Diverse organizations of actin and nuclei underpin the evolution of indeterminate growth in Chytridiomycota and Dikarya

Abstract

Indeterminate growth, as in the hyphae of the “Humongous Fungus” of Michigan requires sustained nuclear migration and cell wall remodeling. We compare actin organization and patterns of nuclear positioning among four distantly related, indeterminate species of phylum Chytridiomycota: Cladochytrium replicatum, Physocladia obscura, Nowakowskiella sp., and Polychytrium aggregatum. We combined light microscopy, nuclear staining with DAPI, and actin staining with rhodamine phalloidin to analyze actin distribution and nuclear migration during somatic growth in the four Chytridiomycota species. Actin formed plaques, filaments, cables and perinuclear shells in patterns that varied across the four species. All four species initiated indeterminate growth by extending branching, anucleate rhizomycelium, <1 µm in diameter. Nuclei, some elongated as if migrating, first appear in intercalary segments that widened to diameters >1 µm. After mitosis, an intercalary swelling in C. replicatum became septate and a single, distal nucleus migrated tipwards to a new swelling. In Physocladia obscura, swellings were aseptate and multinucleate, and several nuclei migrated tipwards into a new swelling. Nuclei migrated tipwards from irregularly cylindrical filaments in Nowakowskiella sp., and in Polychytrium aggregatum, from regular, hypha-like filaments. Thus, distantly related lineages of zoosporic fungi deploy ancestral morphogenetic machinery in differing patterns that resulted in convergent, indeterminate growth.

Diversity of ‘simple’ multicellular eukaryotes: 45 independent cases and six types of multicellularity

“…Many early‐branching Fungi, such as Cladochytrium (Chytridiomycota), go through the following series of developmental stages (Dee & Berbee, 2021): germination of a uninucleate spore, expansion of the cell into a extended, continuous form called a rhizomycelium, proliferation of nuclei in localised swellings, migration of nuclei away from swellings, and finally formation of septa that delimit sections of the cell containing typically only a single, rarely two or three, nuclei. This might be seen as a simple form of the process described above as typical for ‘higher fungi’.…”