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1. Syncytia in Fungi

   https://doi.org/10.3390/cells9102255  

   Mela, Alexander P.; Rico-Ramírez, Adriana M.; Glass, N. Louise (October 2020, Cells)

   null (Ed.)

   Filamentous fungi typically grow as interconnected multinucleate syncytia that can be microscopic to many hectares in size. Mechanistic details and rules that govern the formation and function of these multinucleate syncytia are largely unexplored, including details on syncytial morphology and the regulatory controls of cellular and molecular processes. Recent discoveries have revealed various adaptations that enable fungal syncytia to accomplish coordinated behaviors, including cell growth, nuclear division, secretion, communication, and adaptation of the hyphal network for mixing nuclear and cytoplasmic organelles. In this review, we highlight recent studies using advanced technologies to define rules that govern organizing principles of hyphal and colony differentiation, including various aspects of nuclear and mitochondrial cooperation versus competition. We place these findings into context with previous foundational literature and present still unanswered questions on mechanistic aspects, function, and morphological diversity of fungal syncytia across the fungal kingdom. 

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2. Permissiveness and competition within and between Neurospora crassa syncytia

   https://doi.org/10.1093/genetics/iyad112  

   Mela, Alexander_P; Glass, N_Louise; Mitchell, ed., A. (June 2023, GENETICS)

   Abstract A multinucleate syncytium is a common growth form in filamentous fungi. Comprehensive functions of the syncytial state remain unknown, but it likely allows for a wide range of adaptations to enable filamentous fungi to coordinate growth, reproduction, responses to the environment, and to distribute nuclear and cytoplasmic elements across a colony. Indeed, the underlying mechanistic details of how syncytia regulate cellular and molecular processes spatiotemporally across a colony are largely unexplored. Here, we implemented a strategy to analyze the relative fitness of different nuclear populations in syncytia of Neurospora crassa, including nuclei with loss-of-function mutations in essential genes, based on production of multinucleate asexual spores using flow cytometry of pairings between strains with differentially fluorescently tagged nuclear histones. The distribution of homokaryotic and heterokaryotic asexual spores in pairings was assessed between different auxotrophic and morphological mutants, as well as with strains that were defective in somatic cell fusion or were heterokaryon incompatible. Mutant nuclei were compartmentalized into both homokaryotic and heterokaryotic asexual spores, a type of bet hedging for maintenance and evolution of mutational events, despite disadvantages to the syncytium. However, in pairings between strains that were blocked in somatic cell fusion or were heterokaryon incompatible, we observed a “winner-takes-all” phenotype, where asexual spores originating from paired strains were predominantly one genotype. These data indicate that syncytial fungal cells are permissive and tolerate a wide array of nuclear functionality, but that cells/colonies that are unable to cooperate via syncytia formation actively compete for resources. 

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3. Nuclear Entanglement: New Insights Into the Role of Cytoskeleton and Nucleoskeleton in Plant Nuclear Function

   https://doi.org/10.1002/cm.22048  

   Groves, Norman R; Amstutz, Katelyn; Schumacher, Lily A; Meier, Iris (June 2025, Cytoskeleton)

   ABSTRACT Of the three types of cytoskeleton known in animals—actin, microtubules, and intermediate filaments—only actin and microtubules exist in plants. Both play important roles in cellular shaping, organelle movement, organization of the endomembrane system, and cell signaling. An emerging, but often overlooked role of the plant cytoskeleton is its dynamic and mutually influential interaction with the nucleus. Here, we summarize recent advances in understanding the role of the cytoskeleton in plant nuclear movement in different biological contexts, a role for nuclear envelope‐associated proteins in reorganizing the actin and microtubule cytoskeleton, and the molecular nature of the nucleus‐cytoskeleton interface and specific proteins contributing to it. In animals, the nucleoskeleton consists of the nuclear lamina, an intermediate‐filament meshwork underlying the nuclear envelope. Plants have evolved an equivalent of this structure, built by different types of proteins. Here, we highlight recent advances in understanding its filamentous organization, newly discovered protein interactions connecting it to nuclear pores, and exciting new evidence that—just like the animal lamina—the plant lamina is involved in chromatin reorganization and epigenetic changes. Together, these new developments create new opportunities toward a deeper understanding of this important regulatory connection between the cytoskeleton and the cell's largest organelle. 

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4. The SUMO ligase MMS21 profoundly influences maize development through its impact on genome activity and stability

   https://doi.org/10.1371/journal.pgen.1009830  

   Zhang, Junya; Augustine, Robert C.; Suzuki, Masaharu; Feng, Juanjuan; Char, Si Nian; Yang, Bing; McCarty, Donald R.; Vierstra, Richard D. (October 2021, PLOS Genetics)

   Mittelsten Scheid, Ortrun (Ed.)

   The post-translational addition of SUMO plays essential roles in numerous eukaryotic processes including cell division, transcription, chromatin organization, DNA repair, and stress defense through its selective conjugation to numerous targets. One prominent plant SUMO ligase is METHYL METHANESULFONATE-SENSITIVE (MMS)-21/HIGH-PLOIDY (HPY)-2/NON-SMC-ELEMENT (NSE)-2, which has been connected genetically to development and endoreduplication. Here, we describe the potential functions of MMS21 through a collection of UniformMu and CRISPR/Cas9 mutants in maize ( Zea mays ) that display either seed lethality or substantially compromised pollen germination and seed/vegetative development. RNA-seq analyses of leaves, embryos, and endosperm from mms21 plants revealed a substantial dysregulation of the maize transcriptome, including the ectopic expression of seed storage protein mRNAs in leaves and altered accumulation of mRNAs associated with DNA repair and chromatin dynamics. Interaction studies demonstrated that MMS21 associates in the nucleus with the NSE4 and STRUCTURAL MAINTENANCE OF CHROMOSOMES (SMC)-5 components of the chromatin organizer SMC5/6 complex, with in vitro assays confirming that MMS21 will SUMOylate SMC5. Comet assays measuring genome integrity, sensitivity to DNA-damaging agents, and protein versus mRNA abundance comparisons implicated MMS21 in chromatin stability and transcriptional controls on proteome balance. Taken together, we propose that MMS21-directed SUMOylation of the SMC5/6 complex and other targets enables proper gene expression by influencing chromatin structure. 

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5. Phase Separation as a Driver of Stem Cell Organization and Function during Development

   https://doi.org/10.3390/jdb11040045  

   Parra, Amalia S.; Johnston, Christopher A. (December 2023, Journal of Developmental Biology)

   A properly organized subcellular composition is essential to cell function. The canonical organizing principle within eukaryotic cells involves membrane-bound organelles; yet, such structures do not fully explain cellular complexity. Furthermore, discrete non-membrane-bound structures have been known for over a century. Liquid–liquid phase separation (LLPS) has emerged as a ubiquitous mode of cellular organization without the need for formal lipid membranes, with an ever-expanding and diverse list of cellular functions that appear to be regulated by this process. In comparison to traditional organelles, LLPS can occur across wider spatial and temporal scales and involves more distinct protein and RNA complexes. In this review, we discuss the impacts of LLPS on the organization of stem cells and their function during development. Specifically, the roles of LLPS in developmental signaling pathways, chromatin organization, and gene expression will be detailed, as well as its impacts on essential processes of asymmetric cell division. We will also discuss how the dynamic and regulated nature of LLPS may afford stem cells an adaptable mode of organization throughout the developmental time to control cell fate. Finally, we will discuss how aberrant LLPS in these processes may contribute to developmental defects and disease. 

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