Arabidopsis thaliana RHAMNOSE 1 condensate formation drives UDP-rhamnose synthesis.

Rhamnose is an essential component of the plant cell wall and is synthesized from uridine diphosphate (UDP)-glucose by the RHAMNOSE1 (RHM1) enzyme. RHM1 localizes to biomolecular condensates in plants, but their identity, formation, and function remain elusive. Combining live imaging, genetics, and biochemical approaches in Arabidopsis and heterologous systems, we show that RHM1 alone is sufficient to form enzymatically active condensates, which we name rhamnosomes. Rhamnosome formation is required for UDP-rhamnose synthesis and organ development. Overall, our study demonstrates a novel role for biomolecular condensation in metabolism and organismal development, and provides further support for how organisms have harnessed this biophysical process to regulate small molecule metabolism.

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

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.

Arabidopsis CALMODULIN-LIKE 38 Regulates Hypoxia-Induced Autophagy of SUPPRESSOR OF GENE SILENCING 3 Bodies.

During the energy crisis associated with submergence stress, plants restrict mRNA translation and rapidly accumulate stress granules that act as storage hubs for arrested mRNA complexes. One of the proteins associated with hypoxia-induced stress granules in Arabidopsis thaliana is the calcium-sensor protein CALMODULIN-LIKE 38 (CML38). Here, we show that SUPPRESSOR OF GENE SILENCING 3 (SGS3) is a CML38-binding protein, and that SGS3 and CML38 co-localize within hypoxia-induced RNA stress granule-like structures. Hypoxia-induced SGS3 granules are subject to turnover by autophagy, and this requires both CML38 as well as the AAA+-ATPase CELL DIVISION CYCLE 48A (CDC48A). CML38 also interacts directly with CDC48A, and CML38 recruits CDC48A to CML38 granules in planta. Together, this work demonstrates that SGS3 associates with stress granule-like structures during hypoxia stress that are subject to degradation by CML38 and CDC48-dependent autophagy. Further, the work identifies direct regulatory targets for the hypoxia calcium-sensor CML38, and suggest that CML38 association with stress granules and associated regulation of autophagy may be part of the RNA regulatory program during hypoxia stress.

Analysis of the Maize dicer-like1 Mutant, fuzzy tassel, Implicates MicroRNAs in Anther Maturation and Dehiscence.

Sexual reproduction in plants requires development of haploid gametophytes from somatic tissues. Pollen is the male gametophyte and develops within the stamen; defects in the somatic tissues of the stamen and in the male gametophyte itself can result in male sterility. The maize fuzzy tassel (fzt) mutant has a mutation in dicer-like1 (dcl1), which encodes a key enzyme required for microRNA (miRNA) biogenesis. Many miRNAs are reduced in fzt, and fzt mutants exhibit a broad range of developmental defects, including male sterility. To gain further insight into the roles of miRNAs in maize stamen development, we conducted a detailed analysis of the male sterility defects in fzt mutants. Early development was normal in fzt mutant anthers, however fzt anthers arrested in late stages of anther maturation and did not dehisce. A minority of locules in fzt anthers also exhibited anther wall defects. At maturity, very little pollen in fzt anthers was viable or able to germinate. Normal pollen is tricellular at maturity; pollen from fzt anthers included a mixture of unicellular, bicellular, and tricellular pollen. Pollen from normal anthers is loaded with starch before dehiscence, however pollen from fzt anthers failed to accumulate starch. Our results indicate an absolute requirement for miRNAs in the final stages of anther and pollen maturation in maize. Anther wall defects also suggest that miRNAs have key roles earlier in anther development. We discuss candidate miRNAs and pathways that might underlie fzt anther defects, and also note that male sterility in fzt resembles water deficit-induced male sterility, highlighting a possible link between development and stress responses in plants.