A proxitome-RNA-capture approach reveals that processing bodies repress coregulated hub genes.

Cellular condensates are usually ribonucleoprotein assemblies with liquid- or solid-like properties. Because these subcellular structures lack a delineating membrane, determining their compositions is difficult. Here we describe a proximity-biotinylation approach for capturing the RNAs of the condensates known as processing bodies (PBs) in Arabidopsis (Arabidopsis thaliana). By combining this approach with RNA detection, in silico, and high-resolution imaging approaches, we studied PBs under normal conditions and heat stress. PBs showed a much more dynamic RNA composition than the total transcriptome. RNAs involved in cell wall development and regeneration, plant hormonal signaling, secondary metabolism/defense, and RNA metabolism were enriched in PBs. RNA-binding proteins and the liquidity of PBs modulated RNA recruitment, while RNAs were frequently recruited together with their encoded proteins. In PBs, RNAs follow distinct fates: in small liquid-like PBs, RNAs get degraded while in more solid-like larger ones, they are stored. PB properties can be regulated by the actin-polymerizing SCAR (suppressor of the cyclic AMP)-WAVE (WASP family verprolin homologous) complex. SCAR/WAVE modulates the shuttling of RNAs between PBs and the translational machinery, thereby adjusting ethylene signaling. In summary, we provide an approach to identify RNAs in condensates that allowed us to reveal a mechanism for regulating RNA fate.

Plant condensates: no longer membrane-less?

Cellular condensation is a reinvigorated area of study in biology, with scientific discussions focusing mainly on the forces that drive condensate formation, properties, and functions. Usually, condensates are called 'membrane-less' to highlight the absence of a surrounding membrane and the lack of associated contacts. In this opinion article we take a different direction, focusing on condensates that may be interfacing with membranes and their possible functions. We also highlight changes in condensate material properties brought about by condensate-membrane interactions, proposing how condensates-membrane interfaces could potentially affect interorganellar communication, development, and growth, but also adaptation in an evolutionary context. We would thus like to stimulate research in this area, which is much less understood in plants compared with the animal field.