dwell time, and interacting with cytoplasmic biophysical properties in response to environmental change. We explore how these mechanisms could modulate plant development in response to environmental inputs and discuss challenges and opportunities for further research into deciphering molecular mechanisms to better understand the diverse roles that biomolecular condensates exert on life.

Figure 1.

General molecular mechanisms of biomolecular condensates. A) Sequestration of pathways away from ligands or interacting partners. Biomolecular condensates “hold” proteins or nucleic acids away from their targets or interacting partners not in the condensate. An example of this mechanism is mediated by the processing body and its components (green proteins) that help sequester translationally repressed mRNAs (red line in condensate). During skotomorphogenesis, this phenomenon may be required for the protein DCP5. When these nontranslating mRNAs in processing bodies are released, these mRNAs may undergo translation. B) Increasing dwell time of reaction components. Biomolecular condensates increase the local concentration of proteins (blue RNA-binding proteins) or nucleic acids (red nucleic acid) at a site to enhance a reaction or signaling pathway. An example of this regulation is mediated by FCA condensates that compartmentalize 3′ processing factors and help resolve the R-loop formed by the FLC antisense transcript (COOLAIR) at the FLC locus. C) Condensation mediated changes to cellular biophysical properties. Biomolecular condensate formation or dissolution can change biophysical properties of the cytoplasm, including changes to viscosity and protein diffusion. No published examples of this mechanism are available in plants at this time. The figure shows biomolecular condensate formation resulting in cytoplasmic liquification, based on the current hypothesis for FLOE1 function. The opposite is observed with Tardigrade CAHS, where CAHS condensate formation results in cytoplasmic gelation.

Figure 2.

Summary of biomolecular condensates in plant development. Clockwise from upper right; GERMINATION: FLOE1 is essential for coordinating germination to appropriate environmental conditions. FLOE1 forms condensates upon addition of water to regulate germination in seed cells. DE-ETIOLATION: processing bodies in cotyledons decrease in number in response to light and help young seedlings timely modify morphogenesis. VEGETATIVE GROWTH: ARF19 undergoes nucleo-cytoplasmic shuttling, and biomolecular condensate formation dampens auxin response, regulating root growth. ELF3 forms nuclear localized condensates in hypocotyl cells in response to high temperatures. FLOWERING: multiple biomolecular condensates including FCA and FRIGIDA (FRI) regulate expression of a key repressor to fine-tune the timing of flowering. FCA forms nuclear condensates that are not temperature-responsive, while FRI nuclear condensates become larger and more stable in response to cold.